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Darwin: From the Origin of Species to the Descent of Man

This entry offers a broad historical review of the origin and development of Darwin’s theory of evolution by natural selection through the initial Darwinian phase of the “Darwinian Revolution” up to the publication of the Descent of Man in 1871. The development of evolutionary ideas before Darwin’s work has been treated in the separate entry evolutionary thought before Darwin . Several additional aspects of Darwin’s theory of evolution and his biographical development are dealt with in other entries in this encyclopedia (see the entries on Darwinism ; species ; natural selection ; creationism ). The remainder of this entry will focus on aspects of Darwin’s theory not developed in the other entries. It will also maintain a historical and textual approach. Other entries in this encyclopedia cited at the end of the article and the bibliography should be consulted for discussions beyond this point. The issues will be examined under the following headings:

1.1 Historiographical Issues

1.2 darwin’s early reflections, 2.1. the concept of natural selection.

• 2.2. The Argument of the Published Origin

3.1 The Popular Reception of Darwin’s Theory

3.2 the professional reception of darwin’s theory, 4.1 the genesis of darwin’s descent, 4.2 darwin on mental powers, 4.3 the ethical theory of the descent of man.

• 4.4 The Reception of the Descent

5. Summary and Conclusion

Other internet resources, related entries, acknowledgments, 1. the origins of darwin’s theory.

Charles Darwin’s version of transformism has been the subject of massive historical and philosophical scholarship almost unparalleled in any other area of the history of science. This includes the continued flow of monographic studies and collections of articles on particular aspects of Darwin’s theory (Prestes 2023; R. J. Richards and Ruse 2016; Ruse 2013a, 2009a,b,c; Ruse and Richards 2009; Hodge and Radick 2009; Hösle and Illies 2005; Gayon 1998; Bowler 1996; Depew and Weber 1995; Kohn 1985a). The continuous production of popular and professional biographical studies on Darwin provides ever new insights (Ruse et al. 2013a; Johnson 2012; Desmond and Moore 1991, 2009; Browne 1995, 2002; Bowlby 1990; Bowler 1990). In addition, major editing projects on Darwin’s manuscripts and the completion of the Correspondence , project through the entirety of Darwin’s life, continue to reveal details and new insights into the issues surrounding Darwin’s own thought (Keynes [ed.] 2000; Burkhardt et al. [eds] 1985–2023; Barrett et al. [eds.] 1987). The Cambridge Darwin Online website (see Other Internet Resources ) serves as an international clearinghouse for this worldwide Darwinian scholarship, functioning as a repository for electronic versions of all the original works of Darwin, including manuscripts and related secondary materials. It also supplies a continuously updated guide to current literature.

A long tradition of scholarship has interpreted Darwin’s theory to have originated from a framework defined by endemic British natural history, a British tradition of natural theology defined particularly by William Paley (1743–1805), the methodological precepts of John Herschel (1792–1871), developed in his A Preliminary Discourse on the Study of Natural Philosophy (1830 [1987]), and the geological theories of Charles Lyell (1797–1875). His conversion to the uniformitarian geology of Charles Lyell and to Lyell’s advocacy of “deep” geological time during the voyage of the HMS Beagle (December 1831–October 1836), has been seen as fundamental in his formation (Norman 2013; Herbert 2005; Hodge 1983). Complementing this predominantly anglophone historiography has been the social-constructivist analyses emphasizing the origins of Darwin’s theories in British Political Economy (Young 1985: chps. 2, 4, 5). It has also been argued that a primary generating source of Darwin’s inquiries was his involvement with the British anti-slavery movement, a concern reaching back to his revulsion against slavery developed during the Beagle years (Desmond and Moore 2009).

A body of recent historiography, on the other hand, drawing on the wealth of manuscripts and correspondence that have become available since the 1960s (online at Darwin online “Papers and Manuscripts” section, see Other Internet Resources ) has de-emphasized some of the novelty of Darwin’s views and questions have been raised regarding the validity of the standard biographical picture of the early Darwin. These materials have drawn attention to previously ignored aspects of Darwin’s biography. In particular, the importance of his Edinburgh period from 1825–27, largely discounted in importance by Darwin himself in his late Autobiography , has been seen as critical for his subsequent development (Desmond and Moore 1991; Hodge 1985). As a young medical student at the University of Edinburgh (1825–27), Darwin developed a close relationship with the comparative anatomist Robert Edmond Grant (1793–1874) through the student Plinian Society, and in many respects Grant served as Darwin’s first mentor in science in the pre- Beagle years (Desmond and Moore 1991, chp. 1). Through Grant he was exposed to the transformist theories of Jean Baptiste Lamarck and the Cuvier-Geoffroy debate centered on the Paris Muséum nationale d’histoire naturelle (see entry on evolutionary thought before Darwin , Section 4).

These differing interpretive frameworks make investigations into the origins of Darwin’s theory an active area of historical research. The following section will explore these origins.

In its historical origins, Darwin’s theory was different in kind from its main predecessors in important ways (Ruse 2013b; Sloan 2009a; see also the entry on evolutionary thought before Darwin ). Viewed against a longer historical scenario, Darwin’s theory does not deal with cosmology or the origins of the world and life through naturalistic means, and therefore was more restricted in its theoretical scope than its main predecessors influenced by the reflections of Georges Louis LeClerc de Buffon (1707–1788), Johann Herder (1744–1803, and German Naturphilosophen inspired by Friederich Schelling (1775–1854) . This restriction also distinguished Darwin’s work from the grand evolutionary cosmology put forth anonymously in 1844 by the Scottish publisher Robert Chambers (1802–1871) in his immensely popular Vestiges of the Natural History of Creation , a work which in many respects prepared Victorian society in England, and pre-Civil War America for the acceptance of a general evolutionary theory in some form (Secord 2000; MacPherson 2015). It also distinguishes Darwin’s formulations from the theories of his contemporary Herbert Spencer (1820–1903).

Darwin’s theory first took written form in reflections in a series of notebooks begun during the latter part of the Beagle voyage and continued after the return of the Beagle to England in October of 1836 (Barrett et al., 1987). His reflections on the possibility of species change are first entered in March of 1837 (“Red Notebook”) and are developed in the other notebooks (B–E) through July of 1839 (Barrett et al. 1987; Hodge 2013a, 2009). Beginning with the reflections of the third or “D” “transmutation” Notebook, composed between July and October of 1838, Darwin first worked out the rudiments of what was to become his theory of natural selection. In the parallel “M” and “N” Notebooks, dating between July of 1838 and July of 1839, and in a loose collection called “Old and Useless Notes”, dating from approximately 1838–40, he also developed many of his main ideas on human evolution that would only be made public in the Descent of Man of 1871 (below, Section 4).

To summarize a complex issue, these Notebook reflections show Darwin proceeding through a series of stages in which he first formulated a general theory of the transformation of species by historical descent from common ancestors. He then attempted to work out a causal theory of life that would explain the tendency of life to complexify and diversify (Hodge 2013a, 2009, 1985; Sloan 1986). This causal inquiry into the underlying nature of life, and with it the search for an explanation of life’s innate tendency to develop and complexify, was then replaced by a dramatic shift in focus away from these inquiries. This concern with a causal theory of life was then replaced by a new emphasis on external forces controlling population, a thesis developed from his reading of Thomas Malthus’s (1766–1834) Essay on the Principle of Population (6th ed. 1826). For Malthus, human populaton was assumed to expand geometrically, while food supply expanded arithmetically, leading to an inevitable struggle of humans for existence. The impact of Darwin’s reading of this edition of the Essay in August of 1838, was dramatic. It enabled him to theorize the existence of a constantly-acting dynamic force behind the transformation of species.

Darwin’s innovation was to universalize the Malthusian “principle of population” to apply to all of nature. In so doing, Darwin effectively introduced what may be termed an “inertial” principle into his theory, although such language is never used in his text. Newton’s first law of motion, set forth in his Mathematical Principles of Natural Philosophy (1st ed. 1687), established his physical system upon the tendency of all material bodies to persist eternally either at rest or in uniform motion in a straight line, requiring a causal force explanation for any deviations from this initial state. But Newton did not seek a deeper metaphysical explanation of this inertial state. Law One is simply an “axiom” in Newton’s Principia. Similarly, the principle of population supplied Darwin with the assumption of an initial dynamic state of affairs that was not itself explained within the theory—there is no attempt to account causally for this tendency of living beings universally to reproduce geometrically. Similarly for Darwin, the principle of population functions axiomatically, defining a set of initial conditions from which any deviance from this ideal state demands explanation.

This theoretical shift enabled Darwin to bracket his earlier efforts to develop a causal theory of life, and focus instead on the means by which the dynamic force of population was controlled. This allowed him to emphasize how controls on population worked in company with the phenomenon of slight individual variation between members of the same species, in company with changing conditions of life, to produce a gradual change of form and function over time, leading to new varieties and eventually to new species. This opened up the framework for Darwin’s most important innovation, the concept of “natural” selection.

2. Darwinian Evolution

The primary distinguishing feature of Darwin’s theory that separates it from previous explanations of species change centers on the causal explanation he offered for how this process occurred. Prior theories, such as the theory of Jean-Baptiste Lamarck (see entry on evolutionary thought before Darwin ), relied on the inherent dynamic properties of matter. The change of species was not, in these pre-Darwinian efforts, explained through an adaptive process. Darwin’s emphasis after the composition of Notebook D on the factors controlling population increase, rather than on a dynamic theory of life grounded in vital forces, accounts for many of the differences between Darwin’s theory and those of his predecessors and contemporaries.

These differences can be summarized in the concept of natural selection as the central theoretical component of Darwinian theory. However, the exact meaning of this concept, and the varying ways he stated the principle in the Origin over its six editions (1859–1872), has given rise to multiple interpretations of the meaning of this principle in the history of Darwinism, and the different understandings of his meaning deeply affected different national and cultural receptions of his theory (see below, Section 3 .1).

One way to see the complexity of Darwin’s own thinking on these issues is to follow the textual development of this concept from the close of the Notebook period (1839) to the publication of the Origin of Species in 1859. This period of approximately twenty years involved Darwin in a series of reflections that form successive strata in the final version of his theory of the evolution of species. Understanding the historical sequence of these developments also has significance for subsequent controversies over this concept and the different readings of the Origin as it went through its successive revisions. This historical development of the concept also has some bearing on assessing Darwin’s relevance for more general philosophical questions, such as those surrounding the relevance of his theory for such issues as the concept of a more general teleology of nature.

The earliest set of themes in the manuscript elaboration of natural selection theory can be characterized as those developed through a particular form of the argument from analogy. This took the form of a strong “proportional” form of the analogical argument that equated the relation of human selection to the development of domestic breeds as an argument of the basic form: human selection is to domestic variety formation as natural selection is to natural species formation (White, Hodge and Radick 2021, chps. 4–5). This makes a direct analogy between the actions of nature with those of humans in the process of selection. The specific expressions, and changes, in this analogy are important to follow closely. As this was expressed in the first coherent draft of the theory, a 39-page pencil manuscript written in 1842, this discussion analogized the concept of selection of forms by human agency in the creation of the varieties of domestic animals and plants, to the active selection in the natural world by an almost conscious agency, a “being infinitely more sagacious than man (not an omniscient creator)” who acts over “thousands and thousands of years” on “all the variations which tended towards certain ends” (Darwin 1842 in Glick and Kohn 1996, 91). This agency selects out those features most beneficial to organisms in relation to conditions of life, analogous in its action to the selection by man on domestic forms in the production of different breeds. Interwoven with these references to an almost Platonic demiurge are appeals to the selecting power of an active “Nature”:

Nature’s variation far less, but such selection far more rigid and scrutinizing […] Nature lets <<an>> animal live, till on actual proof it is found less able to do the required work to serve the desired end, man judges solely by his eye, and knows not whether nerves, muscles, arteries, are developed in proportion to the change of external form. (Ibid., 93)

These themes were continued in the 230 page draft of his theory of 1844. Again he referred to the selective action of a wise “Being with penetration sufficient to perceive differences in the outer and innermost organization quite imperceptible to man, and with forethought extending over future centuries to watch with unerring care and select for any object the offspring of an organism produced” (Darwin 1844 in ibid., 101). This selection was made with greater foresight and wisdom than human selection. As he envisions the working of this causal agency,

In accordance with the plan by which this universe seems governed by the Creator, let us consider whether there exist any secondary means in the economy of nature by which the process of selection could go on adapting, nicely and wonderfully, organisms, if in ever so small a degree plastic, to diverse ends. I believe such secondary means do exist. (Ibid., 103).

Darwin returned to these issues in 1856, following a twelve-year period in which he published his Geological Observations on the Volcanic Islands (1844), the second edition of his Journal of Researches (1845), Geological Observations on South America (1846), the four volumes on fossil and living barnacles ( Cirripedia ) (1851, 54, 55), and Geological Observations on Coral Reefs (1851). In addition, he published several smaller papers on invertebrate zoology and on geology, and reported on his experiments on the resistance of seeds to salt water, a topic that would be of importance in his explanation of the population of remote islands.

These intervening inquiries positioned Darwin to deal with the question of species permanence against an extensive empirical background. The initial major synthesis of these investigations takes place in his long manuscript, or “Big Species Book”, commenced in 1856, known in current scholarship as the “Natural Selection” manuscript. This formed the immediate background text behind the published Origin . Although incomplete, the “Natural Selection” manuscript provides insights into many critical issues in Darwin’s thinking. It was also prepared with an eye to the scholarly community. This distinguishes its content and presentation from that of the subsequent “abstract” which became the published Origin of Species . “Natural Selection” contained tables of data, references to scholarly literature, and other apparatus expected of a non-popular work, none of which appeared in the published Origin .

The “Natural Selection” manuscript also contained some new theoretical developments of relevance to the concept of natural selection that are not found in earlier manuscripts. Scholars have noted the introduction in this manuscript of the “principle of divergence”, the thesis that organisms under the action of natural selection will tend to radiate and diversify within their “conditions of life”—the contemporary name for the complex of environmental and species-interaction relationships (Kohn 1985b, 2009). Although the concept of group divergence under the action of natural selection might be seen as an implication of Darwin’s theory from his earliest formulations of the 1830s, nonetheless Darwin’s explicit definition of this as a “principle”, and its discussion in a long late insertion in the “Natural Selection” manuscript, suggests its importance for Darwin’s mature theory. The principle of divergence was now seen by Darwin to form an important link between natural variation and the conditions of existence under the action of the driving force of population increase.

Still evident in the “Natural Selection” manuscript is Darwin’s implicit appeal to some kind of teleological ordering of the process. The action of the masculine-gendered “wise being” of the earlier manuscripts, however, has now been given over entirely to the action of a selective “Nature”, now referred to in the traditional feminine gender. This Nature,

…cares not for mere external appearance; she may be said to scrutinise with a severe eye, every nerve, vessel & muscle; every habit, instinct, shade of constitution,—the whole machinery of the organisation. There will be here no caprice, no favouring: the good will be preserved & the bad rigidly destroyed.… Can we wonder then, that nature’s productions bear the stamp of a far higher perfection than man’s product by artificial selection. With nature the most gradual, steady, unerring, deep-sighted selection,—perfect adaption [sic] to the conditions of existence.… (Darwin 1856–58 [1974: 224–225])

The language of this passage, directly underlying statements about the action of “natural selection” in the first edition of the published Origin , indicates the complexity in the exegesis of Darwin’s meaning of “natural selection” when viewed in light of its historical genesis (Ospovat 1981). The parallels between art and nature, the intentionality implied in the term “selection”, the notion of “perfect” adaptation, and the substantive conception of “nature” as an agency working toward certain ends, all render Darwin’s views on teleological purpose more complex than they are typically interpreted from the standpoint of contemporary Neo-selectionist theory (Lennox 1993, 2013). As will be discussed below, the changes Darwin subsequently made in his formulations of this concept over the history of the Origin have led to different conceptions of what he meant by this principle.

The hurried preparation and publication of the Origin between the summer of 1858 and November of 1859 was prompted by the receipt on June 18 of 1858 of a letter and manuscript from Alfred Russel Wallace (1823–1913) that outlined his remarkably similar views on the possibility of continuous species change under the action of a selection upon natural variation (Wallace 1858 in Glick and Kohn 1996, 337–45). This event had important implications for the subsequent form of Darwin’s published argument. Rapidly condensing the detailed arguments of the unfinished “Natural Selection” manuscript into shorter chapters, Darwin also universalized several claims that he had only developed with reference to specific groups of organisms, or which he had applied only to more limited situations in the manuscript. This resulted in a presentation of his theory at the level of broad generalization. The absence of tables of data, detailed footnotes, and references to the secondary literature in the published version also resulted in predictable criticisms which will be discussed below in Section 3.2 .

2.2. The Central Argument of the Published Origin

The Origin of Species by Means of Natural Selection, or the Preservaton of Favoured Races in the Struggle for Life was issued in London by the publishing house of John Murray on November 24, 1859 (Darwin 1859 [1964]). The structure of the argument presented in the published Origin has been the topic of considerable literature and can only be summarized here. Although Darwin himself described his book as “one long argument”, the exact nature of this argument is not immediately transparent, and alternative interpretations have been made of his reasoning and rhetorical strategies in formulating his evolutionary theory. (Prestes 2023; White, Hodge and Radick 2021; Hodge 2013b, 1977; Hoquet 2013; Hull 2009; Waters 2009; Depew 2009; Ruse 2009; Lennox 2005; Hodge 1983b).

The scholarly reconstruction of Darwin’s methodology employed in the Origin has taken two primary forms. One approach has been to reconstruct it from the standpoint of currently accepted models of scientific explanation, sometimes presenting it as a formal deductive model (Sober 1984). Another, more historical, approach interprets his methodology in the context of accepted canons of scientific explanation found in Victorian discussions of the period (see the entry on Darwinism ; Prestes 2023; White, Hodge and Radick 2021; Hodge 2013b, 1983b, 1977; Hoquet 2013; Hull 2009; Waters 2009; Depew 2009; Lennox 2005). The degree to which Darwin did in fact draw from the available methodological discussions of his contemporaries—John Herschel, William Whewell, John Stuart Mill—is not fully clear from available documentary sources. The claim most readily documented, and defended particularly by White, Hodge and Radick (2021) and M. J. S. Hodge (1977, 1983a), has emphasized the importance of John Herschel’s A Preliminary Discourse on the Study of Natural Philosophy (1830 [1987]), which Darwin read as a young student at Cambridge prior to his departure on the HMS Beagle in December of 1831.

In Herschel’s text he would have encountered the claim that science seeks to determine “true causes”— vera causae— of phenomena through the satisfaction of explicit criteria of adequacy (Herschel, 1830 [1987], chp. 6). This concept Newton had specified in the Principia as the third of his “Rules of Reasoning in Philosophy” (see the entry on Newton’s philosophy , Section 4). Elucidation of such causes was to be the goal of scientific explanation. Vera causae , in Herschel’s formulation, were those necessary to produce the given effects; they were truly active in producing the effects; and they adequately explained these effects.

The other plausible methodological source for Darwin’s mature reasoning was the work of his older contemporary and former Cambridge mentor, the Rev. William Whewell (1794–1866), whose three-volume History of the Inductive Sciences (Whewell 1837) Darwin read with care after his return from his round-the-world voyage (Ruse 2013c, 1975). On this reading, a plausible argument has been made that the actual structure of Darwin’s text is more closely similar to a “Whewellian” model of argument. In Whewell’s accounts of his philosophy of scientific methodology (Whewell 1840, 1858), the emphasis of scientific inquiry is, as Herschel had also argued, to be placed on the discovery of “true causes”. But evidence for the determination of a vera causa was to be demonstrated by the ability of disparate phenomena to be drawn together under a single unifying “Conception of the Mind”, exemplified for Whewell by Newton’s universal law of gravitation. This “Consilience of Inductions”, as Whewell termed this process of theoretical unification under a few simple concepts, was achieved only by true scientific theories employing true causes (Whewell 1840: xxxix). It has therefore been argued that Darwin’s theory fundamentally produces this kind of consilience argument, and that his methodology is more properly aligned with that of Whewell.

A third account, related to the Whewellian reading, is that of David Depew. Building on Darwin’s claim that he was addressing “the general naturalist public,” Darwin is seen as developing what Depew has designated as “situated argumentation”, similar to the views developed by contemporary Oxford logician and rhetorical theorist Richard Whately (1787–1863) (Depew 2009). This rhetorical strategy proceeds by drawing the reader into Darwin’s world by personal narration as it presents a series of limited issues for acceptance in the first three chapters, none of which required of the reader a considerable leap of theoretical assent, and most of which, such as natural variation and Malthusian population increase, had already been recognized in some form in the literature of the period.

As Darwin presented his arguments to the public, he opens with a pair of chapters that draw upon the strong analogy developed in the manuscripts between the action of human art in the production of domestic forms, and the actions of selection “by nature.” The resultant forms are presumed to have arisen through the action of human selection on the slight variations existing between individuals within the same species. The interpretation of this process as implying directional, and even intentional, selection by a providential “Nature” that we have seen in the manuscripts was, however, downplayed in the published work through the importance given by Darwin to the role of “unconscious” selection, a concept not encountered in the Natural Selection manuscript. Such selection denotes the practice even carried out by aboriginal peoples who simply seek to maintain the integrity and survival of a breed or species by preserving the “best” forms.

The domestic breeding analogy is, however, more than a decorative rhetorical strategy. It repeatedly functions for Darwin as the principal empirical example to which he could appeal at several places in the text as a means of visualizing the working of natural selection in nature, and this appeal remains intact through the six editions of the Origin.

From this model of human selection working on small individual natural variations to produce the domestic forms, Darwin then developed in the second chapter the implications of “natural” variation, delaying discussion of the concept of natural selection until Chapter IV. The focus of the second chapter introduces another important issue. Here he extends the discussion of variation developed in Chapter I into a critical analysis of the common understanding of classification as grounded on the definition of species and higher groups based on the possession of essential defining properties. It is in this chapter that Darwin most explicitly develops his own position on the nature of organic species in relation to his theory of descent. It is also in this chapter that he sets forth the ingredients for his attack on one meaning of species “essentialism”.

Darwin’s analysis of the “species question” involves a complex argument that has many implications for how his work was read by his contemporaries and successors, and its interpretation has generated a considerable literature (see the entries on species and Darwinism ; Mallet 2013; R. A. Richards 2010; Wilkins 2009; Stamos 2007; Sloan 2009b, 2013; Beatty 1985).

Prior tradition had been heavily affected by eighteenth-century French naturalist Buffon’s novel conception of organic species in which he made a sharp distinction between “natural” species, defined primarily by fertile interbreeding, and “artificial” species and varieties defined by morphological traits and measurements upon these (see the entry on evolutionary thought before Darwin , Section 3.3). This distinction was utilized selectively by Darwin in an unusual blending of two traditions of discussion that are conflated in creative ways in Darwin’s analysis.

Particularly as the conception of species had been discussed by German natural historians of the early nineteenth-century affected by distinctions introduced by philosopher Immanuel Kant (1724–1804), “Buffonian” species were defined by the material unity of common descent and reproductive continuity. This distinguished them by their historical and material character from the taxonomic species of the “Linnean” tradition of natural history. This distinction between “natural” and “logical” species had maintained a distinction between problems presented in the practical classification of preserved specimens, distinguished by external characters, and those relating to the unity of natural species, which was grounded upon reproductive unity and the sterility criterion (Sloan 2009b).

Remarkable in Darwin’s argument is the way in which he draws selectively in his readings from these two preexistent traditions to undermine the different grounds of species “realism” assumed within both of these traditions of discourse. One framework—what can be considered in his immediate context the “Linnean” tradition—regarded species in the sense of universals of logic or class concepts, whose “reality” was often grounded on the concept of divine creation. The alternative “Buffonian” tradition viewed species more naturalistically as material lineages of descent whose continuity was determined by some kind of immanent principle, such as the possession of a conserving “internal mold” or specifying vital force (see evolutionary thought before Darwin 3.3). The result in Darwin’s hands is a complex terminological interweaving of concepts of Variety, Race, Sub-species, Tribe, and Family that can be shown to be a fusion of different traditions of discussion in the literature of the period. This creative conflation also led to many confusions among his contemporaries about how Darwin actually did conceive of species and species change in time.

Darwin addresses the species question by raising the problems caused by natural variation in the practical discrimination of taxa at the species and varietal levels, an issue with which he had become closely familiar in his taxonomic revision of the Sub-class Cirripedia (barnacles) in his eight-year study on this group. Although the difficulty of taxonomic distinctions at this level was a well-recognized problem in the literature of the time, Darwin subtly transforms this practical problem into a metaphysical ambiguity—the fuzziness of formal taxonomic distinctions created by variation in preserved specimens is seen to imply a similar ambiguity of “natural” species boundaries.

We follow this in reading how natural variation is employed by Darwin in Chapter Two of the Origin to break down the distinction between species and varieties as these concepts were commonly employed in the practical taxonomic literature. The arbitrariness apparent in making distinctions, particularly in plants and invertebrates, meant that such species were only what “naturalists having sound judgment and wide experience” defined them to be ( Origin 1859 [1964], 47). These arguments form the basis for claims by his contemporaries that Darwin was a species “nominalist”, who defined species only as conventional and convenient divisions of a continuum of individuals.

But this feature of Darwin’s discussion of species captures only in part the complexity of his argument. Drawing also on the tradition of species realism developed within the “Buffonian” tradition, Darwin also affirmed that species and varieties are defined by common descent and material relations of interbreeding. Darwin then employed the ambiguity of the distinction between species and varieties created by individual variation in practical taxonomy to undermine the ontological fixity of “natural” species. Varieties are not simply the formal taxonomic subdivisions of a natural species as conceived in the Linnaean tradition. They are, as he terms them, “incipient” species (ibid., 52). This subtly transformed the issue of local variation and adaptation to circumstances into a primary ingredient for historical evolutionary change. The full implications to be drawn from this argument were, however, only to be revealed in Chapter Four of the text.

Before assembling the ingredients of these first two chapters, Darwin then introduced in Chapter Three the concept of a “struggle for existence”. This concept is introduced in a “large and metaphorical sense” that included different levels of organic interactions, from direct struggle for food and space to the struggle for life of a plant in a desert. Although described as an application of Thomas Malthus’s parameter of geometrical increase of population in relation to the arithmetical increase of food supply, Darwin’s use of this concept in fact reinterprets Malthus’s principle, which was formulated only with reference to human population in relation to food supply. It now becomes a general principle governing all of organic life. Thus all organisms, including those comprising food for others, would be governed by the tendency to geometrical increase.

Through this universalization, the controls on population become only in the extreme case grounded directly on the traditional Malthusian limitations of food and space. Normal controls are instead exerted through a complex network of relationships of species acting one on another in predator-prey, parasite-host, and food-web relations. This profound revision of Malthus’s arguments rendered Darwin’s theory deeply “ecological” as this term would later be employed. We can cite two thought experiments employed by Darwin himself as illustrations (ibid., 72–74). The first concerns the explanation of the abundance of red clover in England. This Darwin sees as dependent on the numbers of pollinating humble bees, which are controlled in turn by the number of mice, and these are controlled by the number of cats, making cats the remote determinants of clover abundance. The second instance concerns the explanation of the abundance of Scotch Fir. In this example, the number of fir trees is limited indirectly by the number of cattle.

With the ingredients of the first three chapters in place, Darwin was positioned to assemble these together in his grand synthesis of Chapter Four on “natural” selection. In this long discussion, Darwin develops the main exposition of his central theoretical concept. For his contemporaries and for the subsequent tradition, however, the meaning of Darwin’s concept of “natural” selection was not unambiguously evident for reasons we have outlined above, and these unclarities were to be the source of several persistent lines of disagreement and controversy.

The complexities in Darwin’s presentation of his central principle over the six editions of the published Origin served historically to generate several different readings of his text. In the initial introduction of the principle of natural selection in the first edition of Darwin’s text, it is characterized as “preservation of favourable variations and the rejection of injurious variations” (ibid., 81). When Darwin elaborated on this concept in Chapter Four of the first edition, he continued to describe natural selection in language suggesting that it involved intentional selection, continuing the strong art-nature analogy found in the manuscripts. For example:

As man can produce and certainly has produced a great result by his methodical and unconscious means of selection, what may not nature effect? Man can act only on external and visible characters: nature cares nothing for appearances, except in so far as they may be useful to any being. She can act on every internal organ, on every shade of constitutional difference, on the whole machinery of life. Man selects only for his own good; Nature only for that of the being which she tends. Every selected character is fully exercised by her; and the being is placed under well-suited conditions of life. (Ibid., 83)

The manuscript history behind such passages prevents the simple discounting of these statements as mere rhetorical imagery. As we have seen, the parallel between intentional human selectivity and that of “nature” formed the proportional analogical model upon which the concept of natural selection was originally constructed.

Criticisms that quickly developed over the overt intentionality embedded in such passages, however, led Darwin to revise the argument in editions beginning with the third edition of 1861. From this point onward he explicitly downplayed the intentional and teleological language of the first two editions, denying that his appeals to the selective role of “nature” were anything more than a literary figure. Darwin then moved decisively in the direction of defining natural selection as the description of the action of natural laws working upon organisms rather than as an efficient or final cause of life. He also regrets in his Correspondence his mistake in not utilizing the designation “natural preservation” rather than “natural selection” to characterize his principle (letter to Lyell 28 September 1860, Burkhardt Correspondence 8, 397; also see Darwin Correspondence Project in Other Internet Resources ). In response to criticisms of Alfred Russel Wallace, Darwin then adopted in the fifth edition of 1869 his contemporary (1820–1903) Herbert Spencer’s designator, “survival of the fittest”, as a synonym for “natural selection” (Spencer 1864, 444–45; Darwin 1869, 72). This redefinition further shifted the meaning of natural selection away from the concept that can be extracted from the early texts and drafts. These final statements of the late 1860s and early 70s underlie the tradition of later “mechanistic” and non-teleological understandings of natural selection, a reading developed by his disciples who, in the words of David Depew, “had little use for either his natural theodicy or his image of a benignly scrutinizing selection” (Depew 2009, 253). The degree to which this change preserved the original strong analogy between art and nature can, however, be questioned. Critics of the use of this analogy had argued since the original formulations that the comparison of the two modes of selection actually worked against Darwin’s theory (Wallace 1858 in Glick and Kohn 1997, 343). This critique would also be leveled against Darwin in the critical review of 1867 by Henry Fleeming Jenkin discussed below.

The conceptual synthesis of Chapter Four also introduced discussions of such matters as the conditions under which natural selection most optimally worked, the role of isolation, the causes of the extinction of species, and the principle of divergence. Many of these points were made through the imaginative use of “thought experiments” in which Darwin constructed possible scenarios through which natural selection could bring about substantial change.

One prominent way Darwin captured for the reader the complexity of this process is reflected in the single diagram to appear in all the editions of the Origin . In this illustration, originally located as an Appendix to the first edition, but thereafter moved into Chapter Four, Darwin summarized his conception of how species were formed and diverged from common ancestral points. This image also served to depict the frequent extinction of most lineages, an issue developed in detail in Chapter Ten. It displayed pictorially the principle of divergence, illustrating the general tendency of populations to diverge and fragment under the pressure of population increase. It supplied a way of envisioning relations of taxonomic affinity to time, and illstrated the persistence of some forms unchanged over long geological periods in which stable conditions prevail.

Figure: Tree of life diagram from Origin of Species ( Origin 1859:“Appendix”.

Remarkable about Darwin’s diagram of the tree of life is the relativity of its coordinates. It is first presented as applying only to the divergences taking place in taxa at the species level, with varieties represented by the small lower-case letters within species A–L of a “wide ranging genus”, with the horizontal lines representing time segments measured in terms of a limited number of generations. However, the attentive reader could quickly see that Darwin’s destructive analysis of the distinction between “natural” and “artificial” species in Chapter Two, implied the relativity of the species-variety distinction, this diagram could represent eventually all organic relationships, from those at the non-controversial level of diverging varieties within fixed species, to those of the relations of Species within different genera. Letters A–L could also represent taxa at the level of genera, families or orders. The diagram can thus be applied to relationships between all levels of the Linnaean hierarchy with the time segments representing potentially vast expanses of time, and the horizontal spread of branches the degree of taxonomic divergence over time. In a very few pages of argument, the diagram was generalized to represent the most extensive group relations, encompassing the whole of geological time. Extension of the dotted lines at the bottom could even suggest, as Darwin argues in the last paragraph of the Origin , that all life was a result of “several powers, having been originally breathed into a few forms or into one” (Darwin 1859 [1964], 490). This could suggest a single naturalistic origin of all original forms either by material emergence, or through the action of a vitalistic power of life. Darwin’s use of Biblical language could also be read as allowing for the action of a supernatural cause.

In response to criticisms concerning this latter point, Darwin quickly added to the final paragraph in the second edition of 1860 the phrase “by the Creator” (1860: 484), which remained in all subsequent editions. as did the quotations on the frontispiece from familiar discussions in British natural theology concerning creation by secondary causation. Conceptual space was thereby created for the reading of the Origin by some contemporaries, notably by the Harvard botanist Asa Gray (1810–88), as compatible with traditional natural theology (Gray 1860).

The sweep of the theoretical generalization that closed the natural selection chapter, one restated even more generally in the final paragraph of the book, required Darwin to deal with several obvious objections to the theory that constitute the main “defensive” chapters of the Origin (Five–Nine), and occupy him through the numerous revisions of the text between 1859 and 1872. As suggested by David Depew, the rhetorical structure of the original text developed in an almost “objections and response” structure that resulted in a constant stream of revisions to various editions of the original text as Darwin engaged his opponents (Depew 2009; Peckham 2006). Anticipating at first publication several obvious lines of objection, Darwin devoted much of the text of the original Origin to offering a solution in advance to predictable difficulties. As Darwin outlined these main lines of objection, he discussed, first, the apparent absence of numerous slight gradations between species, both in the present and in the fossil record, of the kind that would seem to be predictable from the gradualist workings of the theory (Chps. Six, Nine). Second, the gradual development of organs and structures of extreme complexity, such as the vertebrate eye, an organ which had since Antiquity served as a mainstay of the argument for external teleological design (Chp. Six). Third, the evolution of the elaborate instincts of animals and the puzzling problem of the evolution of social insects that developed sterile neuter castes, proved to be a particularly difficult issue for Darwin in the manuscript phase of his work and needed some account (Chp. Seven). As a fourth major issue needing attention, the traditional distinction between natural species defined by interfertility, and artificial species defined by morphological differences, required an additional chapter of analysis in which he sought to undermine the absolute character of the interbreeding criterion as a sign of fixed natural species (Chp. Eight).

In Chapter Ten, Darwin developed his interpretation of the fossil record. At issue was the claim by Lamarckian and other transformists, as well as Cuvierian catastrophists such as William Buckland (1784–1856) (see the entry on evolutionary thought before Darwin , Section 4.1), that the fossil record displayed a historical sequence beginning with simpler plants and animals, arriving either by transformism or replacement, at the appearance of more complex forms in geological history. Opposition to this thesis of “geological progressionism” had been made by none other than Darwin’s great mentor in geology, Charles Lyell in his Principles of Geology (Lyell 1832 [1990], vol. 2, chp. xi; Desmond 1984; Bowler 1976). Darwin defended the progressionist view against Lyell’s arguments in this chapter.

To each of the lines of objection to his theory, Darwin offered his contemporaries plausible replies. Additional arguments were worked out through the insertion of numerous textual insertions over the five revisions of the Origin between 1860 and 1872, including the addition of a new chapter to the sixth edition dealing with “miscellaneous” objections, responding primarily to the criticisms of St. George Jackson Mivart (1827–1900) developed in his Genesis of Species (Mivart 1871).

For reasons related both to the condensed and summary form of public presentation, and also as a reflection of the bold conceptual sweep of the theory, the primary argument of the Origin could not gain its force from the data presented by the book itself. Instead, it presented an argument from unifying simplicity, gaining its force and achieving assent from the ability of Darwin’s theory to draw together in its final synthesizing chapters (Ten–Thirteen) a wide variety of issues in taxonomy, comparative anatomy, paleontology, biogeography, and embryology under the simple principles worked out in the first four chapters. This “consilience” argument might be seen as the best reflection of the impact of William Whewell’s methodology (see above).

As Darwin envisioned the issue, with the acceptance of his theory, “a grand untrodden field of inquiry will be opened” in natural history. The long-standing issues of species origins, if not the explanation of the ultimate origins of life, as well as the causes of their extinction, had been brought within the domain of naturalistic explanation. It is in this context that he makes the sole reference in the text to the claim that “light will be thrown on the origin of man and his history”. And in a statement that will foreshadow the important issues of the Descent of Man of 1871, he speaks of how “Psychology will be based on a new foundation, that of the necessary acquirement of each mental power and capacity by gradation” (ibid., 488)

3. The Reception of the Origin

The broad sweep of Darwin’s claims, the brevity of the empirical evidence actually supplied in the Origin , and the implications of his theory for several more general philosophical and theological issues, opened up a controversy over Darwinian evolution that has waxed and waned over more than 160 years. The theory was inserted into a complex set of different national and cultural receptions the study of which currently forms a scholarly industry in its own right. European, Latin American and Anglophone receptions have been most deeply studied (Bowler 2013a; Gayon 2013; Largent 2013; Glick 1988, 2013; Glick and Shaffer 2014; Engels and Glick 2008; Gliboff 2008; Numbers 1998; Pancaldi, 1991; Todes 1989; Kelly 1981; Hull 1973; Mullen 1964). To these have been added analyses of non-Western recptions (Jin 2020, 2019 a,b; Yang 2013; Shen 2016; Elshakry 2013; Pusey 1983). These analyses display common patterns in both Western and non-Western readings of Darwin’s theory, in which these receptions were conditioned, if not determined, by the pre-existing intellectual, scientific, religious, social, and political contexts into which his works were inserted.

In the anglophone world, Darwin’s theory fell into a complex social environment that in the United States meant into the pre-Civil War slavery debates (Largent 2013; Numbers 1998). In the United Kingdom it was issued against the massive industrial expansion of mid-Victorian society, and the development of professionalized science. To restrict focus to aspects of the British reading public context, the pre-existing popularity of the anonymous Vestiges of the Natural History of Creation of 1844, which had reached 11 editions and sold 23,350 copies by December of 1860 (Secord “Introduction” to Chambers 1844 [1994], xxvii]), with more editions to appear by the end of the century, certainly prepared the groundwork for the general notion of the evolutionary origins of species by the working of secondary natural laws. The Vestiges ’s grand schema of a teleological development of life, from the earliest beginnings of the solar system in a gaseous nebula to the emergence of humanity under the action of a great “law of development”, had also been popularized for Victorian readers by Alfred Lord Tennyson’s epic poem In Memoriam (1850). This Vestiges backdrop provided a context in which some could read Darwin as supplying additional support for the belief in an optimistic historical development of life under teleological guidance of secondary laws with the promise of ultimate historical redemption. Such readings also rendered the Origin seemingly compatible with the progressive evolutionism of Darwin’s contemporary Herbert Spencer (see the entry on Herbert Spencer ). Because of these similarities, Spencer’s writings served as an important vehicle by which Darwin’s views, modified to fit the progressivist views expounded by Spencer, were first introduced in non-Western contexts (Jin 2020, 2019 a,b; Lightman [ed.] 2015; Pusey 1983). Such popular receptions ignored or revised Darwin’s concept of evolution by natural selection to fit these progressivist alternatives.

Outside the United Kingdom, the receptions of Darwin’s work display the importance of local context and pre-existent intellectual and social conditions. Three examples—France, Germany, and China—can be elaborated upon. In France, Darwin’s theory was received against the background of the prior debates over transformism of the 1830s that pitted the theories of Lamarck and Etienne Geoffroy St. Hilaire against Cuvier (Gayon 2013; entry on evolutionary thought before Darwin , 4.1). At least within official French Academic science, these debates had been resolved generally in favor of Cuvier’s anti-transformism. The intellectual framework provided by the “positive philosophy” of Auguste Comte (1798–1857) also worked both for and against Darwin. On one hand, Comte’s emphasis on the historical progress of science over superstition and metaphysics allowed Darwin to be summoned in support of a theory of the progress of science. The Origin was so interpreted in the preface to the first French translation of the Origin made by Clémence Royer (Harvey 2008). On the other hand, the Comtean three stages view of history, with its claim of the historical transcendence of speculative and metaphysical periods of science by a final period of experimental science governed by determinate laws, placed Darwinism in a metaphysical phase of speculative nature philosophy. This view is captured by the assessment of the leading physiologist and methodologist of French Science, Claude Bernard (1813–78). As he stated this in his 1865 treatise on scientific methodology, Darwin’s theory was to be regarded with those of “a Goethe, an Oken, a Carus, a Geoffroy Saint Hilaire”, locating it within speculative philosophy of nature rather than granting it the status of “positive” science (Bernard 1865 [1957], 91–92]).

In the Germanies, Darwin’s work entered a complex social, intellectual and political situation in the wake of the failed efforts to establish a liberal democracy in 1848. It also entered an intellectual culture strongly influenced by the pre-existent philosophical traditions of Kant, Schelling’s Naturphilosophie , German Romanticism, and the Idealism of Fichte and Hegel (R. J. Richards 2002, 2008, 2013; Gliboff 2007, 2008; Mullen 1964). These factors formed a complex political and philosophical environment into which Darwin’s developmental view of nature and theory of the transformation of species was quickly assimilated, if also altered. Many readings of Darwin consequently interpreted his arguments against the background of Schelling’s philosophy of nature. The marshalling of Darwin’s authority in debates over scientific materialism were also brought to the fore by the enthusiastic advocacy of Darwinism in Germany by University of Jena professor of zoology Ernst Heinrich Haeckel (1834–1919). More than any other individual, Haeckel made Darwinismus a major player in the polarized political and religious disputes of Bismarckian Germany (R. J. Richards 2008). Through his polemical writings, such as the Natural History of Creation (1868), Anthropogeny (1874), and Riddle of the Universe (1895–99), Haeckel advocated a materialist monism in the name of Darwin, and used this as a stick with which to beat traditional religion. Much of the historical conflict between religious communities and evolutionary biology can be traced back to Haeckel’s polemical writings, which went through numerous editions and translations, including several English and American editions that appeared into the early decades of the twentieth century.

To turn to a very different context, that of China, Darwin’s works entered Chinese discussions by a curious route. The initial discussions of Darwinian theory were generated by the translation of Thomas Henry Huxley’s 1893 Romanes Lecture “Evolution and Ethics” by the naval science scholar Yan Fu (1854–1921), who had encountered Darwinism while being educated at the Royal Naval College in Greenwich from 1877 to 1879. This translation of Huxley’s lecture, published in 1898 under the name of Tianyan Lun , was accompanied with an extensive commentary by Yan Fu that drew heavily upon the writings of Herbert Spencer which Yan Fu placed in opposition to the arguments of Huxley. This work has been shown to have been the main vehicle by which the Chinese learned indirectly of Darwin’s theory (Jin 2020, 2019 a, b; Yang 2013; Pusey 1983). In the interpretation of Yan Fu and his allies, such as Kan Yuwei (1858–1927), Darwinism was given a progressivist interpretation in line with aspects of Confucianism.

Beginning in 1902, a second phase of Darwinian reception began with a partial translation of the first five chapters of the sixth edition of the Origin by the Chinese scientist, trained in chemistry and metallurgy in Japan and Germany, Ma Junwu (1881–1940). This partial translation, published between 1902 and 1906, again modified the text itself to agree with the progressive evolutionism of Spencer and with the progressivism already encountered in Yan Fu’s popular Tianyan Lun. Only in September of 1920 did the Chinese have Ma Junwu’s full translation of Darwin’s sixth edition. This late translation presented a more faithful rendering of Darwin’s text, including an accurate translation of Darwin’s final views on natural selection (Jin 2019 a, b). As a political reformer and close associate of democratic reformer Sun Yat-Sen (1866–1925), Ma Junwu’s interest in translating Darwin was also was involved with his interest in revolutionary Chinese politics (Jin 2019a, 2022).

The reception of the Origin by those who held positions of professional research and teaching positions in universities, leadership positions in scientific societies, and employment in museums, was complex. These individuals were typically familiar with the empirical evidence and the technical scientific issues under debate in the 1860s in geology, comparative anatomy, embryology, biogeography, and classification theory. This group can usually be distinguished from lay interpreters who may not have made distinctions between the views of Lamarck, Chambers, Schelling, Spencer, and Darwin on the historical development of life.

If we concentrate attention on the reception by these professionals, Darwin’s work received varied endorsement (Hull 1973). Many prominent members of Darwin’s immediate intellectual circle—Adam Sedgwick, William Whewell, Charles Lyell, Richard Owen, and Thomas Huxley—had previously been highly critical of Chambers’s Vestiges in the 1840s for its speculative character and its scientific incompetence (Secord 2000). Darwin himself feared a similar reception, and he recognized the substantial challenge facing him in convincing this group and the larger community of scientific specialists with which he interacted and corresponded widely. With this group he was only partially successful.

Historical studies have revealed that only rarely did members of the scientific elites accept and develop Darwin’s theories exactly as they were presented in his texts. Statistical studies on the reception by the scientific community in England in the first decade after the publication of the Origin have shown a complicated picture in which there was neither wide-spread conversion of the scientific community to Darwin’s views, nor a clear generational stratification between younger converts and older resisters, counter to Darwin’s own predictions in the final chapter of the Origin (Hull et al. 1978). These studies also reveal a distinct willingness within the scientific community to separate acceptance of Darwin’s more general claim of species descent with modification from common ancestors from the endorsement of his explanation of this descent through the action of natural selection on slight morphological variations.

Of central importance in analyzing this complex professional reception was the role assigned by Darwin to the importance of normal individual variation as the source of evolutionary novelty. As we have seen, Darwin had relied on the novel claim that small individual variations—the kind of differences considered by an earlier tradition as merely “accidental”—formed the raw material upon which, by cumulative directional change under the action of natural selection, major changes could be produced sufficient to explain the origin and subsequent differences in all the various forms of life over time. Darwin, however, left the specific causes of this variation unspecified beyond some effect of the environment on the sexual organs. Variation was presented in the Origin with the statement that “the laws governing inheritance are quite unknown” (Darwin 1859 [1964], 13). In keeping with his commitment to the gradualism of Lyellian geology, Darwin also rejected the role of major “sports” or other sources of discontinuous change in this process.

As critics focused their attacks on the claim that such micro-differences between individuals could be accumulated over time without natural limits, Darwin began a series of modifications and revisions of the theory through a back and forth dialogue with his critics that can be followed in his revisions to the text of the Origin . In the fourth edition of 1866, for example, Darwin inserted the claim that the continuous gradualism depicted by his branching diagram was misleading, and that transformative change does not necessarily go on continuously. “It is far more probable that each form remains for long periods unaltered, and then again undergoes modification” (Darwin 1866, 132; Peckham 2006, 213). This change-stasis-change model allowed variation to stabilize for a period of time around a mean value from which additional change could then resume. Such a model would, however, presumably require even more time for its working than the multi-millions of years assumed in the original presentation of the theory.

The difficulties in Darwin’s arguments that had emerged by 1866 were highlighted in a lengthy and telling critique in 1867 by the Scottish engineer Henry Fleeming Jenkin (1833–1885) (typically Fleeming Jenkin). Using an argument previously raised in the 1830s by Charles Lyell against Lamarck, Fleeming Jenkin cited empirical evidence from domestic breeding that suggested a distinct limitation on the degree to which normal variation could be added upon by selection (Fleeming Jenkin 1867 in Hull 1973). Using a loosely mathematical argument, Fleeming Jenkin argued that the effects of intercrossing would continuously swamp deviations from the mean values of characters and result in a tendency of the variation in a population to return to mean values over time. It is also argued that domestic evidence does not warrant an argument for species change. For Fleeming Jenkin, Darwin’s reliance on continuous additive deviation was presumed to be undermined by these arguments, and only more dramatic and discontinuous change—something Darwin explicitly rejected—could account for the origin of new species.

Fleeming Jenkin also argued that the time needed by Darwin’s theory to account for the history of life under the gradual working of natural selection was simply unavailable from scientific evidence, supporting this claim by an appeal to the physical calculations of the probable age of the solar system presented in publications by his mentor, the Glasgow physicist William Thompson (Lord Kelvin, 1824–1907) (Burchfield 1975). On the basis of Thompson’s quantitative physical arguments concerning the age of the sun and solar system, Fleeming Jenkin judged the time since the presumed first beginnings of life to be insufficient for the Darwinian gradualist theory of species transformation to have taken place.

Jenkin’s multi-pronged argument gave Darwin considerable difficulties and set the stage for more detailed empirical inquiries into variation and its causes by Darwin’s successors. The time difficulties were only resolved in the twentieth-century with the discovery of radioactivity that could explain why the sun did not lose heat in accord with Newtonian principles.

As a solution to the variation question, Darwin developed his “provisional hypothesis” of pangenesis, which he presented the year after the appearance of the Fleeming Jenkin review in his two-volume Variation of Plants and Animals Under Domestication (Darwin 1868; Olby 2013). Although this theory had been formulated independently of the Jenkin review (Olby 1963), in effect it functioned as Darwin’s reply to Jenkin’s critique. The pangenesis theory offered a causal theory of variation and inheritance through a return to a theory resembling Buffon’s theory of the organic molecules proposed in the previous century (see entry on evolutionary thought before Darwin section 3.2). Invisible material “gemmules” were presumed to exist within the cells. According to theory, these were subject to external alteration by the environment and other external causes. The gemmules were then shed continually into the blood stream (the “transport” hypothesis) and assembled by “mutual affinity for each other, leading to their aggregation either into buds or into the sexual elements” (Darwin 1868, vol. 2, 375). In this form they were then transmitted—the details were not explained—by sexual generation to the next generation to form the new organism out of “the modified physiological units of which the organism is built” (ibid., 377). In Darwin’s view, this hypothesis united together numerous issues into a coherent and causal theory of inheritance and explained the basis of variation. It also explained how use-disuse inheritance, a theory which Darwin never abandoned, could work.

The pangenesis theory, although not specifically referred to, seems to be behind an important distinction Darwin inserted into the fifth edition of the Origin of 1869 in his direct reply to the criticisms of Jenkin. In this textual revision, Darwin distinguished “certain variations, which no one would rank as mere individual differences”, from ordinary variations (Darwin1869, 105; Peckham 2006, 178–179). This revision shifted Darwin’s emphasis away from his early reliance on normal slight individual variation, and gave new status to what he now termed “strongly marked” variations. The latter were now the forms of variation to be given primary evolutionary significance. Presumably this strong variation was more likely to be transmitted to the offspring, although details are left unclear, and in this form major variation could presumably be maintained in a population against the tendency to swamping by intercrossing as Fleeming Jenkin had argued.

Darwin’s struggles over this issue defined a set of problems that British life scientists in particular were to deal with into the 1930s. These debates over the role of somatic variation in the evolutionary process placed Darwinism in a defensive posture that forced its supporters into major revisions in the Darwinian research program (Gayon 1998; Vorzimmer 1970). The consequence was a complex period of Darwinian history in which natural selection theory was rejected by many research, or defended in modified form by others (Bowler 1983, 2013a; Largent 2009).

4. Human Evolution and the Descent of Man

Darwin had retained his own conclusions on human evolution quietly in the background through the 1860’s while the defense of his general theory was conducted by advocates as diverse as Thomas Henry Huxley (1825–95) in England, Asa Gray (1810–88) in the United States, and Ernst Haeckel (1834–1919) in the emerging new Germany. Darwin’s own position on the “human question” remained unclear to the reading public, and his rhetorical situating of the Origin within a tradition of divine creation by secondary law, captured in the frontispiece quotations from William Whewell and Francis Bacon, allowed many before 1871 to see Darwin as more open to religious interpretations of human origins than those of some of his popularizers.

Darwin’s interest in developing his insights into the origins of human beings and the explanation of human properties through descent with modification was, however, evident in his correspondence as early as January of 1860 when he began collecting evidence on the expressions of the emotions in human beings (Browne 2002, chp. 9). He then developed a questionnaire specifically intended to gain such information from contacts in Patagonia and Tierra del Fuego (Radick 2018). Further engagement with these issues was then generated by the discussions of Lyell (1863) and A. R. Wallace (1864), both of whom suggested that natural selection could not account for the development of the “higher” rational faculties, language, and ethical motivation (R. J. Richards 1987, chp. 4). It was then in February of 1867 that Darwin decided to remove material from his massive manuscript of the Variation of Plants and Animals Under Domestication to create a “very small volume, ‘an essay on the origin of mankind’” (Darwin to Hooker, 8 February 1867 and CD to Turner, 11 February 1867, Burkhardt, Correspondence 15: 74, 80). At this time he also sent to several international correspondents a more detailed questionnaire asking for information on human emotional expression. Further impetus to develop his views was created by the arguments of William R. Greg (1809–1881) in an essay in Fraser’s Magazine (1868), with further support by arguments of A. R. Wallace in 1869, both of whom drew a sharp distinction between human properties and those of animals (R. J. Richards 1987, 172–184). These arguments denied that natural selection could explain the origins of these “higher powers”.

Darwin’s drafting of his views on human issues, begun in early 1868, expanded into a major enterprise in which he became deeply engaged with the issue of the implications of his theory for ethics. The result of this effort devoted to anthropological topics was two separate works: the Descent of Man and Selection in Relation to Sex , delivered to the publisher in June of 1870 with publication in 1871, and its companion, Expression of the Emotions in Man and Animals , which he commenced in early 1871 with publication in early 1872.

As commentators have noted, these two works differ markedly in their arguments, and reflect different relationships to Darwin’s causal theories of natural and sexual selection, with sexual selection predominting over natural selection for the major portion of the Descent , and both of these causal theories generally missing from the descriptive approach of the Expression (Radick 2018).

Sexual selection—the choosing of females by males or vice versa for breeding purposes—had received a general statement by Darwin in Chapter IV of the Origin , but this played only a minor role in the original argument, and its importance was denied by co-evolutionist A. R. Wallace. In the Descent this was now developed in extensive detail as a major factor in evolution that could even work against ordinary natural selection. Sexual selection could be marshaled to explain sexual dimorphism, and also the presence of unusual characters and properties of organisms—elaborate feeding organs, bright colors, and other seemingly maladaptive structures such as the antlers on the Irish Elk or the great horn on the Rhinoceros beetle—that would appear anomalous outcomes of ordinary natural selection working for the optimal survival of organisms in nature. In a dramatic extension of the principle to human beings, the combination of natural and sexual selection is used to explain the origins of human beings from simian ancestors. It also accounts for the sexual dimorphism in humans, and is a major factor accounting for the origin of human races (E. Richards 2017; R. A. Richards 2013).

Although the secondary causal role of sexual selection in the development of species generally was to be the main topic of the bulk of the Descent , this plays an ambiguous role initially in the “treatise on man” that occupies the initial chapters, and functions differently in his treatment of the origins of mental powers, the moral sense, and the origin of races in this opening discussion.

In constructing this presentation, Darwin reaches back to the early Notebooks that he had separated out from the “transformist” discussions to deal with his inquiries into ethics, psychology, and emotions (see Section 1.2 above). Of particular importance for the opening discussions of the Descent was the “M” notebook, commenced in July of 1838, and “N”, begun in October of that year. On occasion he also samples the collection of entries now entitled “Old and Useless Notes”, generally written between 1838 and 1840.

The initial topic of focus in the Descent deals with the far-reaching issues concerning the status and origin of human mental properties, faculties presumed traditionally to be possessed uniquely by human beings. These properties Darwin now places on an evolutionary continuum with those features of animal behavior long regarded as instinctual. In this he placed himself in opposition to the long tradition of discourse that had distinguished humans from animals due to the possession of a “rational principle” related to their possession of a rational soul. This tradition had been given a more radical foundation in the revolutionary reflections on the relation of mind and body initiated by René Descartes (1596–1650) in the middle of the seventeenth century. Descartes deepened this distinction with the separation of the two substances—thinking substance, or res cogitans , possessed only by humans, and extended material substance, res extensa that constituted the rest of the natural world, including animals and plants, rendering animals only lifeless machines without rational faculties.

Darwin’s collapse of this Cartesian barrier with his theory of human origins outlined in the Descent continued a discussion that had been a concern of his transformist predecessors, especially Jean Baptiste Lamarck (Sloan 1999). But Darwin took this issue to a new level as he interpreted the human-animal relationship in the context of his novel theory of divergent evolution from common ancestors. Darwin also broke with the view of humans as the summit of a natural teleological process. Darwin instead denies such teleological ordering, and effectively reduces human properties to those of animals—mental as well as physical—by tracing them to their origin in properties of lower organisms.

The warrant for the identification of human and animal mental properties, however, is not supported by substantial argumentation in the Descent. The opening discussions of the treatise summarize the anatomical evidence for “homologies” —true identities—between humans and animals due to descent from common ancestors, claims already set out in Chapter Thirteen of the Origin. But the transferal of this identity of structure to inner non-anatomical “mental” properties rested on premises that are not made explicit in this text, and were not identities drawn by Huxley, Wallace and Lyell, for example, in their treatments of humans in relation to evolutionary theory, although they acknowledged the anatomical continuities.

To understand Darwin’s arguments, it is useful to return to his Notebook discussions on which he was drawing for his reasoning (see above, Section 1.2). In his “C” Notebook, opened in February of 1838, Darwin has a remarkable entry that displays very early on his commitment to a metaphysical “monism”—the thesis that there is only one substance underlying both mind and body. With this goes the thesis of a parallelism of the complexity of mental properties with those of material structure. In this entry in “C” following on Darwin’s reflections on the issue of instinct, and also recording some of his observations on animals at the Regents Park zoological gardens, Darwin comments:

There is one living spirit, prevalent over this wor[l]d, (subject to certain contingencies of organic matter & chiefly heat), which assumes a multitude of forms <<each having acting principle>> according to subordinate laws.—There is one thinking […] principle (intimately allied to one kind of organic matter—brain. & which <prin> thinking principle. seems to be given or assumed according to a more extended relations [ sic ] of the individuals, whereby choice with memory, or reason ? is necessary.—) which is modified into endless forms, bearing a close relation in degree & kind to the endless forms of the living beings.— We see thus Unity in thinking and acting principle in the various shades of <dif> separation between those individuals thus endowed, & the community of mind, even in the tendency to delicate emotions between races, & recurrent habits in animals.— (Barrett 1987, 305)

As we follow these issues into the “M” Notebook, the assumption of a single “thinking principle,” allied to one kind of organic matter, seems then to underlie Darwin’s subsequent reflections on mind and matter. The “M” Notebook cites numerous “mental”properties common to humans and animals that generally parallel levels of material organization, similar to the identities expressed in the later Descent. The range of this universal extension of mental properties is far-reaching in these early discussions: consciousness and “free will” extends to all animals, including invertebrates:

With respect to free will, seeing a puppy playing cannot doubt that they have free will, if so all animals., then an oyster has & a polype (& a plant in some senses […]; now free will of oyster, one can fancy to be direct effect of organization, by the capacities its senses give it of pain or pleasure, if so free will is to mind, what chance is to matter […] (Barrett 1987, 536).

When these themes reappear in Chapter Two of the first edition of the Descent , Darwin seems to draw implicitly upon this matter-mind identity theory as an obvious consequence of his theory of descent from common ancestry. There he enumerates a long list of traditional human mental and emotional properties to claim that each of them are identities with the properties of simpler forms of life. The list is expansive: courage, deceit, play, kindness, maternal affection, self-complacency, pride, shame, sense of honor, wonder, dread, imitation, imagination, and dreaming. All are considered to be represented in a wide range of animals, with “play”and “recognition” found even in the ants.

When he addresses the more complex mental properties that specifically had been considered by a long tradition of discussion to be the distinctive human properties—possession of language, reason, abstract conceptual thinking, self-reflection—these again are treated as having their manifestations in other forms of life, with none of them unique to human beings. Language, the property that Descartes, for example, had considered to be the primary distinguishing character denoting the human possession of mind as distinct from matter, Darwin treats a developing in a gradual process from animal sounds that parallel the differentiation of species, illustrated by the fact that languages “like organic beings, can be classed in groups under groups” (Darwin 1871 [1981], 60). He closes his discussion of mental powers with an analysis of religious belief that derives it from imagination and belief in spirits found in aboriginal peoples. It can even be homologized with the “deep love of a dog for his master, associated with complete submissions, some fear, and perhaps other feelings” (ibid., 68). Darwin’s discussions of the relation of human and animal mental and emotional properties would set the agenda for a complex discussion that would carry into contemporary debates over animal cognition and the relations of human and animal properties (see the entries on animal cognition ; methods in comparative cognition ; and animal consciousness ).

The subsequent treatment of ethical issues in the third chapter of the Descent was for Darwin a topic to be approached “exclusively from the side of natural history” (ibid., 71). This issue also presented him with some of his most difficult conceptual problems (CD to Gray, 15 March 1870, Burkhardt, Correspondence 18, 68). In this discussion he also employs natural selection theory as an explanatory cause.

Under the heading of “Moral Sense”, Darwin offered some innovations in ethics that do not easily map on to standard ethical positions classified around the familiar categories of Rule or Act Utilitarianism, Kantian Deontology, Hedonism, and Emotivism. Darwin’s closest historical affinities are with the Scottish “Moral Sense” tradition of Frances Hutcheson (1694–1746), Adam Smith (1723?–1790), and David Hume (1711–1776). More immediately Darwin drew from the expositions of the moral sense theory by his distant relative, Sir James Macintosh (1765–1832) (R. J. Richards 1987, 114–122, 206–219).

Traditional moral sense theory linked ethical behavior to an innate property that was considered to be universal in human beings, although it required education and cultivation to reach its full expression (see the entry on moral sentimentalism ). This inherent property, or “moral” sense, presumably explained such phenomena as ethical conscience, the sense of moral duty, and it accounted for altruistic actions that could not be reduced to hedonic seeking of pleasure and avoiding pain. It also did not involve the rational calculation of advantage, or the maximization of greatest happiness by an individual prior to action, as implied by Utilitarianism. For this reason Darwin criticized John Stuart Mill’s version of Utilitarian theory because it relied on acquired habits and the calculation of advantage (Darwin 1871 [1981], 71n5).

Darwin’s reinterpretation of the moral sense tradition within his evolutionary framework also implied important transfomations of this theory of ethics. The moral sense was not to be distinguished from animal instinct but was instead derived historically from the social instincts and developed by natural selection. From this perspective, Darwin could claim a genuine identity of ethical foundations holding between humans and animals, with the precursors of human ethical behavior found in the behavior of other animals, particularly those with social organization. Natural selection then shaped these ethical instincts in ways that favored group survival over immediate individual benefit (ibid., 98). Human ethical behavior is therefore grounded in a natural property developed by natural selection, with the consequence that ethical actions can occur without moral calculus or rational deliberation.

When moral conflict occurs, this is generally attributed to a conflict of instincts, with the stronger of two conflicting instincts favored by natural selection insofar as it favors group benefit (ibid. 84). In human beings the “more enduring Social Instincts” thus come to override the less persistent “individual” instincts.

The adequacy of evolutionary ethical naturalism as a foundation for ethical realism proved to be a point of contention for Darwin’s contemporaries and successors following the publication of the Descent . For some moral philosophers, Darwin had simply reduced ethics to a property subject to the relativizing tendencies of natural selection (Farber 1994: chp. 5). It was, in the view of Darwin’s philosophical critics, to reduce ethics to biology and in doing so, to offer no way to distinguish ethical goods from survival advantages. Not even for some strong supporters of Darwinism, such as Thomas Huxley and Alfred Russel Wallace, was Darwin’s account adequate (ibid., chp. 4). Much of subsequent development of moral philosophy after Darwin would be grounded upon the canonical acceptance of the “is-ought” distinction, which emerged with new force from the critique of “evolutionary” ethical theory. This critique began with Thomas Huxley’s own break with Darwinian ethical theory in his Romanes Lecture, “Evolution and Ethics”of 1893 (Huxley 1893). This lecture, reflecting Huxley’s views eleven years after Darwin’s death, would play an important role in the Chinese reception of Darwinism (Huxley 1895; see above, section 3.1). This line of critique also received an influential academic expression in G. E. Moore’s (1873–1958) Principia Ethica —itself an attack on Spencer’s version of evolutionary ethics (Moore 1903). Debates over the adequacy of evolutionary ethics continue into the present (see the entries on biological altruism and morality and evolutionary biology ; see also, R. J. Richards 2015, 2009, 1999, 1987, Appendix 2; Charmetant 2013; Boniolo and DeAnna (eds.) 2006; Hauser 2006; Katz (ed.) 2000; Maienschein and Ruse (eds.) 1999).

4.4 Reception of the Descent

The international reception of the Descent of Man and Expression of the Emotions is a topic in need of the kind of detailed studies that surround the historical impact of the Origin. These works presented the reading public after 1871 with a more radical and controversial Darwin than had been associated with the author of the popular Journal of Researches or even the Origin itself, and his anthropological works created a watershed in the public reception of Darwin’s views (Radick 2013). The Descent finally made public Darwin’s more radical conclusions about human origins, and seemed to many of his readers, even those previously sympathetic to the Origin , to throw Darwin’s authority behind materialist and anti-religious forces. Public knowledge of Darwin’s own conclusions on human evolution before 1871 had rested on the one vague sentence on the issue in the Origin itself. The Descent made public his more radical conclusions. Even though the question of human evolution had already been dealt with in part by Thomas Huxley in his Man’s Place in Nature of 1863 (Huxley 1863), and by Charles Lyell in the same year in his Geological Evidences of the Antiquity of Man (Lyell 1863), followed by Alfred Russel Wallace’s articles in 1864 and 1870 (Wallace 1864 and online), these authors had either not dealt with the full range of questions presented by the inclusion of human beings in the evolutionary process, or they had emphasized the moral and mental discontinuity between humans and animals. Only Ernst Heinrich Haeckel had drawn out a more general reductive conception of humanity from evolutionary theory and he had not ventured into the specific issues of ethics, social organization, the origins of human races, and the relation of human mental properties to those of animals, all of which are dealt with in the Descent . Darwin’s treatise presented, as one commentator has put it, “a closer resemblance to Darwin’s early naturalistic vision than anything else he ever published” (Durant 1985, 294).

Darwin’s extension of his theory to a range of questions traditionally discussed within philosophy, theology, and social and political theory, has shaped the more general history of Darwinism since the 1870s. It set the agenda for much of the development of psychology of the late nineteenth century (R. J. Richards 1987). It also hardened the opposition of many religiously-based communities against evolutionary theory, although here again, distinctions must be made between different communities (Ellegård 1990, chp. 14). Such opposition was not simply based upon the denial of the literal scriptural account of the origins of humankind, an issue that played out differently within the main religious denominations (Haught 2013; Finnegan 2013; Swetlitz 2013; Artigas, Glick, & Martinez 2006; Moore 1979). The more fundamental opposition was due to the denial of distinctions, other than those of degree, between fundamental human properties and those of animals.

Furthermore, the apparent denial of some kind of divine guidance in the processes behind human evolution and the non-teleological character of Darwin’s final formulations of the natural selection theory in the fifth and sixth editions of the Origin , hardened this opposition. His adoption from Herbert Spencer of designator “survival of the fittest” as a synonym for “natural selection” in the fifth edition of 1869 added to this growing opposition. As a consequence, the favorable readings that many influential religious thinkers—John Henry Newman (1801–1890) is a good example—had given to the original Origin , disappeared. The rhetoric of the Descent , with its conclusion that “man is descended from a hairy quadruped, furnished with a tail and pointed ears” (Darwin 1871 [1981], 389), presented to the public a different Darwin than many had associated with the popular seagoing naturalist.

The new opposition to Darwin is reflected in the many hostile reviews of the Descent to appear in the periodical press (R. J. Richards 1987, 219–230). Particularly at issue were Darwin’s accounts of the origin of ethical principles and intelletual powers, including language, self-reflection, abstract thinking and religious belief as derivations from animal properties (Anon. 1871)

The profound revolution in thought that Darwin created, however, was eventually recognized even by his one-time harsh critics. The once leading British comparative anatomist Richard Owen (1804–1892), who had long been estranged from Darwin since his harsh review of the Origin in 1860, nonetheless could comment on the occasion of Darwin’s burial in Westminster Abbey in a letter to Horace Walpole:

The great value of Darwin’s series of works, summarizing all the evidence of Embryology, Paleontology, & Physiology experimentally applied in producing Varieties of Species, is exemplified in the general acceptance by Biologists of the Secondary Law, by Evolution, of the ‘Origin of Species’ […] In this respect Charles Darwin stands to Biology in the relation which Copernicus stood to Astronomy. […] [Copernicus] knew not how the planets revolved around the sun. To know that required the successive labours of a Galileo, a Kepler and finally a Newton […] Meanwhile our British Copernicus of Biology merits the honour and the gratitude of the Empire, which is manifest by a Statue in Westminster Abbey. (Richard Owen to Horace Walpole, 5 November, 1882, Royal College of Surgeons of England Archives, MS0025/1/5/4).

The subsequent history of the debates surrounding Darwin’s achievement forms a complex story that involves much of the history of life science, as well as ethical theory, psychology, philosophy, theology and social theory since 1870. For a general summary of recent scholarship see Ruse 2013a and articles from this encyclopedia listed below.

This article has intended to give a historical overview of the specific nature of Darwinian theory, and outline the ways in which it differed from the theories of predecessors in the nineteenth century (see the entry evolution before Darwin ). The eventual general consensus achieved by the middle of the twentieth century around the so-named “Synthetic” theory of evolution that would combine population genetics with a mathematical analysis of evolutionary change, has formed a successful research program for more than half a century (Smocovitis 1996; Mayr and Provine 1980; Provine 1971). This “synthesis” has been challenged in recent decades by the current movement known as evolutionary developmental theory, or “evo-devo”. This development represents in some important respects a return to presumably discarded traditions and lines of exploration of the nineteenth and early twentieth centuries which sought to link evolution with embryological development, and to a complex understanding of genetics, with re-examination of the effects of external conditions on inheritance (Gilbert 2015; Newman 2015; Laubichler and Maienschein 2007; Gissis and Jablonka 2011; Pigliucci and Müller 2010; Amundson 2005; Gilbert, Opitz and Raff 1996). Where these debates and revisions in evolutionary theory may lead in another fifty years is a matter of speculation (Gayon 2015 in Sloan, McKenny and Eggleson 2015).

More general philosophical issues associated with evolutionary theory—those surrounding natural teleology, ethics, the relation of evolutionary naturalism to the claims of religious traditions, the implications for the relation of human beings to the rest of the organic world—continue as issues of scholarly inquiry. The status of Darwin’s accounts of human mental powers and moral properties continue to be issues of philosophical debate. The adequacy of his reliance on sexual selection to explain sex and gender roles in human society form heated topics in some feminist scholarship. Such developments suggest that there are still substantial theoretical issues at stake that may alter the future understanding of evolutionary theory in important ways (Sloan, McKenny, & Eggleson [eds] 2015).

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How to cite this entry . Preview the PDF version of this entry at the Friends of the SEP Society . Look up topics and thinkers related to this entry at the Internet Philosophy Ontology Project (InPhO). Enhanced bibliography for this entry at PhilPapers , with links to its database.

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adaptationism | altruism | altruism: biological | animal: cognition | animal: consciousness | biology: philosophy of | comparative cognition, methods in | creationism | Darwinism | evolution: concept before Darwin | evolution: cultural | fitness | genetics: ecological | life | morality: and evolutionary biology | moral sentimentalism | natural selection | natural selection: units and levels of | Newton, Isaac: philosophy | species | Spencer, Herbert | teleology: teleological notions in biology | Whewell, William

The author wishes to acknowledge the valuable comments on this version of the article by David Depew, Gregory Radick, M. J. S. Hodge, Alan Love, and Xiaoxing Jin. Additional comments were made on an earlier version by Michael Ruse, Robert J. Richards, Edward Zalta, M. Katherine Tillman, and the anonymous reviewers for the Stanford Encyclopedia of Philosophy. I am particularly indebted to Dr. Xiaoxing Jin for information contained in his substantial doctoral work and subsequent research on the reception of Darwinism into China. Responsibility for all interpretations is my own.

Copyright © 2024 by Phillip Sloan < sloan . 1 @ nd . edu >

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Evolution: Evidence and Acceptance

Ross H. Nehm ( [email protected] ) is an associate professor of science education and evolution, ecology, and organismal biology at The Ohio State University, in Columbus. His research on evolution education was recently highlighted in Thinking Evolutionarily: Evolution Education Across the Life Sciences (National Academies Press, 2012).

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Ross H. Nehm, Evolution: Evidence and Acceptance, BioScience , Volume 62, Issue 9, September 2012, Pages 845–847, https://doi.org/10.1525/bio.2012.62.9.13

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The Evidence for Evolution. Alan R. Rogers. University of Chicago Press, 2011. 128 pp., illus. $18.00 (ISBN 9780226723822 paper).

A lthough scientists view evolution as an indisputable feature of the natural world, most Americans simply do not believe that it occurs, or they reject naturalistic explanations for biotic change. Empirical studies have revealed that students and teachers often know quite a bit about evolution but still do not accept it. This somewhat counterintuitive finding has been empirically corroborated and has led science educators to investigate this pattern in order to provide suggestions for effective evolution instruction (e.g., Rosengren et al. 2012 ). Within the lucid, compact, up-to-date, and highly readable pages of The Evidence for Evolution , author Alan R. Rogers takes an approach that most science educators have found inadequate: exclusively using logic, parsimony, and the force of evidence to precipitate conceptual change about evolutionary belief. Reactions from both supportive and dissenting readers to this nicely written text will depend on how much faith they place in the use of logic to challenge the worldviews of intelligent-design creationists.

Two premises appear to frame this short book: Biology courses and textbooks are focused on evolutionary mechanisms at the expense of the evidence for evolution, which most people are not aware of, and once disbelievers of evolution are exposed to the massive amount of evidence that exists, they will change their beliefs. I am not sure whether most biologists would agree with the first premise, given the increasingly elaborate coverage of evolution in textbooks. Indeed, having reviewed some of the best-selling introductory biology books ( Nehm et al. 2009 ), I know that many topics that Rogers discusses are, in fact, covered in these texts. I am also doubtful as to whether science educators would agree with the second premise: Empirical studies have shown that learning more about evolution often fails to precipitate a meaningful belief change.

Within the 10 chapters that form the structure of The Evidence for Evolution , the choice of topics is excellent. Also noteworthy are the use of fresh empirical examples, the integration of phylogenetic trees, and the inclusion of paleontological patterns, radiometric dating, and genomic data. The evidence for evolution is vast, and choosing appropriate examples for a short book is no small task.

Writing about evolution can be quite challenging, given that many students and teachers view teleological factors as sufficient explanations for evolutionary change. It is important, therefore, to clarify what we mean when we use such language ( Rector et al. 2012 ). At times, Rogers uses intentional or teleological language: “Every living thing must solve many engineering problems just to stay alive” (p. 34). Although biologists will understand what Rogers means, the same may not be true of novice readers. Individual organisms cannot willfully change the traits that they have (e.g., they cannot intentionally modify a phenotypic feature).

Language may also invoke ideas that are at odds with current scientific thinking, and although Rogers writes with precision and clarity, some exceptions are worth mentioning. Trait loss, for example, has been shown to be a particularly difficult concept for students and teachers to understand ( Nehm and Ha 2011 ). When describing the loss of whale limbs (“Over the next few million years, whales relied less and less on their legs,” p. 20, or “Hind limbs dwindled,” p. 22), his language may be in greater alignment with common misconceptions about use and disuse than with natural selection. When writing about evolution, scientists need to be more cognizant of readers' potential interpretations of the language that we use.

One literary device employed throughout the text is the contrast of supernatural explanations (e.g., “Perhaps we sprang from the hand of God,” p. 81) with naturalistic, evolutionary explanations. Although this approach makes the text engaging, it makes little sense from my perspective and has the potential to exacerbate readers' existing confusions about core ideas relating to the nature of science (NOS). Most students and teachers remain unaware of the ontological presuppositions that undergird the scientific process (e.g., methodological naturalism). By definition (e.g., from the National Academy of Sciences), science cannot speak to or evaluate the relative merits of supernatural explanations; no amount of evidence will ever be able to tip the scale in favor of a naturalistic explanation relative to a supernatural one or vice versa. It is not clear why Rogers takes this approach.

Students' and teachers' evolutionary acceptance levels are known to be related to their understanding of the NOS. Because many Americans are deeply confused about NOS concepts such as observation , inference , testability , theory , law , model , proof , experiment , and hypothesis ( Lederman 2007 ), addressing NOS misconceptions has become de rigueur in evolution education. I was surprised, therefore, to find that The Evidence for Evolution does not discuss what evidence is or how the term is used in evolutionary science. More problematic is the somewhat careless use of NOS terms (e.g., “this experiment proved that,” p. 12, emphasis added, and “we can also see new species forming ,” p. 16, emphasis added). In order to prevent the reinforcement of such NOS misconceptions (e.g., that scientific knowledge is certain because it is proven ; or the conflation of observation and inference ), the meanings of everyday and scientific terms must be carefully distinguished for readers.

To make the most of Rogers's important contribution, pairing The Evidence for Evolution with a textbook about the NOS (e.g., Espinoza 2012 ) is much more likely to achieve what the author admirably aspires to: an understanding, acceptance, and appreciation of evolutionary science. Facts, logic, and parsimony are unlikely, on their own, to affect most people's perceptions of the plausibility of evolution.

Espinoza F . 2012 . The Nature of Science: Integrating Historical, Philosophical, and Sociological Perspectives . Rowman and Littlefield .

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Lederman NG . 2007 . Nature of Science: Past, Present, and Future . Pages 831 – 880 in Abell SK Lederman NG , eds. Handbook of Research on Science Education . Erlbaum .

Nehm RH Ha M . 2011 . Item feature effects in evolution assessment . Journal of Research in Science Teaching 48 : 237 – 256 .

Nehm RH Poole TM Lyford ME Hoskins SG Carruth L Ewers BE Colberg PJS . 2009 . Does the segregation of evolution in biology textbooks and introductory courses reinforce students' faulty mental models of biology and evolution? Evolution: Education and Outreach 2 : 527 – 532 .

Rector MA Nehm RH Pearl D . 2012 . Learning the language of evolution: Lexical ambiguity and word meaning in student explanations . Research in Science Education . Forthcoming. (3 July 2012; www.springerlink.com/content/4117121q46082l30 ) doi:10.1007/s11165-012-9296-z

Rosengren KS Brem SK Evans EM Sinatra GM eds. 2012 . Evolution Challenges: Integrating Research and Practice in Teaching and Learning about Evolution . Oxford University Press .

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• Curriculum and Education
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• Published: 04 May 2022

Correcting misconceptions about evolution: an innovative, inquiry-based introductory biological anthropology laboratory course improves understanding of evolution compared to instructor-centered courses

• Susan L. Johnston 1 ,
• Maureen Knabb 1 ,
• Josh R. Auld 1 &
• Loretta Rieser-Danner 1  

Evolution: Education and Outreach volume  15 , Article number:  6 ( 2022 ) Cite this article

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Comprehensive understanding of evolution is essential to full and meaningful engagement with issues facing societies today. Yet this understanding is challenged by lack of acceptance of evolution as well as misconceptions about how evolution works that persist even after student completion of college-level life science courses. Recent research has suggested that active learning strategies, a focus on science as process, and directly addressing misconceptions can improve students’ understanding of evolution. This paper describes an innovative, inquiry-based laboratory curriculum for introductory biological anthropology employing these strategies that was implemented at West Chester University (WCU) in 2013–2016. The key objectives were to help students understand how biological anthropologists think about and explore problems using scientific approaches and to improve student understanding of evolution. Lab activities centered on scenarios that challenged students to solve problems using the scientific method in a process of guided inquiry. Some of these activities involved application of DNA techniques. Formative and summative learning assessments were implemented to measure progress toward the objectives. One of these, a pre- and post-course evolution concepts survey, was administered at WCU (both before and after the implementation of the new curriculum) and at three other universities with more standard introductory biological anthropology curricula. Evolution survey results showed greater improvement in understanding from pre- to post-course scores for WCU students compared with students at the comparison universities (p < .001). WCU students who took the inquiry-based curriculum also had better understanding of evolution at the post-course period than WCU students who took the course prior to implementation of the new curriculum (p < .05). In-class clicker assessments demonstrated improved understanding of evolution concepts (p < .001) and scientific method (p < .05) over the course of individual labs. Two labs that involved applying DNA methods received the highest percentage ratings by students as ‘very useful’ to understanding important concepts of evolution and human variation. WCU student ratings of their confidence in using the scientific method showed greater improvement pre- to post-course during the study period as compared with the earlier, pre-implementation period (p < .05). The student-centered biological anthropology laboratory curriculum developed at WCU is more effective at helping students to understand general and specific concepts about evolution than are more traditional curricula. This appears to be directly related to the inquiry-based approach used in the labs, the emphasis on knowledge and practice of scientific method, directly addressing misconceptions about evolution, and a structure that involves continual reinforcement of correct concepts about evolution and human variation over the semester.

Understanding the reality of evolution is fundamental to science education. However, many Americans deny the theory of evolution despite overwhelming evidence and uniform support from the scientific community (Nadelson and Hardy 2015 ). In 2006, Miller et al. published an enlightening study demonstrating the low acceptance of evolution in the United States compared to 34 other countries, with the US ranking second to last in acceptance of evolution. Data from the Pew Research Center’s ( 2015 ) Religious Landscape Study show that these results had not changed very much in the intervening decade; at that time, 34% of Americans reported that they reject evolution and believe that humans arrived on earth in their present form. Recent work by Miller et al. ( 2021 ) suggests this may be changing, with increased public acceptance of evolution in the last decade. Even though acceptance of evolution increases with level of education, from 20% in high school to 52% and 65% among college or postgraduates, respectively, the rejection rate of evolution from students in introductory biology classes can reach up to 50% (Brumfield 2005 ; Rice et al. 2010 ; Paz-y-Miño-C and Espinosa 2016 ). Even college-level instruction in evolution, then, may not increase students’ acceptance of evolution.

Perhaps more surprisingly, even when acceptance of evolution is not a factor, college-level instruction does not necessarily result in full understanding of evolution either, and numerous studies identify multiple evolution-related misconceptions held by different groups of students. For example, Cunningham and Wescott ( 2009 ) identified and evaluated biological anthropology students’ misconceptions about evolution and found that, despite acceptance of evolutionary theory, students lack understanding of the process of evolution. Tran et al. ( 2014 ) also identified similar misconceptions among advanced undergraduate biology majors. And Beggrow and Sbeglia ( 2019 ) reported that despite some differences in evolutionary reasoning and in the specific types of evolution misconceptions held by biology and anthropology majors, both populations performed poorly on a measure of evolutionary knowledge (Conceptual Inventory of Natural Selection [CINS]; Anderson et al. 2002 ). Several other instruments to assess both student misconceptions about evolution and student understanding of evolution have been developed, including the Measure of the Acceptance of Evolutionary Theory (MATE; Rutledge and Sadler 2007 ) and the Inventory of Students’ Acceptance of Evolution (I-SEA; Nadelson and Southerland 2012 ) with different student populations (see also Nehm and Mead 2019 ; Furrow and Hsu 2019 ). Results of multiple studies using these instruments show that student misconceptions continue despite college-level classroom instruction (e.g., Beggrow and Sbeglia 2019 ). Use of these types of assessment instruments aids in understanding and addressing student misconceptions, but there clearly remains a need to find the most effective teaching and learning strategies for evolution education (Glaze and Goldston 2015 ).

Pobiner ( 2016 ) recently reviewed the current state of evolution teaching and learning and concluded that focusing on human examples, such as in biological anthropology courses, is an effective way to enhance student understanding and acceptance of evolution. Based on results of the "Teaching Evolution through Human Examples" project (Pobiner et al. 2015 , 2018 ), these authors suggest that the use of human examples is helpful because human examples are relevant, they increase students’ acceptance and understanding of evolution, and they help students to appreciate historical science. Numerous other investigators have supported this suggestion (e.g., see Beggrow and Sbeglia 2019 ) and some research suggests that students across multiple disciplines (majors and non-majors) actually prefer the use of human examples when learning about evolution (e.g., Pobiner et al. 2018 ; Paz-y-Miño-C and Espinosa 2016 ). However, even with a focus on human evolution, misconceptions continue to exist (e.g., Cunningham and Westcott 2009 ; Beggrow and Sbeglia 2019 ).

Some research suggests that instructor-centered pedagogy (lecture) is less successful in helping students recognize and correct their misconceptions about evolution (Bishop and Anderson 1990 ; Gregory 2009 ) compared to historically rich, problem-solving methods of instruction that appear to significantly improve student understanding of evolution (Jensen and Finley 1996 ). Nehm and Reilly ( 2007 ) directly compared pedagogical approaches using pre- and post-course tests and found that students taught using active-learning techniques performed better than those using a more traditional approach.

Pittinsky ( 2015 ) further suggests that firsthand experience with scientific methods, as well as interactions with real scientists, would help address some of the problems in teaching evolution. It seems that when students learn to think like a scientist and use the same actions that led to original discoveries, they gain insight into the strategies and techniques used by scientists studying evolution (Passmore and Stewart 2002 ). Scharmann et al. ( 2018 ) and Nelson et al. ( 2019 ) also suggest that Nature of Science (NOS) principles should be covered before even introducing the theory of evolution. Some research supports this suggestion. For example, DeSantis ( 2009 ) reported that introduction of a curriculum module that included inquiry-based activities that model the work of paleontologists increased interest in and acceptance of the theory of evolution among middle- and high-school age students. Might the inclusion of similar inquiry-based laboratory activities also reduce the evolution misconceptions held by students (at all levels)?

Other research suggests that the order in which concepts are introduced makes a difference in students’ understanding of evolution, at least among high school students. For example, Mead et al. ( 2017 ) reported that teaching genetics first (before evolution) improves student understanding of evolution. And, Alters and Nelson ( 2002 ) as well as Beggrow and Sbeglia ( 2019 ) further suggest that targeting naïve ideas about evolution should be an instructional goal, particularly in anthropology education. Research by Bishop and Anderson ( 1990 ) and Jensen and Finley ( 1996 ) support this suggestion, reporting that confronting students’ misconceptions directly before introducing correct conceptions is associated with significant gains in student understanding of evolution. Wingert et al. ( 2022 ) show that employing instructional activities that directly challenge students' teleological concepts about natural selection improves their acceptance and understanding of evolution. 

Taken together, these results support Nelson’s ( 2008 ) recommendation of three learning strategies to improve student understanding of evolution: (1) extensively using active learning strategies; (2) focusing on science as a process and way of knowing; and (3) identifying and directly addressing student misconceptions. We report on the effectiveness of an inquiry-based laboratory curriculum that incorporates all of these strategies in an undergraduate biological anthropology course.

Evolutionary theory is central to the discipline of biological anthropology, which is fundamentally about human evolution. At West Chester University (WCU), Biological Anthropology (ANT 101) is a general education, introductory course taken by majors and non-majors that had, traditionally, been taught using a teacher-centered approach. In 2010, assessment data indicated that many students retained common misconceptions about evolution after completion of the course. For example, responses to the question “What is evolution?” included replies such as: “…survival of the fittest, species do what they need to do to pass their genes on”; “the change that occurs in an environment over time from a change in species”; “the way an organism changes to survive in a changing environment.” Clearly course changes were needed to address these misconceptions, and it seemed a good idea to attempt to do so by actively engaging students in understanding the concepts of evolution as well as the tools used by researchers to solve problems using scientific methods. Based on previous work emphasizing the need to employ human examples using active, hands-on pedagogy that emphasizes the scientific process, we developed an innovative biological anthropology laboratory course that merges these three important components of effective teaching of evolution. Based on our results, this course not only improves overall performance in correcting misconceptions when compared to other biological anthropology courses, but it also significantly improves understanding in specific areas.

Introduction to Biological Anthropology (ANT 101) has been offered annually or more frequently at WCU for nearly two decades. It is a required course for anthropology majors, and for most of that time period non-majors have been permitted to take it to meet a general education distributive requirement. Until the fall semester of 2013, it was configured as a three-hour per week lecture course with no hands-on lab component, and the department had no access to laboratory classroom facilities. For several of those years, the instructor incorporated 3–5 virtual laboratory experiences over the semester using one lecture hour for each. While students said they enjoyed these experiences, assessment data indicated that they still had persistent misconceptions about evolution at course completion.

In fall 2013, a project team at WCU, including the course instructor (a biological anthropologist), a human physiologist experienced in inquiry curricula, an evolutionary biologist, and a psychologist with expertise in assessment and program evaluation were awarded a three-year TUES (Transforming Undergraduate Education in STEM) grant from the National Science Foundation (NSF). The purpose of this award was to develop an innovative, inquiry-based laboratory curriculum targeting student misconceptions about evolution, student ability to use the scientific method, and student understanding of the investigative tools used by biological anthropologists. To accommodate this new curriculum, the course was redesigned to meet four hours per week in an integrated lecture-lab format, with roughly half of that time devoted to laboratory activities and the other half to lecture and/or discussion.

The project was submitted to the West Chester University Human Subjects Committee and received expedited approval in the summer 2013. Informed consent was obtained each semester from students enrolled in the course who wished to participate. Over the period of the project, this was all but one or two students.

During each lab period, brief instruction on methodology was provided, as appropriate to the lab, and students were presented with a challenge scenario that asked them to apply the scientific process to solving that problem using the relevant method (with the challenge scenario providing a structured context in which to do so). In a standard biological anthropology lab curriculum, students might be asked to describe and identify various casts of hominin fossil skulls using characteristics they had learned about, associate these traits with dietary differences, and receive verification of their assessments by the instructor. In the inquiry-based, structured challenge approach developed at WCU, students were given a problem to solve that required them to hypothesize the likely diet of the various hominins or hominids. They were instructed in a technique that allowed them to test one of their hypotheses, then required to state their results in an organized manner, evaluate them, indicate next steps, and so on. Thus, each lab in the curriculum is configured to (1) help students understand how biological anthropologists think about and explore problems using relevant techniques and (2) gain experience with the scientific process. The lab curriculum includes some instruction and application of basic molecular techniques (e.g., constructing simple primate phylogenies based on morphological v. genetic variation and doing a DNA fingerprinting exercise to attempt to identify a hypothetical hominin fossil), since the curriculum is also designed to help students make connections between phenotypic observations and the molecular level in service of the project goal of helping students to better understand evolution. Table 1 provides a list of the labs with descriptions of the inquiry learning activities performed.

The full lab manual can be accessed at: https://digitalcommons.wcupa.edu/anthrosoc_facpub/72 .

Standard assessments, including periodic exams and laboratory reports, were utilized to measure student learning. Responses to lab challenges at multiple time points were evaluated at the end of each semester using a rubric to measure individual students’ abilities to define the problem, to develop a plan to solve the problem, to analyze and present information, and to interpret findings and solve the challenge problem. Student lab teams also developed a project that they designed and implemented (from hypothesis to interpretation) using one of the methods they learned, and gave group presentations to the class. Other, more formative, measures of student learning were also introduced. For example, during each lab, students completed a pre-post assessment tool which was a modified version of the RSQC2 (Recall, Summarize, Question, Connect, and Comment) classroom assessment technique developed by Angelo and Cross ( 1993 ). Beginning in the second year of the project, pre- and post-lab clicker questions were incorporated for rapid assessment of the lab impact.

Several global surveys were administered at the beginning of each course, prior to any instruction, and again (for all but one survey) on the last day of the course. These included a survey focusing on evolution (17 items in year one, revised to 25 items in the second year) as well as surveys assessing students’ familiarity and comfort level with the scientific process, their level of motivation, and, at the end only, their overall assessment of their course experience. The evolution survey was also administered at WCU for 2 years prior to the course reorganization and lab implementation; data from this period are used for an internal comparison with survey results obtained during the implementation of the new curriculum. Biological anthropology colleagues at three other US universities (reported here as A, B, and C) also administered the evolution concepts survey to their students in introductory courses in biological anthropology, during the grant period, for comparison purposes. All of these courses were taught with some version of a more standard laboratory curriculum for this discipline (example of a standard approach described above). University ‘A’ is a large, midwestern state school (approximately 40,000 students); University ‘B’ is a sizable state school located in the south (approximately 30,000 students). University ‘C’ is a large, northeastern state school (approximately 30,000 students). At all three, introductory biological anthropology is taught in large lecture context with smaller recitation sections that meet one hour per week (i.e., two hours lecture, one hour of recitation or lab). At A and C, these recitations were used for weekly laboratory activities throughout the semester; at B, there were seven labs during the semester. Prior to 2013, the course at University A had no lab at all—only lecture.

The current report first describes the results of the evolution concepts instrument administered at the very beginning of the course and at the end of the course at WCU and across universities. Following a presentation of the results regarding changes in misconceptions we turn our attention to an examination of the specific areas of learning that we believe may have contributed to the reduction in misconceptions, including a look at specific assessments of students’ growing understanding of science as a process throughout the course.

Evolution misconceptions

Two versions of the evolution concepts instrument were used, one prior to the start of the grant period and throughout the first year following the grant award and a revised version used beginning in fall 2014. Each version included statements that students responded to on a 5-option Likert-type scale ranging from strongly agree to strongly disagree, or having no opinion. This instrument was based on a published and freely available tool used by other researchers (Cunningham and Wescott 2009 ). For purposes of analysis, each item was agreed by the project team to be either true or false, such that strong agreement with a true statement and strong disagreement with a false statement were considered to be ‘correct’ responses. A scale ranging from + 2 to − 2, including 0 for ‘no opinion’ was constructed, and several variables were computed from these scores, including total score (pre, post), percent of total points earned (pre, post), number of items correct (pre, post), and percent of items correct (pre, post). The use of percent variables was necessitated by a revision of the survey after the first year of curriculum implementation (2013–2014). The initial version of the survey included 24 items, but a qualitative analysis by study consultants resulted in a set of only 17 items deemed usable for the purposes of our study. This initial survey was then revised for use beginning in fall 2014 to include the 17 items kept from the original survey with the addition of 8 new items, resulting in a set of 25 usable items. The 25-question survey can be found in Additional file 1 .

Several questions were addressed using the results of the evolution concepts instrument. First, we compared WCU student survey responses to responses from the three other institutions whose students completed the survey. We asked if student performance on the evolution concepts instrument improved from pre- to post-course for all institutions and whether the amount of improvement varied by institution. Second, we examined WCU student survey responses (both pre and post surveys) over time, asking if student performance on the evolution concepts instrument improved both prior to and during the grant implementation period. Next, we asked whether the degree of improvement changed following implementation of our new inquiry-based curriculum, relative to the academic years prior to implementation of the grant. Finally, in an attempt to understand the specifics of what evolution-related misconceptions might have improved and which did not, we conducted a qualitative analysis of survey items and compared student performance on sets of related items across universities.

WCU course assessments

A variety of measures were used to assess student learning throughout each semester at WCU and to evaluate the effectiveness of particular pedagogical approaches as well as the overall curriculum. Some of these measures were objective and direct measures of student learning. Some were indirect measures, student perceptions of what they learned and/or which laboratory sessions they believed were most helpful in their learning. In this report, we provide results of four of these measures—in-class clicker questions, laboratory challenges, RSQC2 responses, and student confidence ratings—to provide insights about the effectiveness of the curriculum in meeting its primary objectives.

In-class clicker questions

Students were presented with a set of true/false statements or multiple choice questions at the beginning and end of multiple laboratory sessions. Some items were tied directly to misconceptions about evolution, others to students’ understanding of the scientific method, while others were designed to measure more general understanding of the topics covered by the individual laboratory modules. Students responded, via clickers, to these statements presented visually in class. Responses served as an important source of formative assessment but also provided information on the effectiveness of each of the laboratory modules in correcting student misconceptions about evolution and student understanding of the scientific method.

Laboratory challenges

Laboratory modules included “challenge” activities, designed specifically to enable students to apply problem-solving skills within a structured context (Knabb and Misquith 2006 ). In each of these laboratory challenges, students were asked to state research questions or generate hypotheses, collect data, draw conclusions, report/graph their results, and reflect on those results. Each student completed a laboratory worksheet during each lab module and all worksheets were submitted as part of student lab notebooks at the end of each semester. Selected lab worksheets were reviewed by faculty involved with the grant project at the end of each semester using a developmental assessment screening tool developed by all project faculty. This screening tool underwent its own developmental process, resulting in a final tool that included four measures of scientific thinking (i.e., students’ ability to use the scientific method): Defining the Problem, Developing a Plan to Assess the Problem, Analyzing and Presenting Information, and Interpreting Findings and Solving the Problem. Each of these four areas was assessed on a scale of four developmental levels: beginning, developing, appropriately developed, and exemplary. A copy of this scoring rubric can be found in Additional file 2 . Developmental changes in these four areas of scientific thinking were assessed by comparing assigned developmental levels following an early semester laboratory module with assigned developmental levels following a later semester laboratory module.

RSQC2 (Revised)

A modified version of the RSQC2 classroom assessment technique (Angelo and Cross 1993 ) was completed by students during each laboratory session. Complete details about the multiple sections of this activity can be found in Additional file 3 . For the current report, we present data on one of the sections completed by students at the end of each laboratory session. Students were asked to rate the usefulness of each laboratory session in reaching learning outcomes. Ratings were made on a 4-point Likert scale: 4 = very useful; 3 = somewhat useful; 2 = minimally useful; 1 = not useful. Questions included: How useful was today’s laboratory session in helping you to understand the important concepts of evolution and human variation discussed in this course and used by biological anthropologists? How useful was today’s laboratory session in helping you to understand the tools used by biological anthropologists to understand the concepts of evolution and human variation?

Student confidence in using scientific method

WCU students completed a 10-item survey at both the beginning and the end of each semester asking them to rate their level of confidence in their abilities and/or understanding of several pieces of the scientific process. All items were rated on a 5-point Likert scale: 1 = completely doubtful; 2 = somewhat doubtful; 3 = neutral; 4 = somewhat confident; 5 = strongly confident. A copy of this survey is available in Additional file 4 .

A variety of both univariate and multivariate linear model procedures were used to address questions of interest involving all student assessments, both within and across time periods and universities (where appropriate). Specifics regarding these analyses are discussed within the Results section.

Evolution misconceptions at WCU and other institutions

WCU evolution surveys were collected across all six semesters of the grant implementation period (fall 2013 through spring 2016), with a total of 105 complete survey sets (pre- and post-course). Survey responses from students at the three other universities were provided by institution instructors whenever possible: University A provided 469 complete survey sets across five terms; University B provided 273 complete survey sets across six terms; and University C provided 200 complete survey sets across three terms. Comparisons across universities were made across only the three terms for which data was provided by each university (fall 2014, spring 2015, and fall 2015). Figure  1 shows pre-course and post-course percent items correct at each university (WCU, University A, University B, and University C), collapsed across these three semesters.

Pre-course and post-course evolution concept survey ‘percent items answered correctly’ across 4 universities: WCU (n = 43); University A (n = 308); University B (n = 143); and University C (n = 200)

Significant change from pre- to post-course percent items correct was found within institutions for each of the three terms individually [as assessed after each term] and across all terms combined. Furthermore, significant change from pre- to post-course percent items correct was found across all three terms and 4 institutions, collapsed [t (693) = 25.762, p < 0.001]. Thus, significant improvement in overall performance on the evolution misconceptions instrument occurred at every institution and during each of the three terms considered here.

While there were no significant differences by term, institution, or term x institution in pre-course percent items correct, we did note a near significant effect of institution [F (3, 690) = 2.548, p < 0.10]. An informal review revealed that WCU pre-course scores were higher than pre-course percent items correct at all three other universities. Thus, comparison of post-course percent items correct included the pre-course percent items correct scores as a covariate. ANCOVA results support a significant effect of institution on post-course percent items correct, after controlling for pre-course percent items correct [F (3, 689) = 8.345, p < 0.001]. Post-hoc tests show significant differences between post-course scores at WCU and at all three other institutions. In addition, post-course percent items answered correctly at University B was significantly lower than percent items answered correctly at University C.

Internal WCU comparisons

The results reported above support statistically significant improvement in evolution misconception scores among students at all participating universities but further suggest that post-course scores are significantly higher at WCU than at any of the other three universities, even after controlling for potential differences in pre-course scores. WCU differs from these other institutions in terms of the curriculum focus (our inquiry-based approach versus other, more standard approaches), but WCU also differs from the other institutions in terms of class size. Individual class sections are smaller at WCU, resulting in smaller sample sizes both within and across semesters. If class size is the factor that explains the difference in post-course performance across universities, it should also be the case that post-course performance at WCU would not change following the introduction of the new inquiry-based curriculum. To evaluate this possibility, we compared WCU evolution survey results for pre-grant terms to evolution survey results following implementation of the inquiry-based curricular approach. Survey results are reported here for pre-grant (fall 2011 and fall 2012, N = 22 and 26, respectively), and grant implementation (fall 2013, spring 2014, fall 2014, spring 2015, fall 2015, and spring 2016; Ns = 18, 23, 12, 12, 19, and 21, respectively) (Fig.  2 ).

WCU pre- and post-course ‘percent items answered correctly’ by project phase: pre-grant (n = 48) and post-grant (n = 105)

There were no significant differences by term in pre-course percent items correct or post-course percent items correct during the pre-grant period (fall 2011 and fall 2012) or during the grant implementation period (fall 2013 through spring 2016). Significant change from pre- to post-course percent items correct was found across the pre-grant period [t (47) = 7.387, p < 0.001] and across the grant implementation period [t (104) = 14.871, p < 0.001]. Thus, significant improvement in performance on the evolution conceptions instrument was found both prior to and during the implementation of the grant. There were no significant differences in pre-course percent items correct between pre-grant and grant implementation periods [F (1, 151) = 2.145, p = 0.145]. But, a significant group difference was found in post-course percent items correct [F (1,151) = 5.600, p < 0.05], with students answering a larger percentage of items correctly (i.e., earning full 2 points) across the grant implementation period than during the pre-grant period.

Evolution concepts

The results reported above support the conclusion that our new laboratory curriculum may be more effective in improving student understanding of evolution and evolutionary concepts and may be more effective in reducing student misconceptions of evolution than the curriculums utilized at the other universities. In addition, significantly more WCU students answered certain survey items correctly at the post-course assessment than did students at any of the other three institutions (see Table 2 ), but a clear pattern was difficult to identify. Thus, we conducted a qualitative analysis of the 25 survey items that made up the revised version of the survey (the one implemented beginning fall 2014). We examined the survey results for the three terms for which data were available for all four institutions (fall 2014, spring 2015, fall 2015). This analysis resulted in four groups of items, each addressing one broad theme: (1) understanding of basic scientific evidence and the process of science (5 items); (2) understanding of evolution (from a general or “big picture” perspective) (7 items); (3) understanding of the mechanisms of evolution (i.e., natural selection, mutation, genetic drift, gene flow) (8 items); and (4) understanding of the evidence for evolution (5 items). Table 2 provides a list of all survey items and identifies which theme each item falls into.

A significant multivariate effect of institution was found when we included the four concept scores (i.e., percent of items within each concept grouping answered correctly) in a MANOVA procedure with both pre-course scores and post-course scores included as dependent variables. Univariate follow-up tests suggest a significant institution effect for Concepts #1, and #4. In both cases, pre-course scores were higher for WCU students than for students at other institutions. Thus, a set of Analysis of Covariance (ANCOVA) procedures were conducted, one for each set of post-course concept scores (i.e., percent of items within each concept grouping answered correctly at post-course time period), with institution included as a between-subjects factor and pre-course scores for that concept included as a covariate. Results suggest a significant institution effect for three of the four concepts (#1, #2, and #3). With regard to Concept #1 (understanding of basic scientific evidence and the process of science) post-hoc tests following an overall significant effect of institution [F (3,689) = 3.919, p < 0.05] show significantly higher post-course concept scores at WCU than at any of the other three institutions. A similar result was found for Concept #2 (understanding of evolution from a general/big picture perspective) [F (3,689) = 12.899, p < 0.001]. Again, post-course scores for WCU were significantly greater than those for the other three institutions. In addition, University A post-course scores were significantly greater than those for University B. A significant effect of institution was also found for Concept #3 (understanding of the mechanisms of evolution) [F (3,689) = 7.278, p < 0.001]. Post-hoc tests reveal that WCU post-course scores are significantly greater than those of University A and University B. WCU scores are higher than those of University C but that difference did not reach statistical significance. No significant effect of institution was found for Concept #4 scores (understanding of the evidence for evolution) [F (3,689) = 1.643, p = 0.178). But, despite the lack of an overall significant effect, WCU post-course scores are greater than those of the other institutions for this concept. Descriptive statistics for the concept scores across universities can be found in Additional file 5 .

How might this inquiry-based course have aided in the reduction of evolutionary misconceptions? In an attempt to gain insight about which course components or processes were effective in this regard, we examined student responses to in-class clicker questions about evolution concepts and scientific method , their development of scientific thinking skills over the term via lab worksheets, their perceptions about each lab’s effectiveness in helping them to learn about evolution and human variation concepts, and their confidence in using the scientific method. These results are presented below.

Clicker questions were developed over the course of the second year of the grant, then revised slightly for use across the final year of the grant (Fall 2015–Spring 2016). Questions were developed for eleven laboratory modules (see Table 1 ). Some items were included within each module to measure understanding of specific laboratory content. Items measuring evolution misconceptions were also included for all modules (1, 2, or 3 items). Items measuring scientific thinking (i.e., understanding of the scientific method) were included for only three modules (1 or 2 items): Evolution and Scientific Thinking, Primate Anatomy and Locomotion, and Human Osteology and Forensics. Clicker questions were presented at the beginning and at the end of each laboratory module session. Data for the final year of grant implementation are presented here. Complete data (across all laboratory modules) were available for 24 students across both semesters.

Overall student performance (as measured by % total items answered correctly) increased significantly from 78.64% at pre-module assessment to 91.06% at post-module assessment (across all items and all laboratory modules) [t (23) = 10.89, p < 0.001]. Performance also increased within each of the laboratory modules.

Student performance also increased significantly on the items specifically designed to measure previously identified misconceptions about evolution, with percent total items answered correctly across all laboratory modules increasing from 83.85% correct to 91.93% correct (across all items and all laboratory modules) [t (23) = 4.992, p < 0.001]. Given that evolutionary misconceptions were addressed most steadily during the early part of the semester, we examined the degree to which improvement on misconception items might be different across the semester. Table 3 shows measures of student performance on evolution misconception in-class clicker items during three time periods of the semester: Early Semester (3 modules focused on basic evolutionary concepts); Mid Semester (4 modules focused on non-human primates and human evolution); and Late Semester (4 modules focused on living human biology). While some slight improvement was noted across all time periods, the only period during which a statistically significant improvement occurred was the early semester time period.

Student performance on the items specifically designed to measure student understanding of the scientific method increased significantly from 90.00% to 97.50% (across all items and all three laboratory modules that included those items) [t (23) = 2.584, p < 0.05]. When broken down by individual laboratory module, the greatest improvement in student performance appears in the later modules but is only statistically significant in the Primate Locomotion module (see Table 4 ).

Two laboratory sessions (one early- and one mid-semester) were chosen for comparison: (1) the Evolution and Scientific Thinking laboratory module was chosen for the early-semester session; and (2) the Primate Anatomy and Locomotion module was chosen for the mid-semester session. The Evolution and Scientific Thinking laboratory module was the first laboratory module students participated in and occurred during week two of the semester. The Primate Anatomy and Locomotion session occurred at about week six of the semester. Four variables were scored from the laboratory worksheets of each of these sessions across the final two semesters of the grant implementation period, fall 2015–spring 2016: Defining the Problem; Developing a Plan to Solve the Problem; Analyzing and Presenting Information; and Interpreting Findings and Solving the Problem. All were rated on a scale of 1 to 4 (Beginning, Developing, Appropriately Developed, and Exemplary). Three faculty scorers worked together to determine final scores by consensus for each variable in each laboratory worksheet. Complete data were available for a total of 42 students across both semesters (21 each semester) (see Table 5 ).

Student responses to all items of the RSQC2 classroom assessment tool were collected across the final two semesters of the grant implementation period, fall 2015–spring 2016. As outlined earlier, students were asked to rate the usefulness of each laboratory session in helping them to understand (1) the important concepts of evolution and human variation discussed in the course, and (2) the tools used by biological anthropologists to understand the concepts of evolution and human variation. Students ranked each laboratory session, as it ended, on a 4-point scale, ranging from Not Useful to Very Useful, on each of these items. Table 6 lists the laboratory session topics and the percent of students who rated each one as “Very Useful” to their understanding of the important concepts of evolution and human variation. Table 7 lists the percent of students who rated each one as “Very Useful” to their understanding of the tools used by biological anthropologists (i.e., to their understanding of the scientific method as practiced by biological anthropologists). Some differences in student ratings across the two areas of understanding are apparent.

Student ratings of their confidence in using the scientific method are reported here for the pre-grant period (fall 2011 and fall 2012 combined), and the grant implementation period (fall 2013, spring 2014, fall 2014, spring 2015, fall 2015, and spring 2016 combined) (see Table 8 ). Student ratings increased from pre- to post-course during both time periods, but improvement was greater during the grant implementation period than during the pre-grant period.

The laboratory curriculum developed and evaluated at WCU increases students’ understanding of evolution in introductory biological anthropology compared with other institutions using more standard approaches. While students taking the evolution concepts survey demonstrated improved understanding of evolution at all of the schools that employed this instrument (WCU and comparisons) from the beginning to the end of each semester, WCU students demonstrated a greater increase in percent items answered correctly from pre- to post-course (see Fig.  1 ). Significantly more WCU students answered 18 (of 25) survey items correctly at the post-course assessment than did students at any of the other three institutions (see Table 2 ). Given that WCU class sizes are smaller than those at the three comparison universities, WCU student performance on the evolution survey before the new curriculum was implemented was compared with performance during the first three years of the new, grant-funded curriculum. Students taking the survey during the grant period answered a statistically greater percentage of items correct at the post-survey than students in the pre-grant period, with pre-survey response levels showing no significant difference across these two phases (see Fig.  2 ); class sizes were comparable across the entire time frame.

Thus, we demonstrate the impact on improved student understanding of evolution is related to the new curriculum itself. In the remaining discussion, we focus on the question of what aspects of the new curriculum may be contributing to this improvement, detailing how this curriculum incorporates all three of the key learning strategies outlined by Nelson ( 2008 ): (1) extensive use of active learning approaches; (2) focus on science as a process and way of knowing; and (3) identification and direct targeting of student misconceptions.

First, the WCU curriculum is inquiry-based, engaging students actively and directly with the process of “doing science”. Active learning (also known as student-centered learning) strategies, such as problem- or inquiry-based approaches, have been shown to be superior to instructor-centered approaches (e.g., lecture) in promoting student learning about evolution (e.g., Jensen and Finley 1996 ; Nehm and Reilly 2007 ). One of the stated learning goals of this course is to help students come to understand how biological anthropologists investigate questions. We strive to accomplish this by having them learn and actually use some of the tools scientists in this field employ—both at the ‘outward’ physical (e.g., skeletal, body shape and size, etc.) and molecular/biochemical levels (e.g., gene sequence readouts, DNA fingerprinting)—in a problem-solving context. Student lab teams receive a challenge scenario and have to come up with a methodological approach (usually using techniques they have just learned, and occasionally employing techniques learned earlier in the course), collect data, and then interpret those data—in every lab. This is fundamentally different than the typical approach in an introductory biological laboratory setting, such as those used in the comparison institutions and described earlier in this paper.

We think that this bi-level approach to teaching and using relevant methods in problem-solving helps students connect the evidence for evolution and human variation with the underlying molecular basis of that variation and change over time. Student ratings of each lab on the RSQC2 question pertaining to effectiveness in helping them to learn concepts of evolution and human variation were highest for Tree-Building and Primate Classification and DNA Fingerprinting (Table 6 ). We think it telling that both of these labs involve genetic as well as phenotypic variation linked with evolution. Ratings for the question concerning lab effectiveness in helping students to learn to use the tools biological anthropologists employ to understand evolution and human variation were highest for Forensics 2: DNA Fingerprinting, followed by Human Variation: Anthropometry, Human Genetic Adaptation: ELISA, and the Tree-Building and Primate Classification labs (see Table 7 ); all but the anthropometry lab address directly both genetic/biochemical and physical traits.

Second, the WCU curriculum focuses on the scientific way of knowing and the scientific process from the first week, in both lecture and lab contexts. The first topic after the students are introduced to the discipline is the nature of science: how science seeks to understand phenomena, the meaning of ‘fact’, ‘hypothesis’, and ‘theory’ in a scientific inquiry, and how the scientific approach to understanding natural phenomena differs from others. The first lab, which occurs early in the second week, then provides an opportunity for students to try out the scientific method and to learn, in context, about generating hypotheses, developing methods, collecting data, and interpreting those observations. They also learn about bias caused by preconceptions, measurement error, and different approaches to understanding the world (e.g., science and religion). Each lab module thereafter requires students to methodically think through and structure their work using the standard methodological sequence: question/hypothesis, explication of methods, data collection and reporting, discussion, and interpretation (see Table 1 ). Further examples of how the process of science is addressed in the curriculum are described below in the discussion about addressing evolution misconceptions.

The effectiveness of this approach is supported by the qualitative evolution concepts analysis that we undertook to look for thematic patterns in the evolution survey statements (see Table 2 and associated text). Three broad concepts showed a significant effect of institution, with WCU student post-course scores being higher than those at the other institutions; the first of these was understanding of basic scientific evidence and the process of science. The in-class clicker data we analyzed (see Table 4 ) support the idea that students gained knowledge about the scientific method during lab classes. Analysis of the change in student performance on lab challenges relevant to steps of the scientific process from early to mid-semester (see Table 5 ) also supports improved student ability to develop a plan to solve the problem (Methods) and to analyze and present information (Results) from the early time point to the later one. Additionally, students’ report of their confidence in using the scientific method (see Table 8 ) indicated greater improvement from pre- to post-course during the grant implementation period than during the pre-grant period at WCU. Firsthand experience with the scientific method and opportunities to ‘think like a scientist’ have been linked with improved ability of students to understand and accept evolution (see, e.g., Pittinsky 2015 ; DeSantis 2009 ; Robbins and Roy 2007 ; Nelson 2008 ).

Third, the WCU curriculum is designed to identify and directly address student misconceptions about evolution, and it does so from early in the course (Nelson 2008 ). Students take the evolution concepts survey on the first day of class, before any instruction about evolution. This provides a baseline of their understanding, and the concepts included in the survey are among those that the curriculum proceeds to address. The order of the labs over the semester (Table 1 ) ensures that basic concepts of evolutionary theory and mechanisms, genetics, and classification/phylogeny are covered early. As part of this attention to foundational ideas, class discussions during and at the end of labs include a focus on misconceptions about evolution and, indeed, about how scientific inquiry is conducted. For example, in the Evolution and Scientific Thinking lab (the first one), students nearly always assume the male skeleton will be the taller of the two—whether or not they overtly state that as a hypothesis. This and other ideas that students mention lead to a discussion of assumption bias and how we try to avoid that in the process of “doing” science. This is followed by a dialogue (sometimes precipitated by a student-expressed view, but more often introduced by the instructor as a story) focused on the idea some people hold that the male should have one less rib than the female. We talk through whether this is a scientific hypothesis (yes, because it can be tested); how they would test it (go count the ribs); what kind of evolution mechanism this idea reflects (Lamarkism, i.e., inheritance of acquired characteristics); and what genetic assumption is also being made (that rib number is sex-linked). We also tell students that, in reality, there is a range of variation in number of rib pairs in humans. In fact, the male skeleton is shorter than the female, and this fact also fosters a framework in which to look at what kinds of factors may affect variation in height in humans, besides sex (e.g., population or individual ancestry, various environmental influences, age). In the Tree Building and Primate Classification two-part lab, we address directly the relationship among monkeys, apes, and humans. At the outset, most students think that monkeys and apes are more closely related evolutionarily than either group is to humans; this is also typically how they interpret the anatomic evidence of the comparative skulls and build their initial trees. However, when they do the counts of pairwise differences in the gene sequence for the three primate groups, they come to understand that the genetic evidence is indicating that apes and humans are more closely related than either group is to monkeys. The discussion in this lab is also focused on the conduct of science inquiry (e.g., can we say a hypothesis is “proven” based on one gene sequence or a limited set of anatomic traits?) and evolution misconceptions (e.g., that extant species differ from each other in “how evolved” or better adapted they are, based on body size or some other assumption).

In addition, we assess student understanding about common misconceptions in all labs directly via some of the in-class clicker questions administered as a formative assessment at the beginning and end of each lab module. Use of clickers allows us to assess immediately, at the conclusion of a lab module, how well students grasped the key concepts and techniques on which the lab was based, including evolution concepts. In the data presented in this paper, scores on evolution concept clicker questions improved significantly in the early lab modules analyzed as a group compared with mid-semester and later semester groupings of lab modules (see Table 3 ). In the later phases, the baseline (pre-lab) scores were higher, reflecting student mastery of evolution concepts generally over course duration. Finally, evolution misconceptions were also addressed in ‘lecture’ class discussions as well as queried on exams. In other words, the focus on correcting misconceptions occurred at multiple levels and time points in the course.

The kind of repetition and reinforcement that we describe here has been termed “spaced practice” or “varied practice” and is documented as improving student conceptual learning (Brown et al. 2014 ; Cepeda et al. 2006 ; Lang 2016 ). Spaced practice improves learning for a variety of reasons and in a variety of ways, but one thing that spaced practice supports is long-term consolidation of information; practice over time and in various forms allows for the connection of new information to existing knowledge and for the strengthening of memory traces over time (Brown et al. 2014 ; Cepeda et al. 2006 ; Goode et al. 2008 ; Moulton et al. 2006 ). We think that reinforcing on a weekly basis both the scientific method and correct general and specific concepts about evolution (including the mechanisms of evolution) represents this kind of spaced and varied practice and may well be contributing to the comparative success of this curriculum. The close integration of lecture and lab is likely also a factor.

Following the project, the course instructor, in consultation with the project team, made a number of changes to the curriculum based on the promising findings described above. The steps of the scientific method were more explicitly built into all of the lab worksheets, for emphasis. Opportunities to emphasize key evolution concepts within particular labs were enhanced during post-lab discussions. Clicker questions were revised to incorporate more statements reflecting science process and understanding, as well as additional repetitions of evolution concepts (with altered wording each time). Eventually, two new labs were developed related to human physiological adaptability. The first of these was added in spring of 2017 and focused on blood pressure response to stress; this lab, done late in the semester, then became the basis for the students’ final group project (instead of the population ancestry lab). After the students conduct a pro-forma experiment assessing cardiovascular response to a stressor using the blood pressure sensor and software, they design and conduct their own experiments, which they then present orally the following week. In fall 2017, a second physiology lab was added in the first half of the course, focused on skin temperature response to cold, and provided another, and earlier, opportunity for students to develop their own experiments once they learned the technique, with an emphasis at this early stage on hypothesizing. Students present these first ‘mini’ projects briefly (focusing on hypothesis and results) the following week. We felt that it was important to provide students with two experiences that allow them to ask and answer research questions of their own, under guidance. In fall 2017 the course topic order was also altered, bringing most of the human biology material previously covered at the end (biological variability and adaptation) into the sequence immediately after evolutionary theory and genetics—thus the relevance of a temperature adaptability lab in week 5.

Conclusions and suggestions

The student-centered biological anthropology laboratory curriculum developed at WCU is more effective at helping students to understand general and specific concepts about evolution than are more traditional curricula. We argue here that this is not just a function of small class size, but is directly related to the inquiry-based approach used in the labs, the emphasis on knowledge of science and practice applying the scientific method regularly, the very intentional confronting of misconceptions about evolution starting early in the course, and the structure that allows for ‘spaced practice’, i.e., continual reinforcement of correct concepts about evolution and human variation. Inquiry-based approaches can be incorporated in lab sections of otherwise large lecture courses (Casotti et al. 2008 ) or as small-group activities within lecture-only science courses. Evidence suggests that these student-centered approaches also work well for diverse learners (Tuan et al. 2005 ).

We encourage instructors of introductory biological anthropology and other life science courses to incorporate these key elements in their curricula to support improved student understanding about science process and evolution. Three general suggestions that might be applied fairly readily based on our study would be: (1) assess students’ level of understanding of evolution and how science proceeds right at the beginning of the course or relevant unit, and again at the end—to take stock of the impact of the curriculum on student learning; (2) provide hands-on problem-solving opportunities, such as case studies, guided challenges, or self-designed experiments, that iteratively emphasize scientific method and correct understanding of evolution; (3) use human examples where possible, and look for opportunities to help students connect the phenotypic changes reflecting evolution with the underlying genetic changes. The WCU curriculum is freely available to those who are interested in more detail or who may wish to adapt and incorporate components of what we have discussed here in their own courses—e.g., specific labs, etc.—at the following link ( https://digitalcommons.wcupa.edu/anthrosoc_facpub/72 ); inquiries or requests for additional information may be sent directly to the first author.

Availability of data and materials

The lab manual can be accessed at the open source link: https://digitalcommons.wcupa.edu/anthrosoc_facpub/72 . Other materials can be obtained from the first author on request.

Abbreviations

West Chester University

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Acknowledgements

The support of the (then) College of Arts and Sciences and its dean, the Provost, and the Office of Sponsored Research and Faculty Development of West Chester University are gratefully acknowledged. In addition, the authors would like to acknowledge the support and counsel of the three external advisors on the project, all biological anthropologists teaching at the three other universities that provided evolution survey comparative data.

This project was supported by an NSF TUES Award (DUE-1245013) and West Chester University.

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Susan L. Johnston, Maureen Knabb, Josh R. Auld & Loretta Rieser-Danner

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SLJ, MK, and JA designed the curriculum. SLJ is the instructor of record for the course and was responsible for obtaining informed consent and for implementing the curriculum. LR-D served as the project evaluator and conducted all analyses. All authors read and approved the final manuscript.

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SLJ is a biological anthropologist and Professor of Anthropology (Department of Anthropology and Sociology); MK is a physiologist and Emeritus Professor of Biology (Department of Biology); JA is an evolutionary biologist and Professor of Biology (Department of Biology); and LR-D is Professor of Psychology (Department of Psychology).

All are affiliated with West Chester University, West Chester, PA, 19383, USA.

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Supplementary Information

Additional file 1..

Revised version of the evolution survey that includes 25 items; administered at WCU and three other universities from Fall 2014 on.

Additional file 2.

Rubric used to review student laboratory worksheets. Includes 4 measures of scientific thinking (defining the problem, developing a plan to assess the problem, analyzing and presenting information, and interpretating findings and solving the problem), with each assessed on a scale of 4 developmental levels (beginning, developing, appropriately developed, and exemplary).

Additional file 3.

A modified version of the RSQC2 classroom assessment technique (Angelo and Cross, 1993 ), completed by students during and after each laboratory module.

Additional file 4.

A 10-item survey completed by WCU students at both the beginning and the end of each semester asking them to rate their level of confidence in their abilities and/or understanding of several pieces of the scientific process. All items were rated on a 5-point Likert scale: 1 = completely doubtful; 2 = somewhat doubtful; 3 = neutral; 4 = somewhat confident; 5 = strongly confident.

Additional file 5.

Evolution survey, concept scores: descriptive statistics by institution

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Johnston, S.L., Knabb, M., Auld, J.R. et al. Correcting misconceptions about evolution: an innovative, inquiry-based introductory biological anthropology laboratory course improves understanding of evolution compared to instructor-centered courses. Evo Edu Outreach 15 , 6 (2022). https://doi.org/10.1186/s12052-022-00164-4

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Evolutionary Theory: a Hierarchical Perspective. — Edited by Niles Eldredge, Telmo Pievani, Emanuele Serrelli, and Ilya Tëmkin, 2016. vii+385 pp. Chicago: Chicago University Press. ISBN 978-0-226-42605-1 $US105 (hardcover). ISBN 978-0-226-42622-8 $US35 (paperback). ISBN 978-0-226-42619-8 $US35 (e...

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MUTATIONS VERSUS SUBSTITUTIONS

It is important to note that, in this article, we will only be considering de novo point mutations. We will not discuss large insertions or deletions or horizontal gene transfer events. To proceed, we must define some terms.

For the purpose of this article, we will define “DNA mutations” as single nucleotide changes in the DNA sequence of an individual organism. These will be the end result of the molecular DNA change, and of the fact that this DNA change was not repaired by the cellular repair systems. Once a mutation occurs and is present within an individual, it will either increase in frequency within the population, or will vanish from the population. The ultimate fate of mutations depends on a combination of natural selection and stochastic forces, such as genetic drift.

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Different types of mutations (represented by differently colored arrows) occur at different frequencies (represented by arrow thickness). Selection acts as a sieve and allows only a subset of these mutations to persist and become the differences we see between genomes. Such differences are referred to as substitutions. Various types of mutations have different fitness effect distributions, and will be differently affected by selection. ( A ) Under normal levels of selection, selection will introduce its own biases into patterns of variation. Thus, biases in the patterns of observable substitutions between genomes are likely not to reflect mutational biases. ( B ) When selection is extremely relaxed, it is expected to affect patterns of variation to a much lesser extent, because it will affect only mutations with very high-fitness effects. Under such conditions, observed substitutions between genomes approximate a random sample of the mutations that have occurred. Because of this, when selection is relaxed, biases in the patterns of substitutions observed between genomes will better approximate mutational biases.

We will define a phenotypic, or marker mutation, as a phenotypic change occurring in an individual. For example, an antibiotic resistance phenotypic mutation causes an individual bacterium to become resistant to an antibiotic. Similarly, we can define a phenotypic, or marker substitution, as a phenotypic change we are able to observe, for example, an increase in the frequency of resistant mutants within a bacterial population. Such an increase can occur because the resistance mutation occurs more frequently or because of natural selection favoring the resistant mutant.

Often, mutation is studied by assuming that certain types of DNA mutations (e.g., synonymous mutations) or certain marker mutations (e.g., antibiotic resistance mutations when a bacterium is not exposed to antibiotics) evolve entirely neutrally. If there is absolutely no selection acting on an observed class of substitutions, their patterns and rates will indeed be a derivative of the patterns and rates of mutation. However, as we will see later in this article, it is rare to find cases in which DNA or marker mutations are totally unaffected by selection. Determining mutational patterns and rates is therefore a tricky business that requires one to find creative ways to eliminate or minimize the effects of natural selection on observed substitutions.

LURIA AND DELBRUCK—ESTIMATING MUTATION RATES CAN BE A NOISY BUSINESS

In their seminal 1943 “fluctuation experiments,” Luria and Delbruck showed that even if mutational markers truly did evolve neutrally, estimates of mutation rates based on such markers would be extremely noisy ( Luria and Delbruck 1943 ). Luria and Delbruck were attempting to understand the following phenomenon. When a pure bacterial culture is exposed to a bacteriophage, the culture will disappear because of destruction of cells sensitive to the virus. After further incubation, the culture will often become turbid again because of growth of a variant that is resistant to the phage. Once the variant is isolated, it often remains resistant even if it is cultured for many generations in the absence of any phage. At the time Luria and Delbruck were considering this problem, very little was known about the molecular mechanisms of mutation. Yet, they already understood that such a phenomenon could either occur because of resistance mutations occurring before the viral challenge, or because a certain proportion of sensitive cells somehow acquire resistance once they are exposed to phage ( Luria and Delbruck 1943 ).

Luria and Delbruck modeled the variance expected in the number of resistant mutants under both these scenarios ( Luria and Delbruck 1943 ). Their models showed that a much higher variance would be expected if the emergence of resistance were caused by mutations occurring before exposure to viruses. If mutation is a Poisson process and if mutations occur after and in response to viral exposure, one would expect the number of resistant mutants following exposure to be distributed around a certain mean, with the variance equal to the mean (a known characteristic of the Poisson distribution). If, however, mutations occur before exposure, they can occur in any generation of growth. Mutations occurring in earlier generations will rise to higher frequencies by the end of an experiment, compared with mutations occurring in later generations. Therefore, the number of resistant mutants at the end of an experiment will depend not only on the number of mutations that have occurred, but also on when these mutations occurred. This should greatly enhance the variance in the numbers of resistant mutants observed between different experiments. Indeed, Luria and Delbruck then went on to show that in different experiments they saw a variance that was much higher than the mean number of resistant mutants. This provided the first ever demonstration that mutations occurred before selection for their outcome ( Luria and Delbruck 1943 ).

In addition to showing for the first time that mutation precedes selection, the Luria and Delbruck study also shed light on the great variance in substitution rates one can expect to observe when considering phenotypic markers ( Luria and Delbruck 1943 ). First, as mentioned above, they showed that the variance in marker substitution frequency was expected to be much higher than the mean marker substitution frequency. Second, Luria and Delbruck found that the mean substitution frequency they estimated by simply averaging substitution frequencies across different experiments was much higher than the substitution frequency estimated by assuming a Poisson distribution and considering the number of experiments in which no resistance substitutions were observed. This exemplifies the strong effect mutations occurring early on in the experiment can have on calculated average mutation frequencies. One or a few experiments in which a relatively high number of mutations occurred early on, may greatly skew the estimated average frequency of mutations upward. Thus, estimates of mutation frequencies and rates obtained by using marker substitutions can often be very noisy ( Luria and Delbruck 1943 ). Fortunately, we can now, in many cases, move away from using markers and rather use whole-genome sequencing to study mutation.

METHODS FOR ELIMINATING THE EFFECTS OF NATURAL SELECTION WHEN STUDYING MUTATION

To be able to study different parameters of the mutational process, we must be able to disentangle mutation from the effects of natural selection. The easiest way of accomplishing this is by focusing on scenarios in which selection is expected to have less of an effect on patterns of substitution ( Fig. 1 ). A number of studies have used pseudogenes to study mutational biases (e.g., see Andersson and Andersson 1999 ; Nachman and Crowell 2000 ). Such studies assume that sequence variation within pseudogenes is unaffected by selection, because pseudogenes are no longer under selection to maintain function. Therefore, it is assumed that patterns of sequence variation within pseudogenes will be determined solely by mutation. Although useful, this approach has limitations. For one, although pseudogenes should not be under selection stemming from protein function, they may be under selection owing to genome-wide factors. For example, if there is selection to maintain a certain genomic nucleotide content ( Hershberg and Petrov 2010 ; Hildebrand et al. 2010 ), it might affect pseudogenes as strongly as it does other sequences. Second, for most microbial genomes, we can only identify a very small number of pseudogenes, because bacterial pseudogenes tend to be lost very quickly ( Kuo and Ochman 2010 ).

A second approach is to focus on evolutionary scenarios in which the efficiency of selection is reduced across the entire genome ( Fig. 1 ). Such genome-wide relaxations of selection can be the result of either close relatedness ( Akashi 1995 ; Messer 2009 ) and/or small effective population sizes ( N e ) ( Lynch 2007 ). Bacterial lineages exist for which genetic variation between members of the lineage has naturally been only weakly affected by selection, probably caused by a combination of close relatedness and small N e ( Hershberg et al. 2008 ; Holt et al. 2008 ; Hershberg and Petrov 2010 ; Lieberman et al. 2011 ). Large quantities of genomic data from many members of several such lineages are publicly available. Patterns of sequence variation between members of bacterial lineages evolving under relaxed selection can be used to characterize mutational patterns ( Fig. 1 ).

The efficiency of selection can also be artificially reduced in the laboratory through repeated single-cell bottlenecking of growing bacterial populations, which severely reduces N e . Such experiments are called mutation accumulation (MA) experiments ( Elena and Lenski 2003 ; Lind and Andersson 2008 ; Brockhurst et al. 2010 ). It is now possible to follow up MA experiments with whole-genome sequencing of the ancestor strain and its resulting progeny, thus allowing for the genome-wide identification of the MA mutations. The number of generations a bacterial population underwent during an MA experiment can be easily estimated. MA experiments therefore make it possible to estimate not only the relative rates with which different classes of mutations occur, but also the overall, absolute mutation rates. This is a clear advantage of MA experiments over approaches that rely on sequencing data from naturally evolving bacteria, which cannot be used to estimate absolute mutation rates. At the same time, MA experiments are much more labor intensive. It is also important to note that the mutation rates and patterns estimated through MA experiments may be influenced by the conditions under which these experiments are performed. This is a particular concern if mutation rates and patterns change under different growth conditions. For example, the stress-induced mutagenesis theory suggests that mutation rates could be much higher during stationary phase (reviewed in Galhardo et al. 2007 , and discussed in depth later in this review).

ABSOLUTE/OVERALL RATES OF MUTATION

One of the key parameters of the mutational process is the absolute rate with which mutations happen, on average, across all types of mutations and along the entire genome. In 1991, based on data collected by using a combination of fluctuation and MA experiments, and quantifying mutation rates based on the frequency of marker substitutions, John Drake coined “Drake’s rule” ( Drake 1991 ). According to this rule, per nucleotide point mutation rates inversely correlate with genome size in microbes. As a result, genome-wide mutation rates are an approximate constant of ∼0.003-point mutations per genome per generation ( Drake 1991 ). These results were based on mutation rates of only seven microbes, but later results from many additional microbes provided further support for Drake’s rule, particularly in prokaryotes and in double-stranded DNA (dsDNA) viruses ( Lynch 2010 ). Drake argued that such a fine-tuned mutation rate must be an evolved trait ( Drake 1991 ).

It is generally accepted that natural selection favors the lowering of mutation rates, as mutations are mostly deleterious ( Kimura 1967 ; Drake 1991 ; Dawson 1998 ; Lynch 2010 ). Drake and others postulated that reducing mutation rates comes at a certain physiological cost ( Kimura 1967 ; Drake 1991 ; Dawson 1998 ). Drake suggested that mutation rates reached equilibrium when the benefit of further lowering mutation rates matched the physiological cost of so doing. In other words, according to Drake, natural selection drives both the reduction in mutation rates, as well as the ultimate tapering off of this reduction. In contrast, Michael Lynch suggested an alternative model under which the lower limit on mutation rates is not set by natural selection on physiological cost, but rather by genetic drift ( Lynch 2010 ). As per-base mutation rates become lower, selection to further reduce mutation rates becomes weaker, until a point is reached in which selection is no longer strong enough to counteract the action of genetic drift ( Lynch 2010 ). Supporting this model, Lynch was able to show that per-base mutation rates inversely correlated with effective population sizes ( N e ) in both prokaryotes and eukaryotes ( Lynch 2010 ; Sung et al. 2012 ). Because N e is inversely related to the power of drift, it can therefore be said that mutation rates become higher as the power of drift relative to selection becomes stronger, congruent with Lynch’s model.

Lynch later refined his “drift-barrier” model by showing that the regression of the mutation rates versus N e is elevated for prokaryotes compared with eukaryotes ( Sung et al. 2012 ). This finding suggested that, for a given N e , selection is less effective at reducing mutation rates in prokaryotes. To explain this phenomenon, Lynch suggested that the magnitude of selection to reduce mutation rates is not just a function of the per-base mutation rate, but rather also of the genome-wide deleterious mutation potential of the genome ( Sung et al. 2012 ). Prokaryotes that tend to have less coding sequences in total, provide a smaller target for the origin of deleterious mutations than eukaryotic genomes. Under this refined model, the strength of selection to reduce per nucleotide mutation rates will scale positively with what Lynch defined as the effective genome size, which he approximated as the sum of coding DNA within a genome. Fitting with this, Lynch observed that the effective genome-wide mutation rate, calculated as the per-site mutation rate multiplied by the effective genome size, inversely correlated with N e , in a way that did not depend on whether an organism is a prokaryote or a eukaryote ( Sung et al. 2012 ).

Under both Drake’s and Lynch’s models, the cost of deleterious mutations is what drives mutation rates down ( Drake 1991 ; Lynch 2010 ; Sung et al. 2012 ). Therefore, under both models, an increase in the average cost of mutations would lead to a decrease in mutation rates. To examine this, Drake examined mutation rates of thermophiles and compared them to those of mesophiles ( Drake 2009 ). The rationale was that many mutations that are tolerated at the standard growth temperature are highly harmful when temperatures are higher. Thus, more mutations will have a fitness cost in thermophiles than in mesophiles, which should lead to lower mutation rates within thermophiles ( Drake 2009 ). By again using data derived by use of marker substitutions, Drake then showed that mutation rates in two different thermophilic microbes were indeed much lower than in mesophilic microbes and phages ( Drake 2009 ). This seems to support the model under which selection favors lowering of mutation rates, because of the deleterious effects of mutations.

Recently, many studies have been conducted in which MA lines from various microbes were fully sequenced to determine mutation rates (e.g., Lind and Andersson 2008 ; Lee et al. 2012 ; Sung et al. 2012 ). As discussed above, measures of mutation rates from whole-genome sequencing are expected to be more precise than those measured via the use of phenotypic markers. These recent studies have shown that although the Drake rule seems to generally apply in prokaryotes and dsDNA phages, the range of per genome mutation rates appears to be higher than originally postulated by Drake. For example, Lee et al. (2012) estimated mutation rates for a wild-type Escherichia coli laboratory strain, based on whole-genome sequencing of 59 MA lines. Based on these data, they estimated a mutation rate of ∼0.001 mutations per genome per generation (lower than the 0.003 constant suggested by Drake) ( Lee et al. 2012 ). Sung et al. (2012) sequenced MA lines of one of the smallest culturable bacteria, Mesoplasma florum , and found a genome-wide mutation rate of 0.008.

MUTATIONAL BIASES

Various types of mutations may occur at different rates. Such consistent variation in the rates of different categories of mutations means that the mutational process in itself, even in the absence of any natural selection, may introduce biases into patterns of genetic variation. Characterizing these biases is important for understanding which biases in patterns of genetic variation are selected and thus functionally important, and which may just be introduced by the mutational process.

Adenine-Thymine (AT) Bias of Mutation and Bacterial Nucleotide Content Variation

Bacterial nucleotide content is extremely variable. Some bacteria have guanine-cytosine (GC) content <25%, whereas the GC content of other bacteria can reach 75%. This variation was for a very long time considered to be entirely neutral, and the result of extreme variation in mutational biases between different bacteria ( Sueoka 1962 ; Muto and Osawa 1987 ). It was thought that GC-rich bacteria were simply ones in which AT to GC mutations occurred more frequently than GC to AT mutations. The opposite pattern of mutation was thought to occur in AT-rich bacteria ( Sueoka 1962 ; Muto and Osawa 1987 ). However, it was more recently shown, using data from bacteria evolving under varying degrees of relaxed selection, that mutation is universally AT biased across both AT-rich and GC-rich bacteria ( Balbi et al. 2009 ; Hershberg and Petrov 2010 ; Hildebrand et al. 2010 ). Given that mutation is always AT biased, some other force must be driving elevated GC content in bacteria with intermediate to high GC content. The most obvious culprit is natural selection, favoring such higher GC content, but other nonselective mechanisms could also be involved.

One nonselective mechanism that may be driving GC content up in bacteria with intermediate to high GC content, is biased gene conversion (BGC) (reviewed in Duret and Galtier 2009 ). It has been shown that gene conversion is GC biased in many eukaryotes, including humans and other mammals. In other words, the probability of a GC allele to be passed on to the next generation through gene conversion is higher in these eukaryotes than that of an AT allele. As a result of such BGC, in these eukaryotes, regions with lower recombination rates tend to be more AT rich, whereas regions undergoing more recombination will tend to be more GC rich ( Fullerton et al. 2001 ). A relationship between levels of recombination and GC content was also demonstrated for many bacteria, suggesting that BGC, or a mechanism similar to BGC, may affect nucleotide content in bacteria in a similar manner ( Touchon et al. 2009 ; Lassalle et al. 2015 ).

A second nonselective mechanism that may be increasing GC content in bacteria relates to mismatch-repair (MMR) systems. Lee et al. (2012) conducted MA experiments on both wild-type E. coli and mutants deficient in MMR. They found that although mutation was indeed AT biased in wild-type E. coli , it was GC biased in the absence of MMR. This suggests that the nucleotide content of genomes might be influenced by how well their MMR systems function ( Lee et al. 2012 ). Nucleotide content is a slowly evolving trait, because many substitutions need to occur for genome-wide patterns of nucleotide content to substantially change. Therefore, the nucleotide content of a bacterium may not be influenced solely by its current MMR functionality. Rather, MMR function during the evolution of the lineage to which the bacterium belongs may influence its current GC content. Fitting with this, it has been shown that the relationship between the nucleotide content of a bacterium and the current presence of MMR genes within its genome is not a straightforward one ( Garcia-Gonzalez et al. 2012 ).

When it comes to selection affecting nucleotide content, the first big question that arises concerns the nature of selection. If indeed natural selection favors higher GC content in some bacteria, why? What is the advantage conferred on these bacteria by having higher genome-wide GC content? The currently available answers to this question are far from complete.

A study that examined metagenomic samples collected from aquatic and soil environments, was successful in demonstrating that soil bacteria are substantially more GC rich than aquatic bacteria, even when differences in phylogeny are accounted for ( Foerstner et al. 2005 ). These results suggest that environmental selection plays a role in determining nucleotide content. The study in question was performed in 2005 when metagenomic data were only starting to become available, and used samples from only four different environments ( Foerstner et al. 2005 ). A more recent study used a much larger collection of 183 metagenomic data sets, extracted from 14 environment types, to investigate the effects of environment on nucleotide composition ( Reichenberger et al. 2015 ). This study supported the results of the smaller scale metagenomic analysis and demonstrated that environment affects microbial nucleotide content in a manner that cannot be entirely explained by differences in phylogenetic composition. Intriguingly, the data used in the more recent study made it possible to show that environmental factors drive changes in nucleotide content, not only between highly diverged environment types (e.g., soil vs. aquatic), but also between samples extracted from the guts of different human subjects ( Reichenberger et al. 2015 ). These results imply that the environmental factors that select for certain nucleotide compositions may be quite subtle.

The most obvious reason selection would favor high GC content in some bacteria is that higher GC content may provide better genome stability when temperatures are elevated. Many studies have attempted to investigate the correlation between GC content and optimal growth temperatures, with mixed results ( Galtier and Lobry 1997 ; Lobry 1997 ; Hurst and Merchant 2001 ; Marashi and Ghalanbor 2004 ; Musto et al. 2004 , 2006 ; Wang et al. 2006 ). In the end, it is very possible that growth temperature does affect nucleotide content. However, high growth temperatures are likely not the only environmental factors affecting nucleotide content, and they likely do not explain why so many bacteria have high or intermediate GC content in the face of universally AT-biased mutation.

Recently, Raghavan et al. (2012) have suggested an alternative force selecting for elevated GC content related to gene expression. Raghavan et al. inserted a plasmid containing the green florescent protein (GFP) gene into strains of E. coli . They generated their GFP genes to differ in the GC content of their synonymous sites. This allowed them to show that strains harboring a more GC-rich GFP gene grew faster than strains harboring a more AT-rich version of the gene, in a manner that depended on the construct being expressed, at both the mRNA and protein levels ( Raghavan et al. 2012 ). They then showed that this effect was not limited to the GFP gene but also occurred when other genes were so inserted into E. coli ( Raghavan et al. 2012 ). This finding fits the observation that bacteria with intermediate to high GC content tend use GC-rich optimal codons ( Hershberg and Petrov 2009 )—a trend that results in a much higher GC content of protein-coding synonymous sites, compared with noncoding intergenic sequences, within GC-intermediate and GC-rich genomes ( Hershberg and Petrov 2009 , 2012 ; Raghavan et al. 2012 ). If indeed GC-rich coding sequences are expressed more efficiently and/or accurately, selection may indeed drive GC content up in coding sequences. However, this suggested mechanism does not explain why intergenic, noncoding regions also have higher GC content than expected at mutational equilibrium in genomes with intermediate to high GC content ( Hershberg and Petrov 2010 ). Thus, although selection for genes to be more GC rich may contribute to elevated GC content, it cannot explain them in their entirety.

A second question that arises when considering natural selection acting on nucleotide composition is the question of how such selection would work. A problem arises because each individual base mutation only minutely alters overall nucleotide content, and an enormous number of mutations are needed to have any significant effect on overall nucleotide content. If so, how can selection on GC content affect each individual mutation? Additionally, if selection were to affect each mutation, the associated genetic load would be staggering. A possible solution to this conundrum is that natural selection may not act on individual mutations. Rather if there is selection in favor of elevated GC content and there is a nonselective mechanism, such as BGC, that elevates GC content ( Duret and Galtier 2009 ), it is possible that strong selection will exist on that mechanism. For example, if indeed BGC affects nucleotide content in some bacteria, as has been shown for eukaryotes ( Duret and Galtier 2009 ), bacteria that lose the ability to carry out BGC may gradually become more AT rich. Once their GC content becomes low enough to be disfavored by natural selection, these bacteria will be removed from the population. In this example, it is not each GC to AT mutation that is affected by selection, but rather the mutational event that leads to the loss of BGC. This is currently just an idea, and much further theoretical and experimental work needs to be performed to examine its validity.

Variation in Mutation Rates along the Chromosome

Mutation may also bias patterns of genetic variation if certain regions of the genome are more prone to mutation than other regions. In a recent study, Foster et al. (2013) sequenced 24 MA lines of MMR defective E. coli . They found a striking pattern by which mutations are not randomly distributed along the chromosome. Rather, mutations fall in a wave-like pattern that is repeated in an almost exact mirror image in the two separately replicated halves (replicores) of the E. coli chromosome ( Foster et al. 2013 ). They further showed that mutation density was higher in regions of the E. coli chromosome where gene expression is regulated by nucleoide-associated proteins. These results were interpreted by Foster et al. (2013) to imply that mutation rates are affected by chromosome structure.

In a recent study, Martincorena et al. (2012) claimed to show that mutation rates are significantly lower in highly expressed genes and genes undergoing stronger selection. They postulated that by lowering mutation rates, particularly in genes that are more highly expressed and more important, E. coli was using an evolutionary risk-management strategy. These results were obtained by analyzing patterns of synonymous substitution between 34 E. coli strains, and relied on an assumption that these patterns of substitution evolved under relaxed selection, because of close relatedness of these strains ( Martincorena et al. 2012 ). It is important to note, however, that different E. coli strains are highly diverged and that patterns of substitution between strains of E. coli are, in fact, subject to extremely strong selection ( Hershberg et al. 2007 ). It is therefore quite possible that the differences in the frequency of E. coli synonymous substitutions between highly expressed and less highly expressed genes are because of selection, rather than mutation. Indeed, it was very recently shown that the theory of adaptive risk management via lowering of mutation rates in highly expressed genes is theoretically untenable ( Chen and Zhang 2013 ). Furthermore, the negative correlation suggested by Martincorena et al. (2012) between mutation rates and levels of expression was not supported by MA studies in E. coli , Salmonella , and yeast ( Lind and Andersson 2008 ; Lee et al. 2012 ; Park et al. 2012 ; Chen and Zhang 2013 ; Foster et al. 2013 ). To the contrary, in some MA studies, a significant positive correlation is observed between levels of expression and mutation frequencies ( Lind and Andersson 2008 ; Park et al. 2012 ; Chen and Zhang 2013 ).

CONSTITUTIVE MUTATORS AND STRESS-INDUCED MUTAGENESIS

As mentioned above, natural selection is thought to favor the lowering of mutation rates, because many mutations are deleterious ( Kimura 1967 ; Drake 1991 ; Dawson 1998 ; Lynch 2010 ). In sharp contrast to this expectation, it was observed that ∼1% of all natural bacterial isolates are mutators that have high mutation rates, compared with the reminder of the population ( Gross and Siegel 1981 ; LeClerc et al. 1996 ). If indeed selection disfavors high mutation rates, why would hypermutating bacteria be present at such high frequencies? The best explanation currently available is that mutators accelerate adaptation in asexual clonal populations ( Sniegowski et al. 1997 ; Taddei et al. 1997 ; Giraud et al. 2001 ; Notley-McRobb et al. 2002 ). Mutator alleles may thus be linked to adaptive alleles that arise as a result of hypermutation. It is therefore thought that when bacteria are exposed to strong pressure to adapt quickly (e.g., when they are faced with new challenges), mutator alleles may become beneficial, which increases their frequencies ( Sniegowski et al. 1997 ; Taddei et al. 1997 ; Giraud et al. 2001 ; Notley-McRobb et al. 2002 ).

The mutators discussed above are constitutive mutators—bacteria that are defective in their repair mechanisms and that constitutively mutate at higher frequencies ( LeClerc et al. 1996 ). However, it has also been postulated that bacteria may be able to selectively increase mutation rates when they are exposed to certain “stressful” or growth-limiting conditions (reviewed in Foster 2007 ; Galhardo et al. 2007 ). Modeling has shown that such stress-induced mutagenesis (SIM) should be highly beneficial ( Ram and Hadany 2012 ), as it could allow bacteria to transiently increase mutagenesis particularly when they are most pressured to adapt. Yet, the study of SIM has been plagued by fierce debate (e.g., Slechta et al. 2002 , 2003 ; Roth et al. 2003 , 2006 ; Wrande et al. 2008 ; Katz and Hershberg 2013 ). In this review, I do not have sufficient space to delve into the full debate, but will only introduce some points of contention.

The strongest support of SIM, and the most detailed understanding of its mechanisms has come from the use of a particular assay suggested originally by Cairns and Foster (1991) . In this assay, a special E. coli strain, deleted for its chromosomal lac operon, and carrying a lacI-lacZ fusion gene with a frameshift mutation in lacI on an F′ conjugative plasmid, is plated onto lactose plates. On such plates, only cells that become lac positive can form colonies, and so the frequency of reversion mutants can be monitored. Original proponents of SIM assumed that growth could only be achieved on the plates by reversion mutants that corrected the frame-shift mutation in lacI . Colonies forming from mutants that arose before plating were expected to emerge within 2 days of plating, and any subsequent colonies were assumed to result from mutations occurring on the plates, in nongrowing bacteria. Any such mutations were assumed to be the result of SIM.

Studies utilizing the Crains and Foster Lac assay suggested that the occurrence of stress-induced frameshift mutations depended on double-strand breaks (DSBs), repair of these DSBs by an error-prone polymerize, dinB , and also depended on the bacterial stress response, mediated by the stationary phase σ factor, rpoS (reviewed in Galhardo et al. 2007 ). Although these results suggested a mechanism by which SIM could occur, use of the Lac assay was severely debated. First, it was argued that increased reversion could be caused by amplification of the inactive lac gene, slow growth of cells carrying this amplification, consequent frameshift reversion mutations, and selection for these mutants that could now grow freely on the lactose plates (reviewed in Roth et al. 2006 ). Thus, it was suggested that frameshift reversions were not necessarily because of SIM. Second, it was argued that the particular F′ conjugative plasmid used was problematic, as it contained an extra copy of the dinB gene that was shown to be important for increased frequency of reversion ( Roth et al. 2006 ). It was therefore argued that the results obtained using the Lac assay were not general, but rather particular to the assay used.

To address these concerns, Shee et al. (2011) more recently developed an alternative chromosomal assay for studying SIM. In this assay, the frequency of frameshift reversions to an artificially introduced tetracycline resistance cassette containing a deactivating frameshift mutation is quantified. DSBs are induced artificially by placing the tetracycline cassette 8.5 kb from an I-sceI double-strand endonuclease cut-site. The cells are engineered to contain an SceI gene, controlled by a P BAD promoter, which is repressed when glucose is available, but derepressed once glucose becomes depleted and cells begin to starve. Using this assay, Shee et al. (2011) could show that there was an increase in the frequency of tetracycline-resistant reversion mutants in response to starvation. This increase was shown to be dependent on DSBs, dinB , and rpoS ( Shee et al. 2011 ). Shee et al. interpreted their results as demonstrating that results obtained using the Lac assay are not specific to that assay, and that SIM indeed occurs in E. coli, and depends on the stress response being induced and on error-prone repair of DSBs.

So far, I have discussed SIM as it has been studied in artificial laboratory models, but has SIM been shown to occur within natural bacterial populations? Until very recently, the best, most well cited evidence for the natural occurrence of SIM came from experiments conducted by Bjedov et al. in 2003 ( Bjedov et al. 2003 ). In these experiments, ∼800 natural isolates of E. coli , extracted from a large variety of host-associated and non-host-associated environments were tested for the frequency with which they accumulate resistance to rifampicin in young and aging colonies. It was observed that, to varying extents in different isolates, the frequency of mutants resistant to rifampicin increases in aging colonies compared with young colonies. This increase in the frequency of resistant mutants was a priori assumed to result from increased mutagenesis, resulting from the starvation stress incurred via growth in aging colonies. Indeed the resulting paper was titled “stress-induced mutagenesis in bacteria” ( Bjedov et al. 2003 ). A subsequent study, published in 2008, showed that increased frequency of resistance to rifampicin could also be explained by natural selection, as it showed that many rifampicin-resistant mutants carried a growth advantage in aging colonies ( Wrande et al. 2008 ). Yet the Bjedov et al. study continued to be very widely cited as conclusive evidence for the occurrence of SIM within natural bacterial populations (e.g., Bogumil and Dagan 2012 ; Buerger et al. 2012 ; Feher et al. 2012 ; Obolski and Hadany 2012 ; Rosenberg et al. 2012 ; Ryall et al. 2012 ; Sanchez-Alberola et al. 2012 ; Maclean et al. 2013 ; Martincorena and Luscombe 2013 ).

We have recently repeated the Bjedov et al. experiments on a single laboratory strain of E. coli . Consistent with their results, we were able to show a substantial increase in the frequency of resistance to rifampicin in aging colonies compared with young colonies. We also observed a sharp increase in the frequency of resistance to a second antibiotic, nalidixic acid ( Katz and Hershberg 2013 ). We then used whole-genome sequencing to show conclusively that increased mutagenesis could not explain the increased frequency of resistance observed to either of the two antibiotics ( Katz and Hershberg 2013 ). Therefore, SIM cannot explain the Bjedov et al. results, and these results cannot be seen as evidence of SIM occurring in natural bacterial populations.

We further showed that, as was previously shown for rifampicin resistance mutations ( Wrande et al. 2008 ), nalidixic acid resistance mutations can also confer a growth advantage in aging colonies ( Katz and Hershberg 2013 ). An additional study showed that a mutation conferring resistance to streptomycin can also improve growth when bacteria are grown on poor carbon sources ( Paulander et al. 2009 ). Combined, these results show that using antibiotic resistance as a marker for the study of mutation in general and SIM in particular may be highly problematic.

CONCLUDING REMARKS

Much remains to be understood about the rates and patterns of mutation and about how these vary between different bacterial isolates, within populations, as a factor of growth conditions, and along the chromosome. Mutation is difficult to study because it is a highly noisy process and because it affects variation in a manner that is highly entangled with the effects of natural selection. To characterize the effects of mutation, we need to acknowledge these complications and find creative ways to address them. Future studies will undoubtedly take advantage of our increasing ability to examine variation at the whole-genome level to reveal much more about mutation and how it acts as an engine of evolution in bacteria and beyond.

ACKNOWLEDGMENTS

I thank Sophia Katz, Wesley Field, and Talia Karasov for their helpful comments. R.H. is supported by a European Research Council (ERC) FP7 CIG Grant (No. 321780), by a BSF Grant (No. 2013463), by a Yigal Allon Fellowship awarded by the Israeli Council for Higher Education, and by the Robert J. Shillman Career Advancement Chair. Work by R.H. is performed in the Rachel & Menachem Mendelovitch Evolutionary Process of Mutation & Natural Selection Research Laboratory.

Editor: Howard Ochman

Additional Perspectives on Microbial Evolution available at www.cshperspectives.org

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Pierre Kory’s Medical Musings

The History And Evolution Of The Somatic Mutation Theory In Cancer

The consensus theory explaining the cause of cancer is called the somatic mutation theory. it has guided research and treatment in cancer for over 70 years. let's re-examine its (non) validity..

In this post, I plan to, as succinctly and simply as possible, introduce the two competing theories regarding the origin of cancer and then go through the evidence for the current “consensus” theory which is called the Somatic Mutation Theory or SMT. The competing theory, called the Metabolic Theory of Cancer (MTOC) will be summarized in my next post in this series.

First, let’s define cancer. From the seminal paper “ Hallmarks of Cancer ” by Weinberg and Hanahan, a cell is defined as “cancerous” when they exhibit these 8 characteristics;

it stimulates its own growth

it evades growth suppressing signals

it resists cell death (apoptosis)

it enables replicative immortality

it induces the ability to grow new blood vessels to further tumor growth (angiogenesis)

it spreads to distant sites (metastasis)

it has the ability to evade the immune system

it has a “reprogramming of energy metabolism” ( the “Warburg Effect)

In layman’s speak - cancer is the uncontrolled growth of a cell - ever dividing and not dying off naturally nor allowing itself to be cleared by the immune system. Plus, it allows itself to spread and then multiply in areas of the body distant from its origin (a characteristic for which no mutation has ever been found to explain this property but forgive me for I am getting ahead of myself).

Now, one of the main points of this post is that characteristic #8, that of having undergone a “reprogramming of energy metabolism” (the central pillar supporting the MTOC) was only added to the list above after one of the top SMT cancer researchers in the world was “admonished” to do so by one of the top researchers of the MTOC. Although it was added only 10 years ago, Warburg discovered this unique property of a cancer cell back in 1927.

Now, to understand the core difference between the two theories you will need a simple understanding of cell biology, i.e. the basic structure and function of a cell. So, as simply as possible, know these two things about cells:

THE NUCLEUS (Central to the Somatic Mutation Theory)

What you need to know about the nucleus is:

The nucleus is generally considered the control center of the cell because it stores all the genetic instructions (DNA) for manufacturing proteins used by the cell.

The DNA is the blueprint of instructions that dictates everything a cell will do and all of the products it will make (the information is contained in “genes” within the DNA - short sequences of “instructions”).

When a cell divides, the DNA must be duplicated so that each new cell receives a full complement of the parent cell’s DNA.

The “Somatic Mutation Theory” posits that cancer arises from the accumulation of genetic mutations (errors) in tumor suppressor or tumor promoter genes within the DNA of the nucleus, causing the aberrant behaviors listed above. These mutations are caused by various “carcinogens” (agents that cause cancer) within our environment.

THE MITOCHONDRIA (Central to the Metabolic Theory)

All you need to know about the mitochondria is:

A  mitochondrion is a membranous, bean-shaped organelle that is the “energy transformer” of the cell. Each cell has numerous mitochondrion.

Along its inner membrane is a series of proteins, enzymes, and other molecules that perform the biochemical reactions that convert either oxygen or glucose into energy in the form of adenosine triphosphate (ATP), which provides usable cellular energy

Cells use ATP constantly, and so the mitochondria are constantly at work.

Oxygen molecules are required to make ATP, which is why you must constantly breathe. Converting oxygen to ATP is a process called “aerobic respiration.” There is also another, less efficient pathway that a mitochondrion can make energy by, and that is via using sugar (glucose), a process called “anaerobic respiration” or “fermentation.”

The “Metabolic Theory of Cancer” posits that carcinogens, instead of directly damaging DNA, instead first damage the mitochondria in such a way that they cannot use oxygen to create energy and are instead forced to rely near solely on sugar (glucose) for energy.

This abnormal respiration is exhibited by ALL cancer cells. The MTOC experts argue that it is this reliance on an alternative energy pathway by dysfunctional mitochondria which then induce mutations in the nucleus such that tumor suppressor genes are “turned off” and tumor promoter genes are “turned on .“

An important concept to know which will begin to reveal my bias in support of the MTOC is that abnormal respiration is present in every cancer cell, but not every cancer cell has been found to have mutations in their DNA. Tumors free of any mutations can even possess aggressively cancerous properties.

THE HISTORY OF THE SOMATIC MUTATION THEORY (SMT)

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Kilometer-Scale Convection Allowing Model Emulation using Generative Diffusion Modeling

Storm-scale convection-allowing models (CAMs) are an important tool for predicting the evolution of thunderstorms and mesoscale convective systems that result in damaging extreme weather. By explicitly resolving convective dynamics within the atmosphere they afford meteorologists the nuance needed to provide outlook on hazard. Deep learning models have thus far not proven skilful at km-scale atmospheric simulation, despite being competitive at coarser resolution with state-of-the-art global, medium-range weather forecasting. We present a generative diffusion model called StormCast, which emulates the high-resolution rapid refresh (HRRR) model—NOAA’s state-of-the-art 3km operational CAM. StormCast autoregressively predicts 99 state variables at km scale using a 1-hour time step, with dense vertical resolution in the atmospheric boundary layer, conditioned on 26 synoptic variables. We present evidence of successfully learnt km-scale dynamics including competitive 1-6 hour forecast skill for composite radar reflectivity alongside physically realistic convective cluster evolution, moist updrafts, and cold pool morphology. StormCast predictions maintain realistic power spectra for multiple predicted variables across multi-hour forecasts. Together, these results establish the potential for autoregressive ML to emulate CAMs – opening up new km-scale frontiers for regional ML weather prediction and future climate hazard dynamical downscaling.

Publication Date

Research area, uploaded files.

Inference for Local Projections

Òscar Jordà

Atsushi Inoue

Guido M. Kuersteiner

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2024-29 | August 19, 2024

Inference for impulse responses estimated with local projections presents interesting challenges and opportunities. Analysts typically want to assess the precision of individual estimates, explore the dynamic evolution of the response over particular regions, and generally determine whether the impulse generates a response that is any different from the null of no effect. Each of these goals requires a different approach to inference. In this article, we provide an overview of results that have appeared in the literature in the past 20 years along with some new procedures that we introduce here.

Suggested citation:

Inoue, Atsushi, Òscar Jordà, and Guido M. Kuersteiner. 2024. “Inference for Local Projections.” Federal Reserve Bank of San Francisco Working Paper 2024-29. https://doi.org/10.24148/wp2024-29