The Baldwin effect and genetic assimilation: revisiting two mechanisms of evolutionary change mediated by phenotypic plasticity

Two different, but related, evolutionary theories pertaining to phenotypic plasticity were proposed by James Mark Baldwin and Conrad Hal Waddington. Unfortunately, these theories are often confused with one another. Baldwin's notion of organic selection posits that plasticity influences whether an individual will survive in a new environment, thus dictating the course of future evolution. Heritable variations can then be selected upon to direct phenotypic evolution (i.e., "orthoplasy"). The combination of these two processes (organic selection and orthoplasy) is now commonly referred to as the "Baldwin effect." Alternately, Waddington's genetic assimilation is a process whereby an environmentally induced phenotype, or "acquired character," becomes canalized through selection acting upon the developmental system. Genetic accommodation is a modern term used to describe the process of heritable changes that occur in response to a novel induction. Genetic accommodation is a key component of the Baldwin effect, and genetic assimilation is a type of genetic accommodation. I here define both the Baldwin effect and genetic assimilation in terms of genetic accommodation, describe cases in which either should occur in nature, and propose that each could play a role in evolutionary diversification.     

How stabilizing selection and nongenetic inheritance combine to shape the evolution of phenotypic plasticity

Relatively little is known about whether and how nongenetic inheritance interacts with selection to impact the evolution of phenotypic plasticity. Here, we empirically evaluated how stabilizing selection and a common form of nongenetic inheritance—maternal environmental effects—jointly influence the evolution of phenotypic plasticity in natural populations of spadefoot toads. We compared populations that previous fieldwork has shown to have evolved conspicuous plasticity in resource‐use phenotypes (“resource polyphenism”) with those that, owing to stabilizing selection favouring a narrower range of such phenotypes, appear to have lost this plasticity. We show that: (a) this apparent loss of plasticity in nature reflects a condition‐dependent maternal effect and not a genetic loss of plasticity, that is “genetic assimilation,” and (b) this plasticity is not costly. By shielding noncostly plasticity from selection, nongenetic inheritance generally, and maternal effects specifically, can preclude genetic assimilation from occurring and consequently impede adaptive (genetic) evolution.     

A heuristic model on the role of plasticity in adaptive evolution: plasticity increases adaptation,population viability and genetic variation

An ongoing new synthesis in evolutionary theory is expanding our view of the sources of heritable variation beyond point mutations of fixed phenotypic effects to include environmentally sensitive changes in gene regulation. This expansion of the paradigm is necessary given ample evidence for a heritable ability to alter gene expression in response to environmental cues. In consequence, single genotypes are often capable of adaptively expressing different phenotypes in different environments, i.e. are adaptively plastic. We present an individual-based heuristic model to compare the adaptive dynamics of populations composed of plastic or non-plastic genotypes under a wide range of scenarios where we modify environmental variation, mutation rate and costs of plasticity. The model shows that adaptive plasticity contributes to the maintenance of genetic variation within populations, reduces bottlenecks when facing rapid environmental changes and confers an overall faster rate of adaptation. In fluctuating environments, plasticity is favoured by selection and maintained in the population. However, if the environment stabilizes and costs of plasticity are high, plasticity is reduced by selection, leading to genetic assimilation, which could result in species diversification. More broadly, our model shows that adaptive plasticity is a common consequence of selection under environmental heterogeneity, and hence a potentially common phenomenon in nature. Thus, taking adaptive plasticity into account substantially extends our view of adaptive evolution.     

Gene regulation,quantitative genetics and the evolution of reaction norms

Summary The ideas of phenotypic plasticity and of reaction norm are gaining prominence as important components of theories of phenotypic evolution. Our understanding of the role of phenotypic plasticity as an adaptation of organisms to variable environments will depend on (1) the form(s) of genetic and developmental control exerted on the shape of the reaction norm and (2) the nature of the constraints on the possible evolutionary trajectories in multiple environments. In this paper we identify two categories of genetic control of plasticity: allelic sensitivity and gene regulation. These correspond generally to two classes of response by the developmental system to environmental change: phenotypic modulation, in which plastic responses are a continuous and proportional function of environmental stimuli and developmental conversion, where responses tend to be not simply proportional to the stimuli. We propose that control of plasticity by regulatory actions has distinct advantages over simple allelic sensitivity: stability of phenotypic expression, capacity for anticipatory response and relaxation of constraints due to genetic correlations. We cite examples of the extensive molecular evidence for the existence of environmentally-cued gene regulation leading to developmental conversion. The results of quantitative genetic investigations on the genetics and evolution of plasticity, as well as the limits of current approaches are discussed. We suggest that evolution of reaction norms would be affected by the ecological context (i.e. spatial versus temporal variation, hard versus soft selection, and fine versus coarse environmental grain). We conclude by discussing some empirical approaches to address fundamental questions about plasticity evolution.     

Developmental capacitance, genetic accommodation, and adaptive evolution

The concept of genetic accommodation remains controversial, in part because it remains unclear whether evolution by genetic accommodation forces a revolution, or merely a shift in emphasis, in our understanding of how evolution produces adaptive new traits. Here I outline a perspective that largely favors the latter view. I argue that evolution by genetic accommodation can easily be integrated into traditional evolutionary concepts. At the same time, evolution by genetic accommodation invites novel empirical and theoretical approaches that may allow biologists to push the boundaries of our current understanding of the process of evolution and to solve some long-standing controversies. Specifically, I discuss the role of developmental mechanisms as natural, and likely ubiquitous, capacitors of cryptic genetic variation, and the role of environmental perturbations as mechanisms by which such variation can become visible to selection on an individual to population-wide scale. I argue that in combination, developmental capacitance and large-scale environmental perturbations have the potential to facilitate rapid evolution including the origin of novel adaptive features while circumventing otherwise powerful genetic and population-biological constraints on adaptive evolution. I end by highlighting several promising avenues for future empirical research to explore the mechanisms and significance of evolution by genetic accommodation.     

The role of developmental plasticity in evolutionary innovation

Explaining the origins of novel traits is central to evolutionary biology. Longstanding theory suggests that developmental plasticity, the ability of an individual to modify its development in response to environmental conditions, might facilitate the evolution of novel traits. Yet whether and how such developmental flexibility promotes innovations that persist over evolutionary time remains unclear. Here, we examine three distinct ways by which developmental plasticity can promote evolutionary innovation. First, we show how the process of genetic accommodation provides a feasible and possibly common avenue by which environmentally induced phenotypes can become subject to heritable modification. Second, we posit that the developmental underpinnings of plasticity increase the degrees of freedom by which environmental and genetic factors influence ontogeny, thereby diversifying targets for evolutionary processes to act on and increasing opportunities for the construction of novel, functional and potentially adaptive phenotypes. Finally, we examine the developmental genetic architectures of environment-dependent trait expression, and highlight their specific implications for the evolutionary origin of novel traits. We critically review the empirical evidence supporting each of these processes, and propose future experiments and tests that would further illuminate the interplay between environmental factors, condition-dependent development, and the initiation and elaboration of novel phenotypes.     

Evolution of “determinants” in sex-determination: A novel hypothesis for the origin of environmental contingencies in avian sex-bias

Sex-determination is commonly categorized as either “genetic” or “environmental”—a classification that obscures the origin of this dichotomy and the evolution of sex-determining factors. The current focus on static outcomes of sex-determination provides little insight into the dynamic developmental processes by which some mechanisms acquire the role of sex determinants. Systems that combine “genetic” pathways of sex-determination (i.e., sex chromosomes) with “environmental” pathways (e.g., epigenetically induced segregation distortion) provide an opportunity to examine the evolutionary relationships between the two classes of processes and, ultimately, illuminate the evolution of sex-determining systems. Taxa with sex chromosomes typically undergo an evolutionary reduction in size of one of the sex chromosomes due to suppressed recombination, resulting in pronounced dimorphism of the sex chromosomes, and setting the stage for emergence of epigenetic compensatory mechanisms regulating meiotic segregation of heteromorphic sex chromosomes. Here we propose that these dispersed and redundant regulatory mechanisms enable environmental contingency in genetic sex-determination in birds and account for frequently documented context-dependence in avian sex-determination. We examine the evolution of directionality in such sex-determination as a result of exposure of epigenetic regulators of meiosis to natural selection and identify a central role of hormones in integrating female reproductive homeostasis, resource allocation to oocytes, and offspring sex. This approach clarifies the evolutionary relationship between sex-specific molecular genetic mechanisms of sex-determination and non-sex-specific epigenetic regulators of meiosis and demonstrates that both can determine sex. Our perspective shows how non-sex-specific mechanisms can acquire sex-determining function and, by establishing the explicit link between physiological integration of oogenesis and sex-determination, opens new avenues to the studies of adaptive sex-bias and sex-specific resource allocation in species with genetic sex-determination.     

Genetic evolution,plasticity, and bet‐hedging as adaptive responses to temporally autocorrelated fluctuating selection: A quantitative genetic model

Adaptive responses to autocorrelated environmental fluctuations through evolution in mean reaction norm elevation and slope and an independent component of the phenotypic variance are analyzed using a quantitative genetic model. Analytic approximations expressing the mutual dependencies between all three response modes are derived and solved for the joint evolutionary outcome. Both genetic evolution in reaction norm elevation and plasticity are favored by slow temporal fluctuations, with plasticity, in the absence of microenvironmental variability, being the dominant evolutionary outcome for reasonable parameter values. For fast fluctuations, tracking of the optimal phenotype through genetic evolution and plasticity is limited. If residual fluctuations in the optimal phenotype are large and stabilizing selection is strong, selection then acts to increase the phenotypic variance (bet‐hedging adaptive). Otherwise, canalizing selection occurs. If the phenotypic variance increases with plasticity through the effect of microenvironmental variability, this shifts the joint evolutionary balance away from plasticity in favor of genetic evolution. If microenvironmental deviations experienced by each individual at the time of development and selection are correlated, however, more plasticity evolves. The adaptive significance of evolutionary fluctuations in plasticity and the phenotypic variance, transient evolution, and the validity of the analytic approximations are investigated using simulations.     

Evolution of ontogeny: linking epigenetic remodeling and genetic adaptation in skeletal structures

Evolutionary diversifications are commonly attributed to thecontinued modifications of a conserved genetic toolkit of developmentalpathways, such that complexity and convergence in organismalforms are assumed to be due to similarity in genetic mechanismsor environmental conditions. This approach, however, confoundsthe causes of organismal development with the causes of organismaldifferences and, as such, has only limited utility for addressingthe cause of evolutionary change. Molecular mechanisms thatare closely involved in both developmental response to environmentalsignals and major evolutionary innovations and diversificationsare uniquely suited to bridge this gap by connecting explicitlythe causes of within-generation variation with the causes ofdivergence of taxa. Developmental pathways of bone formationand a common role for bone morphogenetic proteins (BMPs) inboth epigenetic bone remodeling and the evolution of major adaptivediversifications provide such opportunity. We show that variationin timing of ossification can result in similar phenotypic patternsthrough epigenetically induced changes in gene expression andpropose that both genetic accommodation of environmentally induceddevelopmental pathways and flexibility in development acrossenvironments evolve through heterochronic shifts in bone maturationrelative to exposure to unpredictable environments. We suggestthat such heterochronic shifts in ossification can not onlybuffer development under fluctuating environments while maintainingepigenetic sensitivity critical for normal skeletal formation,but also enable epigenetically induced gene expression to generatespecialized morphological adaptations. We review studies ofenvironmental sensitivity of BMP pathways and their regulationof formation, remodeling, and repair of cartilage and bone toexamine the hypothesis that BMP-mediated skeletal adaptationsare facilitated by evolved reactivity of BMPs to external signals.Surprisingly, no empirical study to date has identified themolecular mechanism behind developmental plasticity in skeletaltraits. We outline a conceptual framework for future studiesthat focus on mediation of phenotypic plasticity in skeletaldevelopment by the patterns of BMP expression.     

Selection on heritable seasonal phenotypic plasticity of body mass

The ability to cope with environmental change is fundamental to a species' evolution. Organisms can respond to seasonal environmental variation through phenotypic plasticity. The substantial plasticity in body mass of temperate species has often been considered a simple consequence of change in environmental quality, but could also have evolved as an adaptation to seasonality. We investigated the genetic basis of, and selection acting on, seasonal plasticity in body mass for wild bighorn sheep ewes (Ovis canadensis) at Ram Mountain, Alberta, under two contrasting environmental conditions. Heritability of plasticity, estimated as mass-specific summer and winter mass changes, was low but significant. The additive genetic variance component of relative summer mass change was greater under good environmental conditions (characterized by a population increase and high juvenile survival) than under poor conditions (population decrease and low juvenile survival). Additive genetic variance of relative winter mass change appeared independent of environmental conditions. We found evidence of selection on summer (relative) and winter (relative and absolute) mass change. For a given mass, more plastic individuals (with greater seasonal mass changes) achieve greater fitness through reproduction in the following year. However, genetic correlations between mass parameters were positive. Our study supports the hypothesis that seasonal plasticity in body mass in vertebrates is an adaptation that evolved under natural selection to cope with environmental variation but genetic correlations with other traits might limit its evolutionary potential.     

Does phenotypic plasticity initiate developmental bias?

The generation of variation is paramount for the action of natural selection. Although biologists are now moving beyond the idea that random mutation provides the sole source of variation for adaptive evolution, we still assume that variation occurs randomly. In this review, we discuss an alternative view for how phenotypic plasticity, which has become well accepted as a source of phenotypic variation within evolutionary biology, can generate nonrandom variation. Although phenotypic plasticity is often defined as a property of a genotype, we argue that it needs to be considered more explicitly as a property of developmental systems involving more than the genotype. We provide examples of where plasticity could be initiating developmental bias, either through direct active responses to similar stimuli across populations or as the result of programmed variation within developmental systems. Such biased variation can echo past adaptations that reflect the evolutionary history of a lineage but can also serve to initiate evolution when environments change. Such adaptive programs can remain latent for millions of years and allow development to harbor an array of complex adaptations that can initiate new bouts of evolution. Specifically, we address how ideas such as the flexible stem hypothesis and cryptic genetic variation overlap, how modularity among traits can direct the outcomes of plasticity, and how the structure of developmental signaling pathways is limited to a few outcomes. We highlight key questions throughout and conclude by providing suggestions for future research that can address how plasticity initiates and harbors developmental bias.     

Plasticity paves the way in an adaptive radiation

Phenotypic plasticity has been hypothesized to play a central role in the evolution of phenotypic diversity across species (West‐Eberhard 2003 ). Through ‘genetic assimilation’, phenotypes that are initially environmentally induced within species become genetically fixed over evolutionary time. While genetic assimilation has been shown to occur in both the laboratory and the field (Waddington 1953 ; Aubret & Shine 2009 ), it remains to be shown whether it can account for broad patterns of phenotypic diversity across entire adaptive radiations. Furthermore, our ignorance of the underlying molecular mechanisms has hampered our ability to incorporate phenotypic plasticity into models of evolutionary processes. In this issue of Molecular Ecology, Parsons et al. ( 2016 ) take a significant step in filling these conceptual gaps making use of cichlid fishes as a powerful study system. Cichlid jaw and skull morphology show adaptive, plastic changes in response to early dietary experiences (Fig. 1). In this research, Parsons et al. ( 2016 ) first show that the direction of phenotypic plasticity aligns with the major axis of phenotypic divergence across species. They then dissect the underlying genetic architecture of this plasticity, showing that it is specific to the developmental environment and implicating the patched locus in genetic assimilation (i.e. a reduction in the environmental sensitivity of that locus in the derived species).     

Developmental interactions and the constituents of quantitative variation

Development is the process by which genotypes are transformed into phenotypes. Consequently, development determines the relationship between allelic and phenotypic variation in a population and, therefore, the patterns of quantitative genetic variation and covariation of traits. Understanding the developmental basis of quantitative traits may lead to insights into the origin and evolution of quantitative genetic variation, the evolutionary fate of populations, and, more generally, the relationship between development and evolution. Herein, we assume a hierarchical, modular structure of trait development and consider how epigenetic interactions among modules during ontogeny affect patterns of phenotypic and genetic variation. We explore two developmental models, one in which the epigenetic interactions between modules result in additive effects on character expression and a second model in which these epigenetic interactions produce nonadditive effects. Using a phenotype landscape approach, we show how changes in the developmental processes underlying phenotypic expression can alter the magnitude and pattern of quantitative genetic variation. Additive epigenetic effects influence genetic variances and covariances, but allow trait means to evolve independently of the genetic variances and covariances, so that phenotypic evolution can proceed without changing the genetic covariance structure that determines future evolutionary response. Nonadditive epigenetic effects, however, can lead to evolution of genetic variances and covariances as the mean phenotype evolves. Our model suggests that an understanding of multivariate evolution can be considerably enriched by knowledge of the mechanistic basis of character development.     

Rapid adaptation: a new dimension for evolutionary perspectives in ecology

Although the study of adaptation is central to biology, two types of adaptation are recognized in the biological field: physiological adaptation (accommodation or acclimation; an individual organism’s phenotype is adjusted to its environment) and evolutionary–biological adaptation (adaptation is shaped by natural selection acting on genetic variation). The history of the former concept dates to the late nineteenth and early twentieth centuries, and has more recently been systemized in the twenty-first century. Approaches to the understanding of phenotypic plasticity and learning behavior have only recently been developed, based on cellular–histological and behavioral–neurobiological techniques as well as traditional molecular biology. New developments of the former concepts in phenotypic plasticity are discussed in bacterial persistence, wing di-/polymorphism with transgenerational effects, polyphenism in social insects, and defense traits for predator avoidance, including molecular biology analyses. We also discuss new studies on the concept of genetic accommodation resulting in evolution of phenotypic plasticity through a transgenerational change in the reaction norm based on a threshold model. Learning behavior can also be understood as physiological phenotypic plasticity, associating with the brain–nervous system, and it drives the accelerated evolutionary change in behavioral response (the Baldwin effect) with memory stock. Furthermore, choice behaviors are widely seen in decision-making of animal foragers. Incorporating flexible phenotypic plasticity and learning behavior into modeling can drastically change dynamical behavior of the system. Unification of biological sciences will be facilitated and integrated, such as behavioral ecology and behavioral neurobiology in the area of learning, and evolutionary ecology and molecular developmental biology in the theme of phenotypic plasticity.     

Epigenetics in natural animal populations

Phenotypic plasticity is an important mechanism for populations to buffer themselves from environmental change. While it has long been appreciated that natural populations possess genetic variation in the extent of plasticity, a surge of recent evidence suggests that epigenetic variation could also play an important role in shaping phenotypic responses. Compared with genetic variation, epigenetic variation is more likely to have higher spontaneous rates of mutation and a more sensitive reaction to environmental inputs. In our review, we first provide an overview of recent studies on epigenetically encoded thermal plasticity in animals to illustrate environmentally‐mediated epigenetic effects within and across generations. Second, we discuss the role of epigenetic effects during adaptation by exploring population epigenetics in natural animal populations. Finally, we evaluate the evolutionary potential of epigenetic variation depending on its autonomy from genetic variation and its transgenerational stability. Although many of the causal links between epigenetic variation and phenotypic plasticity remain elusive, new data has explored the role of epigenetic variation in facilitating evolution in natural populations. This recent progress in ecological epigenetics will be helpful for generating predictive models of the capacity of organisms to adapt to changing climates.     

Epigenetic population differentiation in field‐ and common garden‐grown Scabiosa columbaria plants

Populations often differ in phenotype and these differences can be caused by adaptation by natural selection, random neutral processes, and environmental responses. The most straightforward way to divide mechanisms that influence phenotypic variation is heritable variation and environmental‐induced variation (e.g., plasticity). While genetic variation is responsible for most heritable phenotypic variation, part of this is also caused by nongenetic inheritance. Epigenetic processes may be one of the underlying mechanisms of plasticity and nongenetic inheritance and can therefore possibly contribute to heritable differences through drift and selection. Epigenetic variation may be influenced directly by the environment, and part of this variation can be transmitted to next generations. Field screenings combined with common garden experiments will add valuable insights into epigenetic differentiation, epigenetic memory and can help to reveal part of the relative importance of epigenetics in explaining trait variation. We explored both genetic and epigenetic diversity, structure and differentiation in the field and a common garden for five British and five French Scabiosa columbaria populations. Genetic and epigenetic variation was subsequently correlated with trait variation. Populations showed significant epigenetic differentiation between populations and countries in the field, but also when grown in a common garden. By comparing the epigenetic variation between field and common garden‐grown plants, we showed that a considerable part of the epigenetic memory differed from the field‐grown plants and was presumably environmentally induced. The memory component can consist of heritable variation in methylation that is not sensitive to environments and possibly genetically based, or environmentally induced variation that is heritable, or a combination of both. Additionally, random epimutations might be responsible for some differences as well. By comparing epigenetic variation in both the field and common environment, our study provides useful insight into the environmental and genetic components of epigenetic variation.     

Stress-induced variation in evolution: from behavioural plasticity to genetic assimilation

Extreme environments are closely associated with phenotypic evolution, yet the mechanisms behind this relationship are poorly understood. Several themes and approaches in recent studies significantly further our understanding of the importance that stress-induced variation plays in evolution. First, stressful environments modify (and often reduce) the integration of neuroendocrinological, morphological and behavioural regulatory systems. Second, such reduced integration and subsequent accommodation of stress-induced variation by developmental systems enables organismal 'memory' of a stressful event as well as phenotypic and genetic assimilation of the response to a stressor. Third, in complex functional systems, a stress-induced increase in phenotypic and genetic variance is often directional, channelled by existing ontogenetic pathways. This accounts for similarity among individuals in stress-induced changes and thus significantly facilitates the rate of adaptive evolution. Fourth, accumulation of phenotypically neutral genetic variation might be a common property of locally adapted and complex organismal systems, and extreme environments facilitate the phenotypic expression of this variance. Finally, stress-induced effects and stress-resistance strategies often persist for several generations through maternal, ecological and cultural inheritance. These transgenerational effects, along with both the complexity of developmental systems and stressor recurrence, might facilitate genetic assimilation of stress-induced effects. Accumulation of phenotypically neutral genetic variance by developmental systems and phenotypic accommodation of stress-induced effects, together with the inheritance of stress-induced modifications, ensure the evolutionary persistence of stress-response strategies and provide a link between individual adaptability and evolutionary adaptation.     

Social structure modulates the evolutionary consequences of social plasticity: A social network perspective on interacting phenotypes

Organisms express phenotypic plasticity during social interactions. Interacting phenotype theory has explored the consequences of social plasticity for evolution, but it is unclear how this theory applies to complex social structures. We adapt interacting phenotype models to general social structures to explore how the number of social connections between individuals and preference for phenotypically similar social partners affect phenotypic variation and evolution. We derive an analytical model that ignores phenotypic feedback and use simulations to test the predictions of this model. We find that adapting previous models to more general social structures does not alter their general conclusions but generates insights into the effect of social plasticity and social structure on the maintenance of phenotypic variation and evolution. Contribution of indirect genetic effects to phenotypic variance is highest when interactions occur at intermediate densities and decrease at higher densities, when individuals approach interacting with all group members, homogenizing the social environment across individuals. However, evolutionary response to selection tends to increase at greater network densities as the effects of an individual's genes are amplified through increasing effects on other group members. Preferential associations among similar individuals (homophily) increase both phenotypic variance within groups and evolutionary response to selection. Our results represent a first step in relating social network structure to the expression of social plasticity and evolutionary responses to selection.     

Genetic accommodation in the wild: evolution of gene expression plasticity during character displacement

Ecological character displacement is considered crucial in promoting diversification, yet relatively little is known of its underlying mechanisms. We examined whether evolutionary shifts in gene expression plasticity (‘genetic accommodation’) mediate character displacement in spadefoot toads. Where Spea bombifrons and S. multiplicata occur separately in allopatry (the ancestral condition), each produces alternative, diet‐induced, larval ecomorphs: omnivores, which eat detritus, and carnivores, which specialize on shrimp. By contrast, where these two species occur together in sympatry (the derived condition), selection to minimize competition for detritus has caused S. bombifrons to become nearly fixed for producing only carnivores, suggesting that character displacement might have arisen through an extreme form of genetic accommodation (‘genetic assimilation’) in which plasticity is lost. Here, we asked whether we could infer a signature of this process in regulatory changes of specific genes. In particular, we investigated whether genes that are normally expressed more highly in one morph (‘biased’ genes) have evolved reduced plasticity in expression levels among S. bombifrons from sympatry compared to S. bombifrons from allopatry. We reared individuals from sympatry vs. allopatry on detritus or shrimp and measured the reaction norms of nine biased genes. Although different genes displayed different patterns of gene regulatory evolution, the combined gene expression profiles revealed that sympatric individuals had indeed lost the diet‐induced gene expression plasticity present in allopatric individuals. Our data therefore provide one of the few examples from natural populations in which genetic accommodation/assimilation can be traced to regulatory changes of specific genes. Such genetic accommodation might mediate character displacement in many systems.     

Using time series analysis to characterize evolutionary and plastic responses to environmental change: a case study of a shift toward earlier migration date in sockeye salmon

Environmental change can shift the phenotype of an organism through either evolutionary or nongenetic processes. Despite abundant evidence of phenotypic change in response to recent climate change, we typically lack sufficient genetic data to identify the role of evolution. We present a method of using phenotypic data to characterize the hypothesized role of natural selection and environmentally driven phenotypic shifts (plasticity). We modeled historical selection and environmental predictors of interannual variation in mean population phenotype using a multivariate state-space model framework. Through model comparisons, we assessed the extent to which an estimated selection differential explained observed variation better than environmental factors alone. We applied the method to a 60-year trend toward earlier migration in Columbia River sockeye salmon Oncorhynchus nerka, producing estimates of annual selection differentials, average realized heritability, and relative cumulative effects of selection and plasticity. We found that an evolutionary response to thermal selection was capable of explaining up to two-thirds of the phenotypic trend. Adaptive plastic responses to June river flow explain most of the remainder. This method is applicable to other populations with time series data if selection differentials are available or can be reconstructed. This method thus augments our toolbox for predicting responses to environmental change.