The Role of Epigenetics in Evolution: The Extended Synthesis

The 21st century will be the century of biology, and evolutionary biology will be the linchpin. Yes, this is a bold statement, but it is certainly in keeping with Dobzhansky's famous dictum about evolution. Dobzhansky was one of the major architects of the Modern Synthesis. This book by Schlichting and Pigliucci (SP the Final Synthesis is just gathering steam. Note that these dates are just rough guides and not meant to imply that significant work did not occur outside those periods. What is critical is that within these periods the relevant disciplines all become focussed on the same research program. We are now in the midst of this final joining of biological disciplines. This joining, if history is a guide, will take the next couple of decades. This joining will be driven from the evolutionary side. It is the evolutionary side within which the disciplines are linked by a synthetic theory. The molecular side is primarily linked by a shared set of techniques and a viewpoint that centers all questions ultimately on DNA sequences. Because the evolution side is much more theory driven, that is where synthetic concepts tend to arise. This book by S&P is an excellent example of such theorydriven synthesis. Also, if truth be told, as a whole evolutionary biologists tend to have a larger perspective than those in many other biological disciplines. Looking back on the Modern Synthesis is useful for the task ahead (Mayr and Provine, 1980). In particular, if we learn anything from that episode in our history, we

Adaptive Phenotypic Plasticity: Target or By-Product of Selection in a Variable Environment?

A review of Evolution: The Extended Synthesis. Edited by Massimo Pigliucci and Gerd B. Muller. Cambridge (Massachusetts): MIT Press. $35.00. viii 495 p.; ill.; index. ISBN: 978-0-26251367-8. 2010. The “Modern Synthesis” (Huxley 1942) or “Evolutionary Synthesis” (Mayr and Provine 1980) that transpired in the 1930s and 1940s is generally considered the first major advance in evolutionary biology after Darwin’s great work. Its major accomplishments were the formulation of a theory of evolutionary processes by joining Mendelian genetics and Darwin’s theory (especially natural selection), the interpretation of the observations of paleontologists, systematists, and naturalists in terms of this theory, and the rejection of some anti-Darwinian ideas, such as neo-Lamarckism, orthogenesis, and the radical saltationism associated with Goldschmidt’s “systemic mutation” and “hopeful monsters.” The Modern Synthesis (MS) occurred before there existed any glimmering of the molecular basis of heredity, but nevertheless could later accommodate newly discovered phenomena such as transposable elements. Even today, the population genetic theory of the MS remains intact, although it is now the foundation for a greatly expanded superstructure. In contrast to genetics, development entered the MS chiefly in phenomenological terms, such as allometry and heterochrony, mostly in a macroevolutionary context. Experimental embryologists described phenomena such as gradients and induction, but hardly anything was known of the mechanisms of development, and so little could be said about the mechanistic basis of phenotypic evolution. With some notable exceptions (Collins 1986), ecology remained distant from evolutionary studies; the study of genetics and natural selection in natural populations had only just begun. Under these circumstances, the chief aim of forward-thinking evolutionary biologists had to be formulating and establishing a rigorous, genetically informed theory of evolutionary processes that could account for adaptation and speciation. During the 1950s and early 1960s, much of the research in evolutionary biology was directed toward developing evidence on major themes of the MS: documenting selection in natural populations, describing and attempting to account for genetic variation, and characterizing reproductive isolation and the geographic setting of speciation. Broad though their vision was, the architects of the MS focused on a narrower range of questions than Darwin had or than their successors would. Beginning in the 1960s, evolutionary science expanded greatly. For example, population genetics and ecology were united as “population biology,” later expanding into “evolutionary ecology” that applied evolutionary thinking to community ecology. The adaptive evolution of classes of phenotypic traits, based explicitly on individual selection, was the focus of new fields such as life-history evolution and behavioral ecology. The first steps were

The main topic of the paper is a discussion of the ways through which the theory of evolution remakes itself, changes and grows, keeping alive and reinforcing its Darwinian explanatory core. The theory shows a 150 years old history of theoretical and empirical extensions and revisions, without any apparent radical change of “paradigm” and without a rival Research Programme able to replace it. The ongoing transition from the Modern Synthesis (MS) to a so-called “Extended Evolutionary Synthesis” (ES) is here interpreted through the Methodology of Scientific Research Programmes, proposed by the epistemologist Imre Lakatos and updated. The current situation in evolutionary biology could be represented by a “progressive” shift of the Darwinian research programme, moving from the quite rigid theoretical framework of the standard version of Modern Synthesis (gradualism, extrapolationism, adaptationism) to the more inclusive and pluralistic “core” and “protective belt” of the Extended Synthesis. Promising and advanced researches – like those concerning evolutionary developmental biology (Evo-Devo), epigenetics, multiple ways of speciation and the role of structural internal constraints – find in this perspective a realistic interpretation as theoretical and empirical novelties with huge implications, nevertheless not incoherent with an extended Neo-Darwinian explanatory core. A Neo-Lakatosian approach seems useful when we discuss the extension of evolutionary models in non biological fields, avoiding the application of just metaphorical forms of “ultra-Darwinism.” This analysis in terms of a rational and continuous dynamics of growth of biological thought seems much needed also for a critical examination of some popular and radicalized controversies about the health of a no better defined “Darwinism or Neo-Darwinism.”

The mid-twentieth century saw the incorporation of Mendelian genetics into Darwinian theories of evolution. This foundation, termed the modern evolutionary synthesis, has developed into the primary current paradigm of evolutionary biology. However, the current modern synthesis does not include a role for epigenetics in developmental modifications or any mechanisms of non-genetic inheritance. With the recent expansion of epigenetic research into non-genetic mechanisms of adaptation and inheritance, there is a need to expand the modern synthesis into a new extended evolutionary theory. The current chapter presents the role of environmentally induced epigenetic transgenerational inheritance in evolutionary biology.KeywordsEpigeneticsEpigenetic transgenerational inheritancePhenotypic plasticityAdaptationEvolution

R.A. Fisher did much to bring about the ‘Modern Synthesis’ of Mendelian genetics with Darwinian natural selection into a theory of evolution that worked. This was the fruit of his dual talent as a mathematician (particularly, but not exclusively, as a statistician) and a biologist. Though his training also in physics would have led him to welcome the subsequent transformation of parts of biology to ‘hard science’ status in the field of molecular and developmental genetics, his insights were in the domain of transmission genetics, acting in populations, from which he derived a cluster of fecund hypotheses that have been particularly influential in the field of behavioral biology/evolutionary psychology.

Current knowledge of the genetic, epigenetic, behavioural and symbolic systems of inheritance requires a revision and extension of the mid-twentieth-century, gene-based, 'Modern Synthesis' version of Darwinian evolutionary theory. We present the case for this by first outlining the history that led to the neo-Darwinian view of evolution. In the second section we describe and compare different types of inheritance, and in the third discuss the implications of a broad view of heredity for various aspects of evolutionary theory. We end with an examination of the philosophical and conceptual ramifications of evolutionary thinking that incorporates multiple inheritance systems.

The present chapter focuses the role that paleoanthropology played in Charles Darwin’s views of evolution and in the formation of the synthetic theory or modern synthesis. It shows the close relationship between these evolutionary conceptions and the central goals of paleontology. Darwin was among the few naturalists in the nineteenth century who fully grasped the importance of fossils for an understanding of evolution. In spite of the incompleteness of the fossil record – and despite opposing views – he referred to paleontology in order to support his theories of common descent and continuous steps in evolutionary history (gradualism) as well as his views on the roots of humans in apelike mammals. Thus, in his The Descent of Man he argued, with some optimism, that the lack of fossil human remains was merely due to the fact that they had not yet been discovered. Indeed, paleoanthropology as a discipline at the interface between paleontology and anthropology was firmly established only in the late nineteenth century. However, up to now it has played a major part in the study of human evolution, and it has also helped in establishing the synthetic theory in the 1940s and 1950s, although only few of the leading proponents of this theory were explicitly concerned with paleoanthropological issues. The synthetic theory has been extraordinary successful as a comprehensive explanation of the mechanisms of evolutionary change of species (mainly variation and natural selection), and it has offered convincing evidence that the very same mechanisms fully apply to human evolution. This chapter also includes some (historical) examples which show how paleoanthropologists were sometimes misguided by ideological questions (Weltanschauungsfragen). Moreover, it brings into the focus some methodological issues and the shift of paleoanthropology from mere narrative to a theory-guided science. These issues are serious, since after all they affect the status of a discipline that is of crucial importance for a deep understanding of past and present conditions of humankind. Finally, therefore, the chapter considers the importance of paleoanthropology as the basis for a synthesis of anthropology that is increasingly needed as the latter gets more and more split into a growing number of highly specialized subdisciplines.

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.

ABSTRACTThe extended evolutionary synthesis (EES) is a school of thought that maintains that genetic determination and natural selection are over‐emphasized in the study of evolution at the expense of non‐genetic inheritance and processes of evolution beyond selection. Its proponents call for the de‐emphasis of genetics and the adoption of a broader model of inheritance that includes cultural and epigenetic transgenerational effects and strong adaptive phenotypic plasticity. Presenting itself as a radical alternative to what it claims is a rigid and ossified theoretical orthodoxy, the EES has lately gained considerable traction among scholars of human evolution, and a distinct sub‐branch of the EES unique to the biological anthropological study of human evolution has emerged (the EES in human evolution). To date, however, no direct comparison between the EES in human evolution and other contemporary evolutionary approaches has been attempted to evaluate whether the EES in human evolution affords researchers an edge in articulating good questions and structuring research programs to answer them. After reviewing the landscape of evolutionary theory, we evaluate whether the EES in human evolution is capable of delivering the processually pluralistic vision of evolution it has long promised and whether it brings something that the decades‐long ongoing synthesis (OS) of evolutionary theory since the modern synthesis does not. We then conduct a head‐to‐head comparison to evaluate the relative explanatory efficacy of the EES and our preferred OS theoretical framework on several issues of human morphological evolution. We demonstrate that evolutionary perspectives as drawn from the OS have a much more clarifying effect on the investigation of human evolution than their EES‐based competitor. Far from being a radical extension of evolutionary thought, the EES in human evolution offers little more than another idiom in which to tell adaptationist stories and triumphalist narratives of the ascent of humanity. Theory from the OS opens up new horizons of possible investigation of human evolution in a uniquely processually pluralistic and rigorous framework.

This paper examines the history of animal behavior studies after the synthesis period. Three episodes are considered: the adoption of the theory of natural selection, the mathematization of ideas, and the spread of molecular methods in behavior studies. In these three episodes, students of behavior adopted practices and standards developed in population ecology and population genetics. While they borrowed tools and methods from these fields, they made distinct uses (inclusive fitness method, evolutionary theory of games, emphasis on individual selection) that set them relatively apart and led them to contribute, in their own way, to evolutionary theory. These episodes also highlight some limitations of "conjunction narratives" centered on the relation between a discipline and the modern synthesis. A trend in conjunction narratives is to interpret any development related to evolution in a discipline as an "extension," an "integration," or as a "delayed" synthesis. I here suggest that this can lead to underestimate discontinuities in the history of evolutionary biology.

The adaptive landscape metaphor is one of the most persistent in evolutionary biology, and has generated much theoretical debate (if far less empirical investigation). This chapter briefly traces the history of the concept since its introduction by Sewall Wright in the 1930s. It then distinguishes four types of landscapes pertinent to evolutionary theory: fitness landscapes, adaptive landscapes, fitness surfaces, and morphospaces. These are more or less loosely related to each other, and sometimes the relationship is complex and difficult to explore empirically. The chapter argues that some versions of the landscape metaphor have lost their utility and should be replaced by more sophisticated metaphors, or abandoned altogether. It suggests that — somewhat surprisingly — the most useful type of landscape may turn out to be the morphospace, a concept that allows for a productive bridge between theoretical analyses and empirical results, especially in fields such as palaeontology and evolutionary developmental biology. In particular, the chapter discusses examples from the paleontological literature that constitute instances of truly (and stunningly) predictive theoretical analysis in what is often considered an entirely descriptive historical science.

Understanding the evolutionary causes of phenotypic variation among populations has long been a central theme in evolutionary biology. Several factors can influence phenotypic divergence, including geographic isolation, genetic drift, divergent natural or sexual selection, and phenotypic plasticity. But the relative importance of these factors in generating phenotypic divergence in nature is still a tantalizing and unresolved problem in evolutionary biology. The origin and maintenance of phenotypic divergence is also at the root of many ongoing debates in evolutionary biology, such as the extent to which gene flow constrains adaptive divergence (Garant et al. 2007) and the relative importance of genetic drift, natural selection, and sexual selection in initiating reproductive isolation and speciation (Coyne & Orr 2004). In this issue, Wang & Summers (2010) test the causes of one of the most fantastic examples of phenotypic divergence in nature: colour pattern divergence among populations of the strawberry poison frog (Dendrobates pumilio) in Panama and Costa Rica (Fig. 1). This study provides a beautiful example of the use of the emerging field of landscape genetics to differentiate among hypotheses for phenotypic divergence. Using landscape genetic analyses, Wang & Summers were able to reject the hypotheses that colour pattern divergence is due to isolation-by-distance (IBD) or landscape resistance. Instead, the hypothesis left standing is that colour divergence is due to divergent selection, in turn driving reproductive isolation among populations with different colour morphs. More generally, this study provides a wonderful example of how the emerging field of landscape genetics, which has primarily been applied to questions in conservation and ecology, now plays an essential role in evolutionary research.

When Charles Darwin was developing his ideas for On the Origin of Species, the most widely accepted estimates of Earth’s age were those of William Thomson (later Lord Kelvin). Kelvin used calculations involving thermodynamics to argue that Earth is only 20–100 million years old—an age far too brief to accommodate evolution by natural selection. Darwin referred to Thomson’s claim as one of his “sorest troubles,” for Darwin understood that the history of life on Earth ultimately relies on geology. Darwin suspected that Earth was much older than Thomson claimed, but Thomson’s enormous stature as a scientist obliged Darwin to reconcile his claims with Kelvin’s data. To accommodate Kelvin’s timeline, Darwin proposed pangenesis as an explanation of inheritance (i.e., every sperm and egg contained “gemmules thrown off from each different unit throughout the body”). Darwin’s explanation sped evolution while avoiding Lamarck’s quasi-spiritual sources of acquired traits. However, Darwin’s explanation of inheritance was wrong (see discussion in Moore et al. 2009a). The age of Earth remains a divisive topic in the modern evolution–creationism controversy. Whereas mainstream science has long acknowledged that Earth is approximately 4.5 billion years old, a vocal group of citizens and religious activists continue to insist that Earth is less than 10,000 years old. Although most geocentrists and flat-Earth advocates have capitulated to scientific evidence, young-Earth creationists continue to reject scientific evidence in favor of religious dictum to claim that Earth is less than 10,000 years old. These antiscience claims have been surprisingly popular with the public. For example, a Gallup Poll in early 2009 reported that “On Darwin’s [200th] Birthday, Only 4 in 10 Believe in Evolution” (Newport 2009), and Berkman et al. (2008) noted that “16% [of biology teachers] believed that human beings were created by God in their present form at one time within the last 10,000 years.” In another study, 12.5% of students were young-Earth creationists (Rutledge and Warden 2000), as are 10%–14% of biology majors (Moore and Cotner 2009). Answers in Genesis’ (AiG) Creation Museum, along with the $27 million in donations required to build it, attest to the appeal of young-Earth creationism. Indeed, AiG’s income for 2005 exceeded $13 million, and that of the Institute for Creation Research (ICR, another religious organization based on young-Earth creationism) exceeded $7 million. For comparison, the 2005 income of National Center for Science Education—the nation’s leading organization that defends the teaching of evolution in public schools—was

Most biologists agree that evolution is contingent on inherited information shaped by natural selection. This apparent consensus could be taken to indicate agreement on the forces shaping evolution, but vivid discussions reveal divergences on how evolution is perceived. The predominant Modern Synthesis (MS) paradigm holds the position that evolution occurs through random changes acting on genomic inheritance. However, studies from recent decades have revealed that evolutionary inheritance also includes DNA-methylation, RNA, symbionts, and culture, among other factors. This has fueled a demand of a broader evolutionary perspective, for example from the proponents of the Extended Evolutionary Synthesis (EES). Despite fundamental disagreements the different views agree that natural selection happens through dissimilar perpetuation of inheritable information. Yet, neither the MS, nor the ESS dwell extensively on the nature of hereditary information. We do - and conclude that information in and of itself is immaterial. We then argue that the quality upon which natural selection acts henceforth is also immaterial. Based on these notions, we arrive at the information-centric Information Continuum Model (ICM) of evolution. The ICM asserts that hereditary information is embedded in diverse physical forms (DNA, RNA, symbionts etc.) representing a continuum of evolutionary qualities, and that information may migrate between these physical forms. The ICM leaves theoretical exploration of evolution unrestricted by the limitations imposed by the individual physical forms wherein the hereditary information is embedded (e.g. genomes). ICM bestows us with a simple heuristic model that adds explanatory dimensions to be considered in the evolution of biological systems.