Common ancestry is one of the pillars of Darwin’s theory of evolution. Today, the tree of life, which represents how all life is genealogically related, is often thought of as an essential component in the foundations of biological systematics and so therefore of evolutionary theory – and perhaps all of biology itself. It is an iconic representation in biology and even penetrates into popular culture.

Massive amounts of time, effort, and money are being put into understanding and reconstructing the tree. Yet there are serious debates as to the usefulness and even the very existence of the tree. Here I will attempt to critically evaluate the merits of some of these worries. In doing so, we will see that questions about the tree and the foundations of systematics can be answered in the light of a wide range not only of empirical considerations but of philosophical considerations as well. A historically informed picture of how and why we got to where we are today is important for understanding these debates; however, here I can give only the briefest of introductions to the history of the tree as it has been used in systematics before turning to contemporary and future considerations.

As part of the 2009 Darwin celebrations, we have seen the emergence and widespread acceptance of a standard narrative of the history of evolutionary biology that construes a more or less direct line from Darwin to present-day evolutionary developmental biology, or evo-devo (Mayr 1982; Larson 2004; Carroll 2005; Zimmer 2006, 2009; Ruse and Travis 2009). It is a story of completions and syntheses that not only celebrates Darwin’s genius but also implies an implicit progression of ideas, with inclusion of new empirical facts and methodological approaches within the general framework of Darwinism leading to an increasingly more complete understanding of the evolutionary process. This narrative involves both scientific and public discourses. It can be found in textbooks of evolutionary biology and in popular accounts of evolution; it is also the basis the many efforts to construct a more inclusive evolutionary worldview.

But the standard narrative “From Darwin to Evo Devo” is also woefully incomplete as it leaves out several important traditions within the history of evolutionary biology (Laubichler and Maienschein 2007). These neglected traditions are not fringe ideas with no relevance to current understanding of evolutionary processes that can therefore be relegated to the dustbin of history. Quite the contrary. The ideas and approaches that are part of a complementary tradition – namely, to explain the evolution of organisms in reference to the developmental mechanisms that first generate phenotypes and phenotypic variation – have informed some of the most important current evolutionary biology research programs, those in developmental evolution (devo-evo) and synthetic experimental evolution (SEE) (Wagner, Chiu, et al. 2000; Davidson 2006; Davidson and Erwin 2006; Laubichler 2007; Erwin and Davidson 2009).

The ancient Greeks were not evolutionists (Essay 1, “Origins and the Greeks”). It was not that they had an a priori prejudice against a gradual developmental origin for organisms (including humans) but that they saw no real evidence for it. More importantly, they could not see how blind law – that is to say, natural law without a guiding intelligence – could lead to the intricate complexity of the world, complexity serving the ends of things, particularly organisms. This need to think in terms of consequences or purposes, what Aristotle called “final causes,” was taken to speak definitively against natural origins.

It was not until the seventeenth century – what is known as the Age of the Enlightenment – that we get the beginnings of evolutionary thinking (Essay 2, “Evolution before Darwin”). This could have happened only if there was something, an ideology, sufficiently strong to overcome the worry about ends. Such an ideology did appear, that of progress: the belief that through unaided effort humans could themselves improve society and culture. It was natural for many to move straight from progress in the social world to progress in the biological world, and so we find people arguing for a full-scale climb upward from primitive forms, all the way up to the finest and fullest form of being, Homo sapiens: from “monad to man,” as the saying went (Fig. Introduction.1). It was not generally an atheistic doctrine, being more one in line with “deism,” the belief that God works through unbroken law. But it did increasingly challenge any biblical reading of the past, and it went against evangelical claims about Providence, the belief that we humans unaided can do nothing except for the sacrifice of Jesus on the cross.

From the last third of the nineteenth century until the middle of the twentieth, official Catholicism, like other sectors of Christianity, had expressed considerable hostility to “Darwinism.” Early Catholic resistance to evolution usually followed from the impression that “Darwinism” is inseparable from “naturalism,” “materialism,” “rationalism, “socialism,” and other creeds taken to be atheistic. From the time of Pope Pius IX (1792–1878) and his promulgation of “The Syllabus of Errors” (1864) until the mid-twentieth century, conservative church officials usually suspected that evolution is especially allied with materialism, the belief that mindless matter is ultimately “all there is” and that therefore God does not exist (Fig. 60.1).

Such a suspicion was not entirely without foundation. During Pius IX’s papacy (1846–78) both Karl Marx and Ernst Haeckel had interpreted Darwin as supporting their own distinct versions of materialism. And in his diaries even Darwin revealed at times his own temptations to materialism. Furthermore, philosophical materialists well into the twenty-first century enthusiastically embraced evolution not only for scientific but also for philosophical reasons. By that time, “postmodern” criticism had called attention to the ideological bias that often accompanies putatively objective discourse, but several highly celebrated biologists and scientific thinkers (e.g., E. O. Wilson, Richard Dawkins, and Daniel Dennett) continued to stitch their evolutionary ideas tightly into a materialist belief system, thus making evolution, at least as they interpreted it, religiously indigestible on any terms. Hence, it is not surprising that scientifically unsophisticated popes and theologians in the late nineteenth and early twentieth century, unable to distinguish clearly between science and materialist beliefs, were often appalled by Darwin’s evolutionary theory.

1. We hold that Evolution’s plan,

2. To give as little as she can,

3. Is sometimes trying.

4. Fair share of brains, indeed, we win;

5. But why not throw the swimming in,

6. Why not the flying?

7. – May Kendall

The 1870s were characterized by debate of the “woman question” – or, more accurately, questions. What were the moral, intellectual, and physical capabilities and limitations of women? What roles should women be afforded in Anglo-American society? From which social arenas should they be excluded? This political climate shaped the contents of Charles Darwin’s Descent of Man, and Selection in Relation to Sex (1871), while also being significantly impacted by it. Antifeminists and feminists alike saw the opportunity to use the power of scientific authority, and specifically the power of Darwin’s name and theory of sexual selection, to promote what were often diverse views of woman’s place in nature and society.

Beginning in the late 1970s, historians of science began to correct a past blind spot in scholarship and university courses on the Darwinian Revolution by including analysis of gender issues, specifically in relation to the content of Descent of Man. For example, Ruth Hubbard (1979), Evelleen Richards (1983), and Rosemary Jann (1997), among others, investigated the extent to which Darwin should be identified as sexist and highlighted feminist responses to the Descent of Man written by nineteenth-century women such as Eliza Burt Gamble (1841–1920), May Kendall (1861–1943), and Charlotte Perkins Gilman (1860–1935).

Like many other naturalists, Charles Darwin did not find the finches to be very interesting. During his five-week visit to the Galapagos Islands, Darwin saw many finches and collected some of them, but they were so different in outward appearance that he failed to recognize that they all came from the same family. Instead, he initially called one a finch, another a blackbird, and another a grosbeak. After his return to England, the ornithologist John Gould (1839), who analyzed and described Darwin’s ornithological collection, convinced Darwin that the finches merited more interest. In the first edition of the Voyage of the Beagle (1839), Darwin noted the similarities among the finches (see Plate XXXIV).

The biological importance of the finches had made an impression on Darwin in the years since his brief encounter with them: “These birds are the most singular of any in the archipelago,” but in most respects of form and function, they remained uninteresting. Nevertheless, the beaks of the various species did capture Darwin’s (1839c) attention: “It is very remarkable that a nearly perfect gradation of structure in this one group can be traced in the form of the beak, from one exceeding in dimensions that of the largest gros-beak, to another differing but little from that of a warbler.”

That Darwin’s contributions toward understanding the evolution of social behavior were significant is undeniable. In the Origin of Species there was detailed treatment of “social evolution,” and this thinking led to much discussion, something given fresh impetus and further fuel in the Descent of Man. Darwin’s chapters in Descent on “The Comparison of the Mental Powers of Man and the Lower Animals” and “On the Development of the Intellectual and Moral Faculties during Primeval and Civilised Times” led to a great deal of speculation and comment with regard to the possibility of social and perhaps moral instincts in lower animals. Yet, as we shall see, although Darwin explicitly engaged this issue, its significance in evolutionary thinking, especially regarding the evolution of behavior, waxed and waned.

Social Insects and Social Instincts

Passages from both the Origin and Descent illuminate Darwin’s position with regard to selection acting on traits involved in social behavior. The following oft-quoted passage, from chapter 3, “The Struggle for Existence,” illustrates the breadth of action that Darwin (1859, 62) assigns to the struggle leading straight into the mechanism of natural selection: “I should premise that I use the term struggle for existence in a large and metaphorical sense, including dependence of one being on another and including (which is more important) not only the life of the individual, but success in leaving progeny.” The problem is that (seemingly) success is at the individual level and the group gets overlooked and lost. This is no recipe for social behavior. Darwin’s solution, however, involved the idea that selection could act at a level above the individual: a family, a colony, a social group, or a community. Later in the Origin, where Darwin is dealing mostly with the social insects, we see how this insight comes into play. Darwin recognizes the difficulty that the neuter insects with their distinct morphology and habits present to his theory and thus, in typical Darwinian style, he does his best to explain and diffuse this potentially devastating case.

One would have thought that, by now, 150 years after the Origin, biologists could agree on a single definition of species. Many biologists had indeed begun to settle on the “biological species concept” in the late modern synthesis (1940–70), when new findings in genetics became integrated into evolutionary biology. However, the consensus was short-lived. From the 1980s until the present, it seems not unfair to say that there arose more disagreement than ever before about what species are. How did we get into this situation? And what does it have to do with Darwin? Here, I argue that a series of historical misunderstandings of Darwin’s statements in the Origin contributed at least in part to the saga of conflict among biologists about species that has yet to be resolved. Today, Darwinian ideas about species are becoming better understood. At long last, the outlines of a new and more robust Darwinian synthesis are becoming evident. This “resynthesis” (as it perhaps should be called) mixes Darwin’s original evolutionary ideas about species with evidence from modern molecular and population genetics.

What Did Darwin Mean by Species?

Darwin realized he had convincing proof that species were not created but evolved. But this understanding caused a terminological problem that he had to address in his book. Species were defined in the minds of many of his Creation-educated readers as members of real groups: all members of a species were related by descent, whereas no individual was descended from members of another species. A second idea, which had been promoted especially by the French naturalist Buffon, was that the intersterility of species was a protective mechanism with which species had been endowed by the Creator to maintain their purity (Fig. 11.1). Thus, the famous anatomist Richard Owen, a powerful creationist opponent of Darwin, had given this succinct definition in his 1858 treatise on chimpanzees and orangutans: “an originally distinct creation, maintaining its primitive distinction by obstructive generative peculiarities” (as cited by Huxley 1860, 544).

With the acclaim for Darwin’s postulate of evolution through natural selection came the excitement and the challenge of explaining ever-more complicated natural phenomena in Darwinian terms. And as biological explorers continued to describe new observations, particularly from tropical habitats, the number of challenges grew rapidly. An avalanche of letters among these naturalists exchanged ideas and hypotheses, with Darwin’s correspondence itself revealing extensive musing on an array of patterns and their possible emergence from natural selection on individuals.

Few observations were as intriguing as those on mimicry and camouflage. While some observations seemed easy to explain – caterpillars that blended with their leafy backgrounds would be less likely to be preyed upon than caterpillars that contrasted with their backgrounds – others were more difficult. Mimicry was one of those more difficult challenges. The early history of Darwinian evolution, as a science, is tightly entwined with the arguments about whether mimicry could be readily explained in Darwinian terms (see Essay 15, “Mimicry and Camouflage”).

It is important to distinguish two distinct phenomena of organismal coloration and pattern (Ruxton, Speed, and Kelly 2004). Crypsis occurs when it is difficult to distinguish an organism from its background. This can happen when an organism’s color or pattern causes it to blend visually into its background, when its shape and color make it resemble an object in its background, or when its pattern and color break the outline of its shape against its natural background and make it difficult to recognize. Our usual understanding of “camouflage” embraces one or the other of these descriptions ( Figs. 40.1 and 40.2 ). Mimicry occurs when the features of one species resemble those of another and, through that resemblance, confer some survival advantage on the mimic.

Nothing in biology makes sense except in the light of evolution.” Dobzhansky’s (1964, 449) sweeping generalization is provocative but also partial. Ecology casts the same indispensable light in biology, particularly on evolution. Nowhere is this clearer than in the origin of evolutionary theory. Although the term “ecology” was not coined until 1866 (Haeckel 1866), ecological insight is at the core of Darwin’s theory. It is reflected both in the theory’s concepts – for example, adaptation and natural selection – and in its compelling accounts of biological phenomena, such as the transmutation of species and the fit between organisms and environments. That evolutionary biology’s chief architect is Darwin is well known. The foundational role his work had in ecology and that an ecological perspective underpins the theory of natural selection are less appreciated.

Reconceptualizing the Environment

Perhaps the most theoretically fertile issue at the intersection of ecology and evolution is the adaptive fit between organisms and their environment. Seeing that relationship as the key to evolutionary dynamics required a reconceptualization of how the environment impacts organisms and the environment itself.

At the turn of the nineteenth century, philosophical and scientific conceptions of the environment reflected a romantic zeitgeist. Thoreau’s Walden , for example, exemplifies the view ( Fig. 47.1). In it, organisms and their environments are coupled components of an encompassing, harmonious system, each complementing the other in a providential symbiosis. The same underlying theological commitment to a beneficent and coherent order in the living world arguably compelled the impressive systematicity (and occasional biological misstep) of Linnaeus’s classification system. But by the mid-nineteenth century a less idyllic, more brutal view of the environment was challenging the prevailing romanticism (Worster 1994 ). Tennyson’s grim characterization of nature as “red in tooth and claw” captured the new sentiment, and would find scientific expression and vindication in Darwin’s theory.

The reception of the theory of evolution by Muslims took place in a setting that differs entirely from the reception by Western Christians and Jews. Because the Islamic world had not participated in the Scientific Revolution, other concepts such as post-Copernican astronomy had become known only slightly earlier (Riexinger 2004, 372–84, 392–410). In many countries, the curricula for religious scholars consisted of the traditional branches of scholarship alone (Riexinger 2009, 246–47). Because the rates of illiteracy remained high in most countries well into the twentieth century, scientific concepts did not find a large audience. And unlike Japan, other East Asian countries that followed Japanese models, and, to a lesser degree, India, the Islamic countries failed to establish institutions of higher education and research capable of producing significant scientific output (United Nations Development Programme 2003).

Furthermore, whereas research on the reception of modern scientific concepts is still at an initial level in much of the Muslim world, for some regions, including North and sub-Saharan Africa and Southeast Asia, even basic studies are still lacking. Hence, this overview on the reception of the theory of evolution, the religious context in which it occurred, the religious responses, and its practical consequences has to be considered preliminary.

Darwinism was received in Latin America always in relationship, whether explicit or not, with positivism, a term first used by the social philosopher Saint-Simon to refer to scientific method and its extension to philosophy: scientific knowledge was viewed as “positive.” As reformulated by Auguste Comte, positivism came to be a system of thought in which science was the only source of authority. It was not a philosophy of science, had no universal notion of truth, and did not promote specific methods or laws. In Europe, it was envisioned as a kind of capstone to the scientific revolution. In Latin America, however, positivism (in its Comtean form) preceded the instauration of science; therefore, it was programmatic, and one of the programs was science (Fig. 31.1).

Schools of Thought

Positivism came in two varieties, Comtean (“social positivism”) and Spencerian (“evolutionary positivism”). Social positivism promoted a more just society through the application of science. Evolutionary positivism was associated with Herbert Spencer and, of course, with Darwin. In Spencer’s writings there was a stress on universal progress as a continuous, unilinear evolution from a primitive nebula to human civilization. He used the term “evolution” as a synonym of progress even before the publication of the Origin of Species (1859), and Darwin’s theory simply gave substance to his view of a general evolutionary process characterized by the passage from the homogeneous to the heterogeneous, from the simple to the complex.

Through most of the twentieth century, the influence of Darwin on the philosophical field of ethics was negligible. Things changed noticeably in the last couple of decades or so of that century, and now “evolutionary ethics” – which had lain dormant since Darwin’s contemporary Herbert Spencer – is a lively and hotly debated topic. There are several Darwinian theses that might have bearing on moral philosophy.

1. Humans are the product of natural selection.

2. (i) + Humans have been forged by that process to be social organisms.

3. (ii) + Among the mechanisms that govern that human sociality is an innate moral sense.

The first two are beyond serious question, but the last – moral nativism – can be reasonably doubted. It is a plausible counterclaim that the human tendency to engage in moral assessment (of oneself and others) is not a discrete psychological adaptation but a learned cultural trait that depends on psychological capacities that evolved for other purposes. Darwin himself, however, arguably endorsed all three theses; he possibly advocates (iii) in The Descent of Man:

Even before Charles Darwin put pen to paper to write up his theory of evolution through natural selection, entomologists knew full well that the colors of insects “deceive, dazzle, alarm or annoy” their enemies (Kirby and Spence 1815–28, 2:219). It was taken as overwhelming proof of the power and beneficence of the good god, a firm plank in the edifice of natural theology (Kimler 1983). In the standard work, An Introduction to Entomology, or Elements in the Natural History of Insects, coauthored by the parson-scientist William Kirby, a prize example was the “mimicry” of the Brazilian walking stick insect (Phasma) that so closely resembled the twigs on which it spent its living days. Although no full-blown theory was offered, it was clearly noted that it had a function, because the author “has often been unable to distinguish it [the insect] from them [the twigs], and the birds probably often make the same mistake and pass it by” (Kirby and Spence 1815–28, 2:220).

The explanation of unusual coloration was muddled, however, by natural theology’s reliance on design. Resemblance to an object or background as deceptive disguise (camouflage) made sense as a providential aid to the species, but what to make of resemblance merely to another animal? The usual answer for such mimicry (or copying), if not left to a creative god’s mysteries, lay in vague, ideal parallelisms or analogies. Darwin’s great breakthrough in the Origin of Species was to show through his mechanism of natural selection how it is that all such cases of exquisite design can be explained naturalistically, as the result of natural selection brought on by the struggle for existence. However, in the first edition of the Origin, Darwin did not take up these problems.

The “evolutionary synthesis” is a phrase widely used for a period in evolutionary studies between 1920 and 1950 when important theoretical developments took place. The period also saw new types of interdisciplinary collaborations develop. These new associations reset the priorities of evolutionary studies for more than fifty years. Contributors came from every country with a significant scientific community and from nearly every discipline in the life sciences. The phrase “evolutionary synthesis” also refers to a period of discipline formation. This involved new community infrastructure, such as new professional societies and journals, dedicated to evolutionary studies. Those at the heart of these organizations who built this infrastructure quickly rose to prominence in the community and found themselves in a strong position to shape outside impressions of community activity.

When these promoters said they had invented the modern science of evolutionary biology, everyone who knew their work understood what they meant. Later, when the same people wrote their history, they were absolutely certain they walked in Darwin’s footsteps. Some said this was because, by and large, they agreed with his theory of natural selection and because they accepted his other major conclusions about evolution. However, the connections to Darwin went far deeper than any agreement about natural selection.

Darwin’s primary goal in The Descent of Man was to convince his readers that the general principles of the evolutionary theory he had laid out in The Origin of Species were equally applicable to humankind as they were to “lower” forms of life – namely, that our species, like all others, was descended from another, preexisting species, and that this process had been accomplished in large part (though not solely) through the agency of natural selection. Conspicuously absent from Descent was any account of the actual forms through which humankind’s line of evolutionary descent had passed. The reason for this was simply that, on the matter of human evolution, the fossil record remained silent, and Darwin was too cautious a scientist to venture into lines of argument for which he saw little supporting evidence. He also knew that the sparseness of the fossil record was not in itself sufficient reason to reject evolution. So, in the absence of any fossilized remains of ancestors, Darwin restricted himself to such genealogical inferences as could be made by comparing humans to other living forms in the light of his evolutionary principles.

As convincing as Darwin may have been using the evidence he had at hand, absence breeds curiosity. The scientific study of human evolution after Darwin has been animated in large part by the desire for the direct, material evidence of our species’ evolutionary ancestry that was still lacking at the time of Darwin’s death in 1882. Pervasive talk of “missing links” throughout the twentieth century testified to the hold that the absent ancestors had on both professional and public minds: Darwin had shown in principle that humans had an evolutionary history, but now the task was to populate that history. This is not to say that the work done by students of human evolution since Darwin has been only to slot newly discovered fossil ancestors into a theoretical framework set in stone by the Great Man. Quite the contrary, Darwin’s model of human evolution was challenged, defended, and modified on a number of fronts simultaneously to the influx of previously unknown fossil evidence.

The incorporation of Darwinism – its theory of modification of species through natural selection – occurred in research programs in France in the 1930s with the development of a remarkable and unique school of genetics of experimental populations. Around the same time, however, France witnessed another remarkable episode, perhaps the most impressive example of a durable and late opposition of French science to evolutionary theory: the general aversion of French paleontologists to phylogenies in the years 1900–50. (For a detailed account of these episodes, see Gayon and Veuille 2001; Gayon 2006, 2009.) As will be seen, images play an important role in this story.

The French Paleontologists’ Aversion to Representing Phylogenies (1900–1950)

This is a rather strange story, well known to paleontologists, but that has escaped the attention of historians of science. A quantitative enquiry into the three French periodicals that published almost the entire production of French paleontology in the years from 1900 to 1950 gave the following results.

Case 1: Annales de paléontologie (1906–1950)

Let us first consider the Annales de paléontologie (Annals of Paleontology). Founded in 1906, this was the very first periodical devoted entirely to paleontology in France. In the first issue of the journal, the editor Marcellin Boulle (known for his work in human paleontology) stated that “philosophical paleontology” should be a priority for the authors. “Philosophical paleontology” was a term Albert Gaudry used as a synonym for “evolutionary paleontology.” “Philosophical” meant that paleontologists should not only describe the presence of fossils in stratigraphic layers but should dare to make phylogenetic inferences.