Epistasis and Evolution

The concept of epistasis was introduced into evolutionary theory more than a hundred years ago. Its history is marked by controversies regarding its importance for the evolutionary process, as exemplified by the debate between Ronald Fisher and Sewall Wright in the wake of the modern synthesis. In this case the disagreement was about the shape of the adaptive landscape, which is determined by epistasis. Wright believed that epistasis causes the adaptive landscape to be rugged with many local peaks, whereas Fisher viewed evolution as a smooth, steady progression toward a unique optimum. Even today, the different meanings attributed to epistasis continue to spawn confusion. Nevertheless, a consensus is emerging, according to which the term should be used to designate interactions between genetic effects on phenotypes in the broadest sense. Stated differently, in the presence of epistasis the phenotypic effects of a gene depend on its genetic context. In evolutionary theory the phenotype of primary interest is organismal fitness, but principally the concept applies to any genotype-phenotype map. Reflecting the Fisherian view, throughout the 20th century epistasis was often considered to be a residual perturbation on the main effects of individual genes. Following the advent of sequencing techniques providing insights into the molecular basis of genotype-phenotype maps, over the past two decades it has become clear, however, that epistasis is the rule rather than an exception. This has motivated a large number of empirical studies exploring the patterns and evolutionary consequences of epistasis across a wide range of scales of organismal and genomic complexity. Correspondingly, mathematical and computational tools have been developed for the analysis of experimental data, and models have been constructed to elucidate the mechanistic and statistical origins of genetic interactions. Despite a certain inherent vagueness, the concept takes center stage in modern evolutionary thought as a framework for organizing the accumulating understanding of the relationship among genotype, phenotype, and organism.

Evolution of Animal Mating Systems

Animal mating systems are fascinating and diverse, and their evolution is central to evolutionary biology. A mating system describes patterns and processes of how females and males mate and reproduce successfully, and how this relates to their reproductive ecologies, including demographic and environmental factors. One of the more stimulating challenges in biology is to provide a comprehensive explanation for the evolution of mating adaptations among animals. In the course of sexual reproduction, animals engage in a dizzying array of traits, behaviors, and strategies. Such diversity simultaneously requires and eludes categorization: it is required for a general understanding, but at once confounds any rigorous classification because an almost inexhaustible supply of animal examples disrupt otherwise neatly ordered systems (see Classifications of Animal Mating Systems). Historically, mating with a single partner was thought to be a common mating system among animals. However, increasing observations of multiple mating by both sexes, supported by genomic evidence of mixed parentage within families, has since revealed that strict genetic monogamy is rare. In this bibliography, the selected literature highlights a compelling diversity and flexibility among animal mating systems, and sexual selection emerges both as a contributing cause and consequence of this variation. Sexual selection plays a central role in animal mating system evolution, and key references provide insights into its operation before and after mating, and describe how it leads to the expression of secondary sexual traits and sexual conflicts. Efforts to explain diversity in animal mating systems have often focused on how acquiring mates or matings relates to variance in reproductive success. This variation and diversity can be approached at the level of an individual, among individuals in a population, or between species. However, a preoccupation with the mean or average pattern often leads to generalizations that obscure important diversity crucial to evolutionary understanding. To avoid unnecessary categorization, the presentation here focus`es on variation in mating patterns and contrasts multiple mating with mating with a single partner. Furthermore, it considers the wider effects of animal mating systems, and includes associations with patterns of parental care. The aim with this bibliography is to provide key citations demonstrating that animal mating systems evolve from diverse, interactive, complex and dynamic processes resulting in a variety of adaptive mating strategies in females and males. A grateful acknowledgment is given to C. Kvarnemo and D. Gwynne for insightful comments.

The Philosophy of Evolutionary Biology

Philosophy of evolutionary biology is a major subfield of philosophy of biology concerned with the methods, conceptual foundations, and implications of evolutionary biology. It also concerns relationships between evolutionary biology and neighboring fields, such as biochemistry, genetics, cell and molecular biology, developmental biology, and ecology. Initially, many of the questions of central concern to philosophy of biology grew out of general philosophy of science. For instance, one long-standing debate in philosophy of science concerns the matter of what is distinctive of scientific inquiry. Various criteria have been proposed, and much of the early work in philosophy of biology concerned whether evolutionary biology meets these criteria. Another long-standing debate in philosophy of science concerns whether there is any legitimate role for values in science. The study of the evolution of human behavior and cognition has been scrutinized as an instance of both potentially pernicious and positive influence of values in science. More recently, philosophers of biology both collaborate with and draw upon evolutionary biology to either address broader philosophical concerns, such as the nature of consciousness, or engage directly with debates internal to evolutionary biology. For example, philosophers have engaged in conceptual and methodological debates within evolutionary biology over the appropriate conditions for testing hypotheses about adaptation, the units, targets, or levels of selection, mechanisms and measures of inheritance, modes of phylogenetic inference, and classification and systematics. In this category, the line between science and philosophy blurs; participants in many of these debates include both philosophers and biologists. This entry will focus on philosophers’ contributions. To be sure, evolutionary biologists have contributed far more. Please see the Oxford Bibliographies on these topics for scientific contributions to all of these topics. I also urge readers to review the excellent Stanford Encyclopedia of Philosophy entries on topics including but not limited to “Evolution,” “Natural Selection,” “Teleological Notions in Biology,” “Units and Levels of Selection,” “Adaptationism,” “Evolutionary Genetics,” “Evolutionary Psychology,” and “Developmental Biology.”

Islands as Evolutionary Laboratories

Islands have inspired biologists for hundreds of years as locations that foster unique biotic assemblages and provide insights into ecological and evolutionary processes dictating life globally. Although by classic definition islands are subcontinental land masses surrounded by water, from a biological perspective, islands can be defined broadly as any isolated piece of habitat that is surrounded by distinct environmental conditions. Therefore the study of island biology applies to any area that is habitable for a given set of organisms and is separated from a source by an inhospitable matrix. Biological islands can include lakes surrounded by land and mountaintops, caves, and land fragments surrounded by habitat in which an organism of interest cannot survive or reproduce. Given sufficient isolation, these attributes can result in a distinctive biota.

Evolution and Development of Individual Behavioral Variation

What makes individuals unique? The answer to this question lies in understanding why and how individuals respond to numerous internal and external factors that they experience over their lifetimes. This fundamental question lies at the heart of the study of human and animal behavior and is best addressed by integrating both proximate and ultimate perspectives. From a proximate perspective, we need to understand the molecular, hormonal, and physiological pathways involved in enacting behavioral changes within individuals. From an ultimate perspective, we need to understand when and why behavior changes in response to different internal and external factors and whether such changes are adaptive, a result of constraints, or pathological. Research on this topic draws links across several fields including developmental and abnormal psychology, personality in humans and animals, developmental plasticity, and parental effects. The development of individual behavioral variation encompasses many different processes because there are so many ways that behavior can vary within and across individuals. This article considers behavioral variation in both of these respects, that is, within-individual plasticity and among-individual differences. Within an individual, behavioral plasticity describes the way in which behavior can change across the lifespan as a result of changes in internal factors such as maturational state, or as a result of salient experiences. Among individuals, differences in average behavior can be a result of individual differences in internal factors, such as genetic variation, variation in their experiences, and variation in how they respond to the same experiences. Traditionally, students of behavioral variation in humans and animals focused on describing the mean levels of behavior expressed by groups of individuals as a function of changes in age or in response to specific experiences. More recently evolutionary and behavioral ecologists have become interested in patterns of within-individual plasticity and among-individual differences in behavior, and the factors that contribute to their development, which is the focus of this review here.

Mutation Rate and Spectrum

Many an introductory or general overview of the biology of mutation begins with the phrase “mutation is the ultimate source of genetic variation.” In the absence of mutation, one genome sequence would eventually become fixed in every species, recombination would become irrelevant, and evolution would grind to a halt. Thus, metaphorically, mutation is the fuel of evolution. To begin, it is important to define what is meant by “mutation.” For the purposes of this article, mutation is defined as the condition in which homologous DNA sequence differs between the parent cell at its origin and the daughter cell at its origin. Of primary interest are those mutations that are heritable across generations. Mutations result either from errors during replication that are not repaired, or damage to nonreplicating DNA that is not repaired prior to the next round of replication. Both of those points of control admit many sources of variation. In this article, mutation is considered in two contexts. First, papers that investigate causes of variation in the mutational process, and second, papers that investigate consequences of variation in the mutational process. The former includes theoretical investigations of the evolution of the mutation rate, as well as empirical studies of variation in the rate and molecular spectrum of mutation within genomes and between individuals and higher taxa. The latter category includes both theoretical and empirical studies of how variation in either the rate or spectrum of mutation affects the phenotype, and especially fitness. The focus is broad, including classical one- and two-locus population genetics, modern sequence-based population genetics, molecular genetics, and quantitative genetics. Theoretical studies are overrepresented, and empirical studies are bimodally distributed, with modes at the old (“classical”) and very recent (“state of the art”).

Post-Copulatory Sexual Selection

The field of post-copulatory sexual selection investigates how female and male adaptations have evolved to influence the fertilization of eggs while optimizing fitness during and after copulation, when females mate with multiple males. When females are polyandrous (one female mates with multiple males), they may optimize their mating rate and control the outcome of mating interactions to acquire direct and indirect benefits. Polyandry may also favor the evolution of male traits that offer an advantage in post-copulatory male-male sperm competition. Sperm competition occurs when the sperm, seminal fluid, and/or genitalia of one male directly impacts the outcome of fertilization success of a rival male. When a female mates with multiple males, she may use information from a number of traits to choose who will sire her offspring. This cryptic female choice (CFC) to bias paternity can be based on behavioral, physiological, and morphological criteria (e.g., copulatory courtship, volume and/or composition of seminal fluid, shape of grasping appendages). Because male fitness interests are rarely perfectly aligned with female fitness interests, sexual conflict over mating and fertilization commonly occur during copulatory and post-copulatory interactions. Post-copulatory interactions inherently involve close associations between female and male reproductive characteristics, which in many species potentially include sperm storage and sperm movement inside the female reproductive tract, and highlight the intricate coevolution between the sexes. This coevolution is also common in genital morphology. The great diversity of genitalia among species is attributed to sexual selection. The evolution of genital attributes that allow females to maintain reproductive autonomy over paternity via cryptic female choice or that prevent male manipulation and sexual control via sexually antagonistic coevolution have been well documented. Additionally, cases where genitalia evolve through intrasexual competition are well known. Another important area of study in post-copulatory sexual selection is the examination of trade-offs between investments in pre-copulatory and post-copulatory traits, since organisms have limited energetic resources to allocate to reproduction, and securing both mating and fertilization is essential for reproductive success.

Cultural Evolution in Non-Human Animals

“Culture” is generally regarded as a population’s shared array of traditions, transmitted between individuals by processes of social learning, and which may persist from one generation to later ones. If we consider genetic material to provide the primary system of inheritance in living things, then social learning—learning from others—provides a second inheritance system in those species of animals that have the cognitive capacity to learn in this way. Once it was thought that cultural traditions inherited in this way were unique to, and defining of, our own species. This view was challenged by research arising particularly in the middle of the 20th century, which revealed evidence of the spread of innovations in the behavior of nonhuman species, generating traditions that passed from one generation to the next. Early examples included regional birdsong dialects and novel foraging techniques in Japanese macaque monkeys. Research over the last seventy years or so has accumulated a wealth of evidence that animal traditions exist in many aspects of behavior, from migration to mate choice and predator avoidance, and in numerous taxa including fish, birds, and mammals. Social learning has also been well documented in insects, although the existence of traditions in the wild remains less clear. Once such a second inheritance system does emerge, supporting the transmission of behavioral traditions, the potential exists for a second system of evolution—cultural evolution—which can be defined most simply as changes in culture over time. As in the case of organic evolution based on genetic inheritance, imperfect copying and sampling error may be sufficient to cause evolutionary changes, known as drift. Alternatively, some innovations may prove to be more adaptive than others, in which case we can expect the essential Darwinian processes of variation, selection, and inheritance to generate some directional cultural evolution. Both drift and Darwinian evolution have long been evident in human cultural evolution, but evidence has begun to accumulate for them also in nonhuman species. Humans additionally display cumulative culture, in which some form of progress builds cumulatively on the achievements of previous generations. Examples are legion, from the evolution of wheeled vehicles to languages and religions. A currently contentious issue is whether such cumulative cultural evolution is unique to our species, or is shared in some ways with others. Other current areas of uncertainty include which cognitive mechanisms underlie animal social learning and whether the precision of animal social learning can support long-lasting traditions; the degree to which animal cultures extend broadly enough across behavioral repertoires, or deeply enough in the complexity of individual traits, to be usefully compared to those of humans; and whether culture creates selection pressures that are long lasting enough to shape animals’ genomes. In general, while it is very clear that human culture is more extensive than in any other species, there is less agreement about which qualitative differences in psychological and cultural processes are responsible for this gulf.

Evolution of Reaction Norms

Phenotypic variance is a function of genetic variability, environmental variation, and the ways in which genetic and environmental variation interact, i.e., VG×E. Reaction norms are a means of conceptually, graphically, and mathematically describing this total variance and are a powerful tool for decomposing it into its constituent parts (i.e., nature, nurture, and, critically, their interaction). A reaction norm is defined as the range of phenotypes expressed by a genotype along an environmental gradient. It is represented by a linear or nonlinear function which describes the value of a phenotypic trait for a particular genotype or group of genotypes in different environments. As such, it is closely related to the concept of phenotypic plasticity, which can be represented by a reaction norm with a non-zero slope (i.e., the phenotype varies with respect to the environment). While the term (which originated as Reaktionsnorm) has been in use for over one hundred years, there has been some debate about the most appropriate way to describe it mathematically. Nonetheless, there is general consensus that a reaction norm has multiple properties, each of which can be the target of selection. Reaction norms are typically described as consisting of: (1) an intercept, elevation, or offset, which describes the mean trait value across all environments, (2) a slope, which quantifies the degree of trait plasticity, and (3) shape or curvature (e.g., linear, quadratic, monotonic). Evidence that trait means and plasticities can evolve separately underscores the necessity of applying a reaction norm framework for studying ecological and evolutionary responses to the environment, because measuring phenotypes in a single environmental context does not necessarily reflect their relative values or diversities in a different context. These contextual differences are particularly important in a world of rapid anthropogenic change and increasing environmental variability. Therefore, in addition to being fundamental to ecological and evolutionary phenomena, reaction norm evolution is relevant for diverse biological fields, including behavior and psychology, conservation and natural resource management, global change biology, agriculture and breeding programs, and human health. Given that evolutionary change is defined by genetic change, we focus this article on variation among reaction norms from different genotypes (i.e., reaction norms that have potentially evolved to be divergent from one another) as well as the forces that promote and constrain reaction norm evolution. For an overview of the literature on plasticity itself (keeping in mind that reaction norms need not be plastic), see the separate Oxford Bibliographies in Evolutionary Biology article Phenotypic Plasticity.

Evolution of Mutualism

Mutualisms, interactions between two species that benefit both, have long captured the public imagination. Humans are undeniably attracted to the idea of cooperation in nature. For thousands of years we have been seeking explanations for its occurrence in other organisms, often imposing our own motivations and mores in an effort to explain what we see. However, the importance of mutualisms lies much deeper than simply providing material for philosophical treatises and natural history documentaries. The influence of mutualisms transcends levels of biological organization from cells to populations, communities, and ecosystems. Mutualisms were key to the origin of eukaryotic cells and perhaps to the invasion of the land. Mutualisms occur in every aquatic and terrestrial habitat; indeed, ecologists now believe that almost every species on Earth is involved directly or indirectly in one or more of these interactions. Mutualisms are crucial to the reproduction and survival of many plants and animals and to nutrient cycles in ecosystems. Moreover, the ecosystem services mutualists provide (e.g., seed dispersal, pollination, and carbon, nitrogen, and phosphorus cycles resulting from plant-microbe interactions) are leading to these interactions increasingly being considered conservation priorities, while acute risks to their ecological and evolutionary persistence are being identified. The field of evolution came very late to the study of mutualism. Charles Darwin clearly recognized that it posed an evolutionary puzzle: In The Origin of Species, he wrote, “If it could be proved that any part of the structure of any one species had been formed for the exclusive good of another species, it would annihilate my theory, for such could not have been produced through natural selection.” The past 150 years have been devoted to trying to solve the challenge that Darwin posed to us.