1. Introduction

An evolutionary novelty can be defined as a discrete phenotypic trait that is new in composition or context of expression relative to established ancestral traits (see, e.g., West-Eberhard Reference West-Eberhard2003; Hall Reference Hall2005; Kaplan Reference Kaplan2007). In this essay, I will consider novelties that are somewhat complex—the kind of phenotypic traits that Darwin attempted to explain as products of selection and gradual change. And I will include the establishment of novelties in populations or lineages as regularly occurring traits, not just their initial appearance. The initial appearance of a novelty is an event that depends on preexisting developmental capacities used in other aspects of development, or on “latent capacities” that become evident (reawakened or newly assembled) when a novelty is initially evoked (Hall Reference Hall2005). I will consider only the evolution of adaptive novelties—that is, Darwinian evolution by natural selection. I will not consider pre-Darwinian or non-Darwinian explanations.

2. Darwin's Theory as a Causal Chain to Explain Adaptive Evolution

A satisfactory theory of novelty has to have a series of explanatory elements lined up in what might be called a “causal chain,” with a satisfactory mechanism for each step. As outlined by Darwin, the evolution of an adaptive novelty under natural selection is a two-step process: first variation, then spread. Beginning with an ancestral population, such a theory has to describe two aspects of variation: its inception—the initiation of change (the new input that gets it started—an upstream, stimulatory, or regulatory event); and the origin of new form—where the phenotypic end product comes from. Then, to account for spread in Darwinian terms, there has to be an explanation for how the novel variant affects selection (differential reproductive success), which causes an increase in frequency of the novelty within a population. But selection alone is not enough to explain evolution, because it does not explain cumulative phenotype-frequency change that continues across many generations. Such cross-generational change requires inheritance of the trait, which, together with selection, produces a change in frequency over time (adaptive evolution). Differential reproduction without inheritance of the fitness-affecting trait variation, as could occur between differently nourished members of a clone, produces only short-term change in phenotype frequencies.

Darwin's theory of novelty is a marvelously complete and ingenious analysis of this causal chain. In describing it, I will translate partially into modern terms for the sake of clarity and brevity. According to Darwin, the initiation of change is often associated with changed conditions (Reference Darwin[1859] 1872, 15–16). The new conditions cause increased variability, including small discrete novel variants, which Darwin called “individual differences” or “pecularities.” These, he observed, can be small, medium, or large—even “monstrous”—in size (Reference Darwin[1859] 1872, 38–39). The variation can be due to direct effects of the new conditions on the preexisting phenotypes (as in the use and disuse of limbs). But Darwin considered newly induced variations to be influenced significantly by the nature of the organism itself, or what Darwin called “constitutional” properties: “Organic beings, when subjected during several generations to any change whatever in their conditions, tend to vary; the kind of variation that ensues depending in most cases in a far higher degree on the nature or constitution of the being, than on the nature of the changed conditions” (Reference Darwin[1868] 1972, 237). In other words, Darwin observed that variation generated in response to conditions depends on what we would now call the genetically influenced makeup of the individual phenotype.

Given an array of newly induced variations, individuals showing different degrees of development of a novel trait will exhibit different degrees of survival or success in reproduction (natural or sexual selection; Darwin Reference Darwin[1859] 1872). But the problem of identifying a mechanism for inheritance remained to be solved. If a novelty is originally environmentally induced, how can natural selection increase that novelty's predominance in a population over time? Even if the conditional responses are seen as being to some degree inherited, or “constitutional,” from their initiation, the response is still dependent upon conditions. How can there be a lasting effect on the constitutional properties of individuals to explain the observed increase in the frequency of environmentally induced traits?

Once the material basis for inheritance was known to be the gene, the spread of genetically influenced conditional phenotypes could be identified with the spread of genes. This would have followed easily from Darwin's observation (discussed above) that variation in the response to conditions depends significantly on variation in constitution. But Darwin could not make the connection between conditional expression and genetic inheritance the way we can make it today nor could he have solved the problems of inheritance he observed had he known about Mendel's work,Footnote ¹ which did not explain the inheritance of condition-sensitive or of quantitatively variable traits.

Darwin reasoned clearly that an increase in the commonness of an environmentally induced trait would have to depend on inheritance, not on the environmental factor itself: “A fancier who wished to decrease the size of his bantams or tumbler-pigeons would never think of starving them, but would select the smallest individuals which spontaneously appeared. … Although every variation is either directly or indirectly caused by some change in the surrounding conditions, we must never forget that the nature of the organization which is acted on, is by far the more important factor in the result” (Reference Darwin[1868] 1972, 415).

To solve the problem of the inheritance of environmentally induced novelties under positive selection, Darwin invented a molecular theory of the gene—his theory of pangenesis (see esp. Reference Darwin[1868] 1972). He hypothesized the existence of tiny particles, which he called “gemmules,” that accumulate over generations of positive selection in the region of the body where a novelty is expressed. These particles could then be transmitted between generations. Darwin realized—and this is something that is often forgotten, for it was a feature of genetics ignored by the twentieth-century synthesis—that inheritance involves both the transmission and the expression of traits; the molecular gemmules, like DNA, were the material basis for both. Only now, when the age of Mendelian transmission genetics has given way to the age of gene expression, are we beginning to adequately appreciate this twofold role of the genome in both the transmission and the expression of phenotypic traits.

In sum, Darwin explained the increased inheritance of acquired traits with a kind of “genetic assimilation,” erroneously ascribed to phenotypically local effects on the particles of inheritance under natural selection. Darwin had to imagine a purely hypothetical mechanism to account for the observed and reported facts because in the late 1800s he had no other choice. He was completely aware of the limitations of his speculations in these respects: he termed his hypothesis of pangenesis “provisional” and acknowledged that it was subject to “a certain portion of incompleteness, and even of error” (Reference Darwin[1868] 1972, 349–350). And he repeatedly mentioned the inadequacy of contemporary understanding of the causes of variation: “At the present time there is hardly any question in biology of more importance than this of the nature and causes of variability” (Reference Darwin1882, vi).

The claim by some (e.g., Pinker Reference Pinker1998, 522) that “Darwin's … embrace of Larmarckism … was perhaps his biggest scientific blunder” seems unfair when one considers Darwin's caution regarding his speculations on the mechanism of inheritance, the tendency in subsequent discussions (including those taking place during the twentieth-century synthesis) to brush aside observations that Darwin considered of major importance (the eventual inheritance of environmentally altered phenotypes), and Darwin's seeming ambivalence regarding the inheritance of acquired traits. On the one hand, his highly tentative theory of pangenesis was Lamarckian (and erroneous) in hypothesizing that use could alter the material of inheritance. On the other hand, his discussion of inheritance was sometimes explicitly dismissive of Larmarck: upon noting that social insect workers (which do not reproduce) have traits passed on via the reproduction of queens (which do not work), Darwin concluded, “I am surprised that no one has hitherto advanced this demonstrative case of neuter insects, against the well-known doctrine of inherited habit, as advanced by Lamarck” (Reference Darwin[1859] 1872, 207). Much of Darwin's discussion (Reference Darwin[1859] 1872, Reference Darwin[1868] 1972) of “direct and definite action of the external conditions of life” and on “use and disuse” refers not to Lamarckian inheritance but to what we would now call “phenotypic plasticity.”

Finally, Darwin placed enormous emphasis on the importance of cumulative gradualism to explain the origin of complexity. In fact, he staked his whole argument on the principle of gradual change and asserted that the whole theory of evolution by natural selection could be falsified if any exception could be found. He wrote: “If it could be demonstrated that any complex organ existed, which could not possibly have been formed by numerous, successive, slight modifications, my theory would absolutely break down” (Reference Darwin[1859] 1872, 135). It is worth noting that with this statement, and others like it, Darwin's theory meets the scientific requirement of falsifiability.

In that passage of his writing, Darwin places great emphasis on gradualism, when at the same time he stated that novel variants could be large and even “monstrous” in size. Isn’t this a contradiction? It would seem that the existence of monstrous selectable variants would make his theory absolutely break down. Although Darwin recognized the existence of large variants, he consistently downplayed their importance. He did so in order to emphasize the central importance of selection. If he had given too much credit to variation, that would have detracted from the power of selection and would, in turn, have opened the door to the possibility of saltatory developmental origins, or even divine creation, of complex novel design. But Darwin had a clever way to remove this contradiction between gradualism and the occurrence of large developmental variants, which I call retrospective gradualism: he argued that some saltatory phenomena such as heterochrony and one-step reversions were simply the altered expressions of traits that had evolved gradually in the past. In other words, complex reorganizational variants are not really novelties—they are just old products of gradual evolution whose timing of expression has changed.

3. Mendelian Genetics: A Mutation-Based Incomplete Causal Chain

People are fond of saying that Mendelian genetics solved the problem of inheritance that Darwin had failed to understand. But Mendelian genetics did not account for all of the facts of inheritance that Darwin had observed. The version of evolutionary theory inspired by Mendelian genetics—the “synthesis” of mid-twentieth-century evolutionary biology—was in some respects oversimplified and incomplete. The mutation-based causal chain for the origin of novelty was depicted as follows (see Huxley Reference Huxley1942, 51): a genetic mutation leads (by an undescribed mechanism) to the production of a small phenotypic change in a single individual. Then, owing to a fitness increase associated with the mutant genetic allele, the mutant gene and the associated phenotype increase in the population over subsequent generations. A complex novelty requires a series of mutations. The problem of inheritance is solved by the cross-generational transmission of genetic alleles that have a one-to-one correspondence to the selected phenotype. This scheme was an incomplete account of the phenomena to be explained:

• • There is no role for environmental induction—even though the environmental induction of developmental variants is an obvious and undeniable fact, as extensively documented by Darwin and many studies since.

• • The mechanism for an effect of mutation on trait development is a black box.

• • And any hint that large developmental variants could play a role in evolution is strongly rejected (by, e.g., Fisher Reference Fisher1930; Charlesworth, Lande, and Slatkin Reference Charlesworth, Lande and Slatkin1982), even though such variants occur and evidently can become established during evolution (see West-Eberhard Reference West-Eberhard2003, Chapters 9–19, on evolution by developmental reorganization of the phenotype, sometimes gradual, sometimes by large steps). No hopeful monsters or macromutations are allowed. This synthesis is a strict version of gradualism, in some respects more uncompromising than Darwin's. It followed Darwin in emphasizing the importance of selection, and it went further than Darwin in the corresponding de-emphasis of developmental causes of variation.

In some respects, this is an evolutionary theory in denial, conceptually blind to the environmental sensitivity of phenotypes and to the fact that selection, which acts on phenotypes, must necessarily act on environmentally induced variation as well as on mutationally induced change.

This is a caricature, of course, and there were exceptions. C. H. Waddington was one of them—others were Baldwin (Reference Baldwin1896, Reference Baldwin1902) and Schmalhausen (Reference Schmalhausen[1949] 1986), but their ideas were less explicitly related to genetics than were Waddington's. Waddington did figure out a way, through his concept of “genetic assimilation” (Reference Waddington1953), to incorporate environmental induction into the genetic theory. Genetic assimilation treated environmentally induced traits as polygenic threshold traits, which could spread if positive selection lowered the threshold for their expression.

Even if this idea had been incorporated into the twentieth-century synthesis, which it was not (for various interesting reasons; see West-Eberhard Reference West-Eberhard2003, 415–416), Waddington's genetic assimilation did not really complete the synthesis as an explanation of novelties. In Section 4, I outline an expanded, remedial proposal.

4. The Origin of Novelty: A Modern Darwinian Causal Chain

5. Conclusion

Whether or not the scheme for the origin of novel traits that I have outlined above is completely convincing, we are in an exciting era for biologists and philosophers who aspire to formulate a complete causal theory of evolutionary novelties. We no longer have to guess at the mechanisms of inheritance and development. But modern molecular genomics and evolutionary developmental biology, important sources of the new information, still pay too little attention to the developmental role of the environment. I find it remarkable that we have yet to achieve the comprehensiveness of Darwin's original theory of novelty, and we will not match it until there is a wider appreciation of the role of the environment in the production of the selectable variation that creates novel form.