Foreword a Perspective on ‘Plasticity’

Foreword A perspective on ‘plasticity’

Mary Jane West-Eberhard Smithsonian Tropical Research Institute

Anyone interested in the nature of living organisms and their adaptive evolution will be stimulated by reading this book. I am no exception. But I have an advantage, the opportunity to write a Foreword, with freedom to comment—or even emote, opine, and reminisce—about the topics at hand without even the corrective of peer review to put a brake on runaway ruminations. I apologize in advance for citing my own work in sections where I am trying to substantiate a thought without doing a proper review. Start with the word ‘plasticity.’ It seems designed to befuddle the uninitiated because it does not bring to mind any obvious characteristic of living organisms, which are not plastic quite in the manner of elastic belts, rubber bands, bubble gum, or food packaging. I could be accused of having promoted the word plasticity by using it as one of four in a book title: Developmental Plasticity and Evolution (West- Eberhard 2003). But those four words cost more hours of agonizing indecision than any other set of four in a book of more than 300,000 words (yes, too long—so it was designed to be read in pieces). The problem with ‘plasticity’ was that it already had a definition, in terms of reaction norms of primarily quantitative traits. But that definition did not readily suggest all that needed attention, which included plasticity-facilitated developmental reorganization of qualitatively distinctive phenotypes. [Schlichting (2021) in this volume, citing Uller and colleagues (2020), notes some of the same reservations that I had about beginning with reaction norms.] I decided to adopt a broad version of the established definition: the ability to respond to an environmental input with a phenotypic change. For my purposes, plasticity might better have been called ‘responsiveness’ or ‘condition sensitivity.’ But plasticity already had a public. And the plasticity public was being enlarged at the time by important books and reviews. So I stuck with the word ‘plasticity.’ This quandary over terms indicates why the word ‘developmental’ as a modi- fier of plasticity is important. Development implies attention to mechanisms and invites looking at responsiveness to both external and internal environments— responsiveness of the phenotype at all levels of organization from the molecular to the behavioral, including internal responsiveness to gene products. Attention to developmental plasticity picks up Darwin’s thoughts where they left off—with a struggle to understand the causes of selectable variation. Those struggles were summarized in Darwin’s theory of pangenesis, which includes what we could now call a molecular theory of the gene, postulating tiny gemmules that, like genes, were seen as being found throughout the body and as mediating both the transmission and the expression of traits. The history of Darwin’s ideas about development

ix x Foreword and evolution, including the idea of phenotypic plasticity, is traced in Costa’s (2021) masterful chapter in this volume, beginning with Darwin’s ideas as a young man and intertwined in his thoughts about variation and selection until the end of his life, most remarkably in his two volumes on variation (Darwin 1868). Costa then traces the fate of those ideas through the history of evolutionary biology into the present, giving an unprecedented account of the history of developmental plasticity in evolutionary biology. Costa’s history is exciting because it shows the connections between Darwin’s ideas and current ones that seem to us to be ‘new’ (see also West-Eberhard 2003, Chapter 8; 2008b). Rediscoveries are no less exciting when their origins can be traced to Darwin or before. But Darwin’s achievement in this area is a lesson in humility for those who suffer from the amnesia that seems to generate new-discovery cycles with a periodicity of about 30 years for almost any idea in evolutionary biology. We now benefit from data that Darwin lacked, including concrete information on gene expression that allows us to see how the material basis for transmission and expression is the same—the dual nature fulfilled by the ‘gemmules’ he imagined. I think that Darwin would have been especially fascinated by the chapter in this book (Lister 2021) showing how fossils can now be used to substantiate the importance of developmental flexibility in the origin of morphological transitions. The same could be said regarding a chapter by Bonduriansky (2021) on non-genetic inheritance and epigenetic effects of the environment, a good entrée into an area that has enormously expanded in the last two decades. This book is sprinkled with histories. Costa’s (2021) history on Darwin and the causes of phenotypic variation is complemented by Sultan’s (2021) reminder of the long history of studies of plastic responses; Scheiner and Levis (2021) on the history of ideas about genetic assimilation; Diamond and Martin (2021) on the history of the plasticity as buying time for genetic adjustments to environmental change; Levis and Pfennig (2021) on the history of ideas about plasticity-led evolution; and Futuyma (2021) and Pfennig (2021, Box 3.2), both of whom track plasticity concepts to the 20th-century synthesis with genetics. Histories invite asking: what has changed in the past? And what might be changing now? The rest of this essay reflects thoughts about those questions. They are based on 60 years of personal observation that started in 1959 with a lab section in zoology at the University of Michigan, taught by a newly hired assistant profes- sor, Richard Alexander, who later became a prominent evolutionary biologist. As an undergraduate and graduate student in zoology, I learned—and internalized—the synthesis that put genetics at the center of evolutionary biology. Mayr (1991), in his own history, characterized ‘The Synthesis’ as a consensus that developed between geneticists (who focused on genes) and naturalists (who focused on phenotypes). It meant that we were all thinking and talking in terms of genes, even those of us who, like me, were naturalists working primarily on phenotypes (e.g., morphology, behavior, or taxonomic traits). A major change between that era (what I will call it the ‘Synthesis Era’) and the present age is an increased focus on the phenotype, including its development and plasticity. The 20th-century synthesis had not too much of genes but too little of phenotypes and their development. Here I briefly discuss some of the changes implied Foreword xi by a shift in evolutionary biology toward increased attention to the phenotype, especially its developmental plasticity. I also respond to some opinions, expressed in the present volume, that indicate resistance to such change. On the nature of selection. It is sometimes said that the role of plasticity for evolution is ‘controversial’ (see Futuyma 2021; Levis and Pfennig 2021; Pfennig 2021 and references therein). That seems to raise doubts about its importance. There may be unresolved questions about the role of developmental plasticity in a particular case or in a particular pattern of evolutionary genetic change, just as there may be unresolved questions about the role of mutation or of selection. But there can be no doubt that developmental plasticity needs to be recognized, alongside genes, as playing an important role in Darwinian (adaptive and social/sexual) evolution, one that needs to be taken into account by any general description of how Darwinian evolution works. Here is a quick summary of the rationale for that assertion:

• Darwinian evolution requires heritable change due to selection. • Selection depends on the existence of phenotypic variation. • All phenotypic variation comes from variation in development. • All variation in development comes from its responsiveness to inputs from two major sources—the genome and the environment. • Therefore, developmental plasticity—developmental responsiveness to environmental inputs—is important for Darwinian evolution.

An important point is that selection does not depend on the presence of genetic variation. It only requires phenotypic variation that affects fitness, regardless of the proximate cause of that variation. Of course, a genetic response to selection (genetic evolution) does depend on the presence of genetic variation. Note also that genetic change in response to selection—adaptive evolution—if it occurs, necessarily depends on, and therefore follows, selection. In this sense genes are virtually always followers in adaptive phenotypic evolution, a point (with one kind of exception) fur- ther discussed below. Failure to appreciate the fact that selection acts on variation in phenotypes—not genotypes—has led to some interesting mistaken ideas. One of my favorites, as a female animal behaviorist, is the ‘lek paradox’ (Borgia 1979). This is the seemingly paradoxical idea that female choice for traits in males—traits that are not associated with any direct fitness benefit (such as paternal care)—persists, even when strong sexual selection might be expected to eliminate genetic variation. The implication is that without genetic variation females would no longer choose. But female choice does not depend on genetic variation (Borgia refers to ‘genetic choice’). Instead, it depends on phenotypic variation among males which could persist indefinitely without genetic variation. Sexual selection would not stop. It would simply stop affecting evolution. The lek paradox has had the good result of stimulating a stream of ideas (continuing into the present; e.g., see Dugand et al. 2019) regarding the maintenance of genetic variation in populations. It has also provided theoretical support suggest- ing the widespread presence of standing genetic variation and therefore for the idea (e.g., in West-Eberhard 2003 and references therein) that selection does not await mutation to affect evolution. xii Foreword

On the origin of novel phenotypes and their reaction norms. There was a void— what Schlichting (2021) in this volume calls a “lacuna”—in our thinking, during the Synthesis Era: there was very little discussion about the origin of the complex phenotypic traits that interested naturalists. Futuyma (2021) raises several important questions about the relevance of developmental plasticity to filling that void. [Remember, this is a personal account of history so I need to explain why I will pay extra attention to Futuyma’s critique of ideas about plasticity in his chapter of this book. Doug Futuyma and I were graduate students and friends at the University of Michigan in the mid-1960s, where we were both steeped in the bur- geoning Evolutionary Synthesis. Our paths then diverged, Doug’s toward a thesis on Drosophila genetics and mine toward a thesis on the natural history and behavior of social wasps—taking us into different branches of the two whose consensus formed the Synthesis. So it is not surprising that we now have somewhat different views about the roles of developmental plasticity and genes in evolution. I will refer to some of them below, in the open spirit of the old Michigan debates.] Doug (henceforth, Futuyma) raises a question about origins in his discussion of reaction norms (Futuyma 2021). He notes, in a discussion of genetic assimilation, that “there is hardly any challenge to standard theory when derived characters are a fixed state of an advantageous ancestral reaction norm.” But, he points out, such discussions always begin with change in reaction norms that are already present in ancestral populations. That is (to insert my own words), they treat evolution as it has been treated in the past, without addressing the old void regarding origins. In fact, there is a great deal of information about the origin of reaction norms. But to take advantage of it you have to consider the genetic architecture of phenotypic traits. Phenotypic traits are characterized by both continuous variation (i.e., variation in the dimensions and regulation of traits, where environmental variation can be described in terms of reaction norms) and modularity of form (organization of phenotypes and gene expression into semi-discrete units). This means that the origin of a (new) phenotypic trait implies the origin of (new) reaction norms— environmentally influenced variation in the dimensions of the trait. And there is a great detail of information about the origin of new phenotypic traits, as discussed below. Given the genetic architecture of traits, thinking in terms of plastic and non-plastic genes (as in Scheiner and Levis 2021) is potentially confusing. Mechanistically, the locus of plasticity—of reaction norms and the on-off regulation of traits—does not reside in the nature of individual genes; it is a product of many kinds of condition- sensitive polygenic, quantitatively variable mechanisms, like hormones and other physiological systems (see Ledón-Rettig and Ragsdale 2021 in this volume). So it is not true that “The loss of plasticity requires the appearance of non-plastic genotypes in a population,” if that means the advent of a mutation (as in the example following that statement in Scheiner and Levis 2021). Schlichting (2021) gives a similar answer to Futuyma’s question about the origins of reaction norms, concluding that “Non-plasticity (i.e., canalization, robustness) is thus arguably a derived state in most biological systems.” Ledón-Rettig and Ragsdale (2021), also in this volume, show how physiological mechanisms can link environmental signals to both continuous and discrete variation in traits, with changes in Foreword xiii physiological systems thus capable of influencing the origin of both novel discrete traits and new reaction norms. The architecture of phenotypes ties the origin of new reaction norms to the origin of new semi-discrete traits. But how do those traits originate? Futuyma (2021) almost, but not quite, answers that question when he goes on to “find most interesting several cases in which the ancestral state seems not to have been an adaptive reaction norm.” To illustrate this, he cites studies that document the advent of novel phenotypes, one of them being the “curious case” of a novel resource-use morph found in spadefoot toad tadpoles, induced by a dietary manipulation and resembling a form established in a related species (described in Levis and Pfennig 2021; Pfennig 2021 in this volume). Futuyma notes that “The developmental response seems not to be an adaptation, even though it can have an advantageous effect.” That sentence could serve as a definition of a novel phenotype at its origin: it is a developmental anomaly that, like a genetic mutation, can have evolutionary potential; then, if it has an advantageous effect, it may become established (genetically accommodated) under selection in a population. It is worth asking, along with Futuyma (2021) in this volume, whether anomalies like the diet-induced morph of the spadefoot toads: “Are cases such as these odd, rare ‘accidents’ of development, rare enough to count for little?” The answer, of course, is that rare accidents of development, like genetic mutations, may count for a lot if they happen to be positively selected and become established traits—that was the point of the spadefoot toad tadpole example and others described in the present book (see especially Scheiner and Levis 2021). It is also shown dramatically by a study (Shubin et al. 1995) of newts, Taricha granulosa, where a phylogeny of salamanders was used to show how rare accidents of development can become established phenotypes: numerous anomalies seen in a large sample of that one species appeared in related species as alternative phenotypes and established traits (Figure 19.3 in Developmental Plasticity and Evolution). Such a pattern of ‘recurrence’ has been documented in numerous taxa (op. cit.). The origin of novel phenotypes due to developmental reorganization—a conse- quence of developmental plasticity—has also been very extensively documented (see Chapters 10–19 in Developmental Plasticity and Evolution). In a large collection of examples surveying numerous kinds of organisms, I found no case where it had been shown that a complex phenotype of the kind I was trying to understand was formed beginning with a mutation, followed by a series of mutations modifying it to produce a genetically and phenotypically complex adaptive trait. Although no such collection can be complete, if the successive-mutation hypothesis were a viable explanation for the evolution of complex phenotypes there should have been numerous well-documented examples. What I did find, to my surprise and satisfaction (as an amateur historian), is a very large number of origins by developmental reorganization that were a déjà vu of classical phylogenetic embryology—heterochrony, deletion, reversion, and four other kinds of developmental rearrangement, including correlated change in reaction norms of multiple traits showing extreme responses to stress. It matters little whether these developmental rearrangements were initiated by a mutation or an environmental induction, factors that are developmentally equiva- lent and easily interchangeable as initiators of phenotypes (see West-Eberhard 2003 xiv Foreword on interchangeability). Whatever the initiator, degree of environmental or genetic control can in principle be adjusted upward or downward by selection on polygenic regulatory mechanisms—pathways created in response to the initiator. Given the strength and variety of evidence that now indicates how developmental plasticity can be integrated with genetics to explain the origin and evolution of phenotypic traits, I regard the burden of proof to lie with those who favor some alternative approach. In sum, since all new phenotypes are subject to environmentally mediated variation in their dimensions and regulation—their reaction norms—as just mentioned, the abundant evidence on how new traits originate via developmental reorganization constitutes abundant evidence regarding the origin of new reaction norms. This should help to assuage Futuyma’s (2021) worry that the study of developmental plasticity “seems not to burrow into the origin of … ancestral reaction norms.” On the role of genes in adaptive evolution. Putting the phenotype in its proper place as a product of development as well as the object of selection leads to a deeper and clearer understanding of the role of genes in adaptive evolution than is possible in purely genetic terms. For example, a discussion of developmental plasticity may view gene products as part of the internal environment that affects a condition-dependent developmental response during ontogeny. Regard for gene products as part of the (internal) environment is implied in genetics by the term ‘epistasis,’ or gene-by-gene interaction, the dependence of a gene’s effect on genetic background (the nature of the other genes present). And, similarly, gene-by-environment interaction recognizes the importance of environmental variation for phenotypic form. Given such terms, it cannot be claimed that traditional genetics has ignored the importance of the environment or of the genotype as a whole. But epistasis, like gene-by-environment interaction, describes a statistical interaction, not a mechanistic developmental one. These quasi-causal terms for statistical correlations are potential traps for the inno- cent. For some, these terms may obscure the fact that research is needed to explain what causes those fundamental genetic phenomena to occur. The studies described in this book conveniently summarize in one place some of the ways in which looking at plasticity and development deepens understanding of the biology underlying patterns observed in genetics. For example, Goldstein and Ehrenreich (2021) discuss how genetics has moved in the direction of understanding mechanisms, and how it can now contribute to the discovery of underlying processes. And Ledón-Rettig and Ragsdale (2021) deepen evolutionary understanding of pleiotropy by discussing its physiological basis, especially focusing on hormones which have diverse (pleiotropic) effects on complex phenotypes. They discuss both the fundamental nature of pleiotropy and the coordinated origin of complex traits. During the Synthesis Era, both naturalists and geneticists assumed complex phenotypes to be underlain by sets of particular genes. Including development in the genetic theory gives substance to that assumption, and to Darwin’s link between the inheritance and the development of traits. But this link requires showing that the phenotypic traits under selection actually are underlain by coordinated sets of expressed genes. Twenty years ago there was indirect evidence for this from studies using electrophoresis and from biochemical analyses of variation in the timing of production of particular enzymes. Now there has been such an explosion of direct Foreword xv information on the molecular biology of gene expression and its relevance to adaptive evolution (e.g., see Schlichting 2021; Sultan 2021 in this volume) that it may seem strange that this has not always been obvious. This kind of progress in understanding the developmental genetics of conditionally expressed adaptive phenotypes means that the idea of developmental plasticity is permeating the collective understanding of genetics and evolution, whether plasticity is mentioned or not. It would be a mistake, however, to think that gene expression is the whole story. Developmental plasticity is a manifestation of pathways that connect the environment with the genome. Without these pathways, the genome would be inert. What might be called ‘intermediate processes’ are crucial—the connections made by biochemical signal-response interactions, hormone systems, and other physiological mechanisms. Physiology and cell biology are areas of mechanism-related biology that, like developmental biology, have been largely estranged from evolutionary biology in the past. They are now crucial contributors to understanding selectable variation and evolution, as evidenced by the discussion in LedÓn-Rettig and Ragsdale’s (2021) chapter in this volume. On the Baldwin effect, genetic accommodation, and genetic assimilation. As Futuyma (2021) says, current ideas about plasticity are compatible with those we learned as graduate students. But I am not as graciously forgiving as he is about the arguments that at that time dampened interest in the evolutionary importance of development and plasticity. Compatibility arguments are often preludes to dis- missals. For example, Simpson (1953) found the ‘Baldwin Effect’ fully compatible with modern evolutionary theory but lacking in evidence that “it is a frequent and important element in adaptation.” In those days, this was undoubtedly taken by many to mean that the Baldwin effect just wouldn’t be worth studying, since, according to this giant of evolutionary biology, “it is seldom assigned an important role in evolution” (p. 110; for discussions of the Baldwin effect in the present volume, see Diamond and Martin 2021; Futuyma 2021; Pfennig 2021, Box 3.2). The idea of evolution by genetic accommodation was bound to be a target of criti- cism because it not only accepts but also dares to extend the idea of genetic assimilation. Genetic assimilation was dismissed during the Synthesis as unworthy of special attention (Mayr 1963; see also Box 3.2 in Pfennig 2021 in this volume). It had a reputation among students of my generation as a crackpot idea with Lamarckian overtones. Futuyma (2021), in this volume, treats genetic accommodation and assimilation as he does the Baldwin effect: as having been “subject to debate” but “compatible with the theory that emerged from the Evolutionary Synthesis.” Nevertheless, even prior to the year 2001, when the writing of Developmental Plasticity and Evolution was finished, there were abundant data from molecular genetics (electrophoresis) and experiments in quantitative genetics showing the presence of sufficient genetic variation to support selection for virtually any selectively favored trait, including, as required for genetic assimilation, changes in the threshold for expression of conditionally expressed (environmentally induced) ones. Now it is even easier to find evidence for the necessary genetic variation using keywords like ‘standing genetic variation’ and ‘cryptic genetic variation’ (for examples in this volume, see Ledón-Rettig and Ragsdale 2021; Levis and Pfennig 2021; Pfennig 2021; Schlichting 2021). Two decades ago there were also numerous examples of transitions xvi Foreword from environmental to genetic determination of traits implying genetic assimilation and supported by phylogenies (e.g., in West-Eberhard 2003). Although Futuyma (2021) found phylogenetic support lacking for the polarity of these transitions, the phylogenies are hidden in plain view in numerous figures (e.g., Figures 5.15, 5.16, 12.3, 17.4, 19.1, 27.4, 28.1, 28.2, and 28.4) in West-Eberhard (2003). Genetic assimilation has survived to be understood as a selection-driven loss of plasticity, an important aspect of evolution, and a worthy topic for future research (see Scheiner and Levis 2021 in this volume). Evidence for polarity of change (direction of evolution, as from environmental to genetic determination) is essential for evolutionary transition hypotheses. But phylogenetic evidence need not involve mapping onto a phylogeny. Indeed, it is important to value the power of indirect evidence in evolutionary biology. Most of the evidence for natural selection in nature, for example, is an accumulation of indirect evidence that combines models and data testing the many implications of the idea (see also Lister 2021 in this volume on the evidence for plasticity in fossils). The likely polarity of a change can be deduced from various kinds of comparative evidence (see, for example, Schwander and Leimar 2011). For instance, the freshwater phenotype of some large anadromous fish populations, with yearly migrations of individuals between marine and freshwater environments, closely resembles the phenotypes of ‘landlocked’ non-migratory populations of the same region that are trapped in lakes, where the freshwater form is fixed. The freshwater form can be deduced with a high degree of probability to be derived from the developmentally plastic anadromous form common in the same region. Phenotype fixation can involve purely environmental change, due to an absence of conditions inducing an alternative form. So in this case showing fixation to involve genetic accommodation would require demon- strating reduced ability to switch to the marine form. But the polarity of the change is clear without a formal phylogeny. Waddington’s genetic assimilation can represent quantitative genetic change in the threshold for expression of a trait, moving it to a level where the trait is no longer expressed; or it can result from a mutation of major effect on regulation affecting a threshold (Waddington 1942, 1953). Such mutations of large effect make complex environmentally influenced human diseases like bipolar illness become ‘genetic’ or characteristic of families (West-Eberhard 2008a). Of the three examples of genetic assimilation described in detail by Scheiner and Levis (2021) in this volume, one involved a mutation (affecting a glycolipid layer on the heterocyst of a bacterium), while another (concerning spadefoot toad tadpoles) likely involved selection affecting standing (i.e., pre-existing) genetic variation. Schlichting (2021) cites reviews of genetic accommodation and describes several exemplary recent studies. It is difficult to define when genetic accommodation would stop in changing environments. So it could be said that all quantitative genetic change in the dimensions or regulation of established traits that is mediated by natural or artificial selection represents genetic accommodation. Clearly, then, genetic accommodation is nothing new. The fact that it fits readily with traditional ideas should give the idea a boost. But why give it a new name? First, giving genetic accommodation a new name draws attention to the special role of quantitative genetic change in the establishment of new qualitatively distinctive Foreword xvii

(discrete) traits. Second, the term genetic accommodation helps distinguish it from phenotypic accommodation (sensu West-Eberhard 2003, 2005)—adaptive phenotypic adjustment in the absence of genetic change following a novel or extreme input during development. Both phenotypic accommodation and genetic accommodation can contribute to the establishment of novel traits even though these two processes may be phenotypically indistinguishable without experimental tests. Finally, a third reason to coin the term genetic accommodation is to emphasize that trait establishment need not imply fixation (assimilation) with a complete and permanent loss of plasticity. Many traits show durable adaptive plasticity in their condition-sensitive regulation. For example, the prolific adaptive radiations of African lake cichlids, Hawaiian drosophilids, and Galapagos finches illustrate how marked and durable plasticity in morphology, biochemistry, and learning, respectively, can facilitate rapid evolution in multiple directions (see Chapter 28 in Developmental Plasticity and Evolution). Furthermore, some lineages change repeatedly between genetic and environmental control: some of the figures cited above as indicating genetic assimilation show transitions to environmental determination of trait expression as well. A term-lover could invent a silly term, like ‘genetic de-assimilation,’ or ‘genetic plastification,’ to contrast genetic assimilation with evolution in the opposite direction. But it seems preferable to use a term like ‘genetic accommodation’ for both directions of change, emphasizing their similarity. Both involve genetic change that adjusts the degree of environmental influence on trait expression. On genes as followers in adaptive evolution. According to Futuyma (2021), this “oft-quoted” statement from Developmental Plasticity and Evolution may have influenced “The critical reactions [to ideas regarding plasticity and evolution] of some traditional evolutionary biologists.” The reactions of traditional evolutionary biologists are of interest for general discussions of phenotypic plasticity like those of this book. Intuition tells me that adverse reactions to genes-as-followers may reflect a strong conviction that genes take the lead in evolution. It also occurs to me that such biologists are unlikely to read books like the present volume that care- fully examine an alternative view. The context of the genes-as-followers statement was to say that if developmental plasticity plays the role proposed for it in adaptive evolution, then genes are followers in adaptive evolution. Within that scheme, the majority of genetic change follows the origin of a developmentally reorganized phenotype: trait initiation is followed by selection and genetic change (genetic accommodation). Accordingly, genes could be leaders in adaptive evolution if a phenotype favored by selection originated due to a genetic mutation or a particular genetic configuration that happened to give rise to a favorable developmental novelty. Still, the majority of genetic change would likely be polygenic modification of the newly expressed trait, either increasing or decreasing the frequency of its expression. Not all traditional evolutionary biologists have reacted negatively to ideas about developmental plasticity implying a somewhat altered view of the role of genes in evolution. Ernst Mayr (1904–2005) noted in correspondence (17 May 2003) that it is a point that “will sink in only slowly… I remember how daring I felt when in 1963 I bluntly stated ‘the phenotype is the target of selection.’ At that time we did not yet have the faintest notion how this plasticity was regulated.” And (15 June 2004), xviii Foreword

“historians have failed to report how gene-centered evolutionary biology was from the 1920, to the 1960s.” Earlier Mayr (1991, p. 157) had identified the role of development in evolution as one of the frontiers of evolutionary biology “likely to see the greatest advances in the next ten or twenty years.” Is developmental plasticity universal? It is often said that plasticity is universal, or a universal property of living things (Chenard and Duckworth 2021; Pfennig 2021; Sultan 2021; see also Nijhout 2003). In one sense plasticity seems to be an “intrinsic property of organisms” (sensu Sultan 2021). It characterizes evolutionary genetics at its most fundamental level because all gene expression is condition dependent (see Schlichting 2021; see also Nijhout 1990): the genome is inert during its transmission between generations, to become important for development only when activated, a piece at a time, by particular developmental conditions. Saying that all gene expression is condition-sensitive is just an updated way of saying what has long been axiomatic in evolutionary biology—that organis- mic traits are products of genes and the environment. But extreme statements regarding universality may invite needless debate, so let’s just say that condition- sensitive—i.e., plastic—trait expression is extremely common. One reason for this is that plasticity, when advantageous, can be adjusted up or down under selection to an advantageous level that enables it to persist. That is a hypothesized role of genetic accommodation that sets it apart from genetic assimilation (West-Eberhard 2003), which eliminates, rather than maintains, phenotypic plasticity (see Scheiner and Levis 2021 in this volume). Ledón-Rettig and Ragsdale (2021) and Pfennig (2021) survey a multitude of ways in which condition-sensitive plastic responses get incorporated into development due to selection, helping to explain why plasticity is so common despite the fact that plasticity is not always advantageous and may be costly (Snell-Rood and Ehlman 2021). Plasticity builds upon itself, for it can use established developmental plasticity to yield new environmentally respon- sive traits via developmental reorganization when it is environmentally induced, a theme developed by Schlichting (2021). Studies that compare plasticity in different taxa need to refer to particular traits. It is not meaningful to classify species or other taxa as plastic or non-plastic and then compare, say, their rates of speciation or diversification without reference to some specific aspect of their phenotypes. Such enumerative tests of the importance of plasticity may be tempting in the age of meta-analyses of the literature but they are meaningless unless they are explicit about the trait whose plasticity is being com- pared. It is also tempting to debate whether or not plasticity promotes evolutionary change, as if it were a question of always or never doing so. Plasticity can or may promote evolutionary change: it can contribute to the phenotypic variation required for organisms to change under selection (see Pfennig 2021; Schlichting 2021 in this volume). However, this does not mean that plasticity always promotes evolutionary change (as discussed by Pfennig 2021 in this volume). The ability for plasticity to facilitate evolutionary change may also tempt thinking that it has evolved under selection for ‘evolvability’—the ability to evolve. Many factors, just mentioned as documented in this book, contribute to the commonness of plasticity, obviating the need to seek an explanation in terms of selection above the individual level, as required by the evolvability hypothesis. Similarly, the universal modular aspect of what we call ‘traits,’ which also contributes to evolvability, should Foreword xix not be regarded as a product of selection for evolvability per se. Instead, the universal modular (discrete) aspect of ‘traits’ is arguably due to the role of development in limiting connectedness at the time of trait origin (West-Eberhard 2019). The present volume indicates that Developmental Plasticity and Evolution is fast becoming an antique. In another 10 years, following the usual cycle of amnesia, it will be forgotten, whether due to dismissal or assimilation. The data it cites will endure; I still consult my battered copy of Mayr 1963 to see the examples cited and how they were used. This brings to mind a passage about facts and theories (‘views’) found in my even more battered copy of Darwin’s The Descent of Man and Selection in Relation to Sex (1871 [1874], p. 909). Darwin noted that facts endure even when false “but false views, if supported by some evidence, do little harm for every one takes a salutary pleasure in proving their falseness: and when this is done, one path towards error is closed and the road to truth is often at the same time opened.” I do not regard the present-day interest in developmental plasticity and evolution as an extension of the mid-20th-century synthesis as do some authors interested in developmental plasticity and evolution (e.g. see Pigliucci 2007; Laland et al. 2015). Instead it reaches back toward Darwin to rescue lost lines of thinking about the origins of selectable variation. Darwin’s integrated view of development and evolution was either sidelined, as in the Synthesis, or actively suppressed, as in the Lysenko era of Russian genetics (Wake 1986; Berg 1988), where there had been a vibrant and broadly integrative evolutionary genetics. The charismatic geneticist Theodosius Dobzhansky, a leader of the Synthesis who was trained in the Russian school, might have imported increased interest in development into the thinking of his time. But that was not his passion. Dobzhansky did bring Schmalhausen’s (1949 [1986]) book to the attention of English-speaking biologists, saying that “it supplies…an important missing link in the modern view of evolution” (Dobzhansky 1949 [1986]). It is gratifying to see the chapters of this book by a diversity of leaders in thinking about plasticity and evolution. I found some of the chapters breathtaking as synthetic summaries of modern findings, full of original thoughts on topics that have interested me for so long. They pinpoint objections, evaluate them, concisely present the authors’ latest ideas, and document consequences for evolution. Studies of plasticity bring developmental environments and phenotypes back toward the center of evolutionary biology, with an improved understanding of their relationship to evolutionary genetic change.

ACKNOWLEDGMENTS I thank Jessica Eberhard, William Eberhard, and David Pfennig for helpful comments. Douglas Futuyma responded rapidly to some last-minute questions.

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