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 plastic- ity-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 envi- ronmental 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 transmis- sion 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 evo- lutionary 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 expres- sion 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 chang- ing 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 phe- notypes 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, espe- cially 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 evolu- tion 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 unre- solved 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 with- out genetic variation. Sexual selection would not stop. It would simply stop affecting evolution. The lek paradox has