Evolutionary stasis of a heritable morphological trait in a wild fish population despite apparent directional selection

Comparing observed versus theoretically expected evolutionary responses is important for our understanding of the evolutionary process, and for assessing how species may cope with anthropogenic change. Here, we document directional selection for larger female size in Atlantic salmon, using pedigree‐derived estimates of lifetime reproductive success as a fitness measure. We show the trait is heritable and, thus, capable of responding to selection. The Breeder's Equation, which predicts microevolution as the product of phenotypic selection and heritability, predicted evolution of larger size. This was at odds, however, with the observed lack of either phenotypic or genetic temporal trends in body size, a so‐called “paradox of stasis.” To investigate this paradox, we estimated the additive genetic covariance between trait and fitness, which provides a prediction of evolutionary change according to Robertson's secondary theorem of selection (STS) that is unbiased by missing variables. The STS prediction was consistent with the observed stasis. Decomposition of phenotypic selection gradients into genetic and environmental components revealed a potential upward bias, implying unmeasured factors that covary with trait and fitness. These results showcase the power of pedigreed, wild population studies—which have largely been limited to birds and mammals—to study evolutionary processes on contemporary timescales.     

EVOLUTION IN FLUCTUATING ENVIRONMENTS: DECOMPOSING SELECTION INTO ADDITIVE COMPONENTS OF THE ROBERTSON–PRICE EQUATION

We analyze the stochastic components of the Robertson–Price equation for the evolution of quantitative characters that enables decomposition of the selection differential into components due to demographic and environmental stochasticity. We show how these two types of stochasticity affect the evolution of multivariate quantitative characters by defining demographic and environmental variances as components of individual fitness. The exact covariance formula for selection is decomposed into three components, the deterministic mean value, as well as stochastic demographic and environmental components. We show that demographic and environmental stochasticity generate random genetic drift and fluctuating selection, respectively. This provides a common theoretical framework for linking ecological and evolutionary processes. Demographic stochasticity can cause random variation in selection differentials independent of fluctuating selection caused by environmental variation. We use this model of selection to illustrate that the effect on the expected selection differential of random variation in individual fitness is dependent on population size, and that the strength of fluctuating selection is affected by how environmental variation affects the covariance in Malthusian fitness between individuals with different phenotypes. Thus, our approach enables us to partition out the effects of fluctuating selection from the effects of selection due to random variation in individual fitness caused by demographic stochasticity.     

Spatial processes and evolutionary models: a critical review

Evolution is a fundamentally population level process in which variation, drift and selection produce both temporal and spatial patterns of change. Statistical model fitting is now commonly used to estimate which kind of evolutionary process best explains patterns of change through time using models like Brownian motion, stabilizing selection (Ornstein–Uhlenbeck) and directional selection on traits measured from stratigraphic sequences or on phylogenetic trees. But these models assume that the traits possessed by a species are homogeneous. Spatial processes such as dispersal, gene flow and geographical range changes can produce patterns of trait evolution that do not fit the expectations of standard models, even when evolution at the local‐population level is governed by drift or a typical OU model of selection. The basic properties of population level processes (variation, drift, selection and population size) are reviewed and the relationship between their spatial and temporal dynamics is discussed. Typical evolutionary models used in palaeontology incorporate the temporal component of these dynamics, but not the spatial. Range expansions and contractions introduce rate variability into drift processes, range expansion under a drift model can drive directional change in trait evolution, and spatial selection gradients can create spatial variation in traits that can produce long‐term directional trends and punctuation events depending on the balance between selection strength, gene flow, extirpation probability and model of speciation. Using computational modelling that spatial processes can create evolutionary outcomes that depart from basic population‐level notions from these standard macroevolutionary models.     

Environmental stress correlates with increases in both genetic and residual variances: A meta‐analysis of animal studies

Adaptive evolutionary responses are determined by the strength of selection and amount of genetic variation within traits, however, both are known to vary across environmental conditions. As selection is generally expected to be strongest under stressful conditions, understanding how the expression of genetic variation changes across stressful and benign environmental conditions is crucial for predicting the rate of adaptive change. Although theory generally predicts increased genetic variation under stress, previous syntheses of the field have found limited support for this notion. These studies have focused on heritability, which is dependent on other environmentally sensitive, but nongenetic, sources of variation. Here, we aim to complement these studies with a meta‐analysis in which we examine changes in coefficient of variation (CV) in maternal, genetic, and residual variances across stressful and benign conditions. Confirming previous analyses, we did not find any clear direction in how heritability changes across stressful and benign conditions. However, when analyzing CV, we found higher genetic and residual variance under highly stressful conditions in life‐history traits but not in morphological traits. Our findings are of broad significance to contemporary evolution suggesting that rapid evolutionary adaptive response may be mediated by increased evolutionary potential in stressed populations.     

A cascade of evolutionary change alters consumer-resource dynamics and ecosystem function

It is becoming increasingly clear that intraspecific evolutionary divergence influences the properties of populations, communities and ecosystems. The different ecological impacts of phenotypes and genotypes may alter selection on many species and promote a cascade of ecological and evolutionary change throughout the food web. Theory predicts that evolutionary interactions across trophic levels may contribute to hypothesized feedbacks between ecology and evolution. However, the importance of 'cascading evolutionary change' in a natural setting is unknown. In lakes in Connecticut, USA, variation in migratory behaviour and feeding morphology of a fish predator, the alewife (Alosa pseudoharengus), drives life-history evolution in a species of zooplankton prey (Daphnia ambigua). Here we evaluated the reciprocal impacts of Daphnia evolution on ecological processes in laboratory mesocosms. We show that life-history evolution in Daphnia facilitates divergence in rates of population growth, which in turn significantly alters consumer-resource dynamics and ecosystem function. These experimental results parallel trends observed in lakes. Such results argue that a cascade of evolutionary change, which has occurred over contemporary timescales, alters community and ecosystem processes.     

Life‐history evolution under fluctuating density‐dependent selection and the adaptive alignment of pace‐of‐life syndromes

We present a novel perspective on life‐history evolution that combines recent theoretical advances in fluctuating density‐dependent selection with the notion of pace‐of‐life syndromes (POLSs) in behavioural ecology. These ideas posit phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits as a continuum from the highly fecund, short‐lived, bold, aggressive and highly dispersive ‘fast’ types at one end of the POLS to the less fecund, long‐lived, cautious, shy, plastic and socially responsive ‘slow’ types at the other. We propose that such variation in life histories and the associated individual differences in behaviour can be explained through their eco‐evolutionary dynamics with population density – a single and ubiquitous selective factor that is present in all biological systems. Contrasting regimes of environmental stochasticity are expected to affect population density in time and space and create differing patterns of fluctuating density‐dependent selection, which generates variation in fast versus slow life histories within and among populations. We therefore predict that a major axis of phenotypic co‐variation in life‐history, physiological, morphological and behavioural traits (i.e. the POLS) should align with these stochastic fluctuations in the multivariate fitness landscape created by variation in density‐dependent selection. Phenotypic plasticity and/or genetic (co‐)variation oriented along this major POLS axis are thus expected to facilitate rapid and adaptively integrated changes in various aspects of life histories within and among populations and/or species. The fluctuating density‐dependent selection POLS framework presented here therefore provides a series of clear testable predictions, the investigation of which should further our fundamental understanding of life‐history evolution and thus our ability to predict natural population dynamics.     

Sperm size evolution in African greenbuls (Passeriformes: Pycnonotidae)

Sperm morphology is highly diversified across the animal kingdom and recent comparative evidence from passerine birds suggests that postcopulatory sexual selection is a significant driver of sperm evolution. In the present study, we describe sperm size variation among 20 species of African greenbuls and one bulbul (Passeriformes: Pycnonotidae) and analyze the evolutionary differentiation of sperm size within a phylogenetic framework. We found significant interspecific variation in sperm size; with some genera exhibiting relatively long sperm (e.g. Eurillas) and others exhibiting short sperm head lengths (e.g. Phyllastrephus). However, our results suggest that contemporary levels of sperm competition are unlikely to explain sperm diversification within this clade: the coefficients of inter‐male variation (CV_bm) in sperm length were generally high, suggesting relatively low and homogeneous rates of extra‐pair paternity. Finally, in a comparison of six evolutionary or tree transformation models, we found support for both the Kappa (evolutionary change primarily at nodes) and Lambda (lineage‐specific evolutionary rates along branches) models in the evolutionary trajectories of sperm size among species. We therefore conclude that African greenbuls have more variable rates of sperm size evolution than expected from a neutral model of genetic drift. Understanding the evolutionary dynamics of sperm diversification remains a future challenge.     

Negative frequency‐dependent selection maintains coexisting genotypes during fluctuating selection

Natural environments are rarely static; rather selection can fluctuate on timescales ranging from hours to centuries. However, it is unclear how adaptation to fluctuating environments differs from adaptation to constant environments at the genetic level. For bacteria, one key axis of environmental variation is selection for planktonic or biofilm modes of growth. We conducted an evolution experiment with Burkholderia cenocepacia, comparing the evolutionary dynamics of populations evolving under constant selection for either biofilm formation or planktonic growth with populations in which selection fluctuated between the two environments on a weekly basis. Populations evolved in the fluctuating environment shared many of the same genetic targets of selection as those evolved in constant biofilm selection, but were genetically distinct from the constant planktonic populations. In the fluctuating environment, mutations in the biofilm‐regulating genes wspA and rpfR rose to high frequency in all replicate populations. A mutation in wspA first rose rapidly and nearly fixed during the initial biofilm phase but was subsequently displaced by a collection of rpfR mutants upon the shift to the planktonic phase. The wspA and rpfR genotypes coexisted via negative frequency‐dependent selection around an equilibrium frequency that shifted between the environments. The maintenance of coexisting genotypes in the fluctuating environment was unexpected. Under temporally fluctuating environments, coexistence of two genotypes is only predicted under a narrow range of conditions, but the frequency‐dependent interactions we observed provide a mechanism that can increase the likelihood of coexistence in fluctuating environments.     

Eco‐evolution on the edge during climate change

We urgently need to predict species responses to climate change to minimize future biodiversity loss and ensure we do not waste limited resources on ineffective conservation strategies. Currently, most predictions of species responses to climate change ignore the potential for evolution. However, evolution can alter species ecological responses, and different aspects of evolution and ecology can interact to produce complex eco‐evolutionary dynamics under climate change. Here we review how evolution could alter ecological responses to climate change on species warm and cool range margins, where evolution could be especially important. We discuss different aspects of evolution in isolation, and then synthesize results to consider how multiple evolutionary processes might interact and affect conservation strategies. On species cool range margins, the evolution of dispersal could increase range expansion rates and allow species to adapt to novel conditions in their new range. However, low genetic variation and genetic drift in small range‐front populations could also slow or halt range expansions. Together, these eco‐evolutionary effects could cause a three‐step, stop‐and‐go expansion pattern for many species. On warm range margins, isolation among populations could maintain high genetic variation that facilitates evolution to novel climates and allows species to persist longer than expected without evolution. This ‘evolutionary extinction debt’ could then prevent other species from shifting their ranges. However, as climate change increases isolation among populations, increasing dispersal mortality could select for decreased dispersal and cause rapid range contractions. Some of these eco‐evolutionary dynamics could explain why many species are not responding to climate change as predicted. We conclude by suggesting that resurveying historical studies that measured trait frequencies, the strength of selection, or heritabilities could be an efficient way to increase our eco‐evolutionary knowledge in climate change biology.     

Strong artificial selection in the wild results in predicted small evolutionary change

Estimates of genetic variation and selection allow for quantitative predictions of evolutionary change, at least in controlled laboratory experiments. Natural populations are, however, different in many ways, and natural selection on heritable traits does not always result in phenotypic change. To test whether we were able to predict the evolutionary dynamics of a complex trait measured in a natural, heterogeneous environment, we performed, over an 8-year period, a two-way selection experiment on clutch size in a subdivided island population of great tits (Parus major). Despite strong artificial selection, there was no clear evidence for evolutionary change at the phenotypic level. Environmentally induced differences in clutch size among years are, however, large and can mask evolutionary changes. Indeed, genetic changes in clutch size, inferred from a statistical model, did not deviate systematically from those predicted. Although this shows that estimates of genetic variation and selection can indeed provide quantitative predictions of evolutionary change, also in the wild, it also emphasizes that demonstrating evolution in wild populations is difficult, and that the interpretation of phenotypic trends requires great care.     

Sex ratio dynamics and fluctuating selection on personality

Fluctuating selection has often been proposed as an explanation for the maintenance of genetic variation in personality. Here I argue that the temporal dynamics of the sex ratio can be a powerful source of fluctuating selection on personality traits, and develop this hypothesis with respect to humans. First, I review evidence that sex ratios modulate a wide range of social processes related to mating and parenting. Since most personality traits affect mating and parenting behavior, changes in the sex ratio can be expected to result in variable selection on personality. I then show that the temporal dynamics of the sex ratio are intrinsically characterized by fluctuations at various timescales. Finally, I address a number of evolutionary genetic challenges to the hypothesis. I conclude that the sex ratio hypothesis is a plausible explanation of genetic variation in human personality, and may be fruitfully applied to other species as well.     

Evolutionary dynamics of a sexual ornament in the house sparrow (Passer domesticus): the role of indirect selection within and between sexes

The relative contribution of sexual and natural selection to evolution of sexual ornaments has rarely been quantified under natural conditions. In this study we used a long-term dataset of house sparrows in which parents and offspring were matched genetically to estimate the within- and across-sex genetic basis for variation and covariation among morphological traits. By applying two-sex multivariate "animal models" to estimate genetic parameters, we estimated evolutionary changes in a male sexual ornament, badge size, from the contribution of direct and indirect selection on correlated traits within males and females, after accounting for overlapping generations and age-structure. Indirect natural selection on genetically correlated traits in males and females was the major force causing evolutionary change in the male ornament. Thus, natural selection on female morphology may cause indirect evolutionary changes in male ornaments. We observed however no directional phenotypic change in the ornament size of one-year-old males during the study period. On the other hand, changes were recorded in other morphological characters of both sexes. Our analyses of evolutionary dynamics in sexual characters require application of appropriate two-sex models to account for how selection on correlated traits in both sexes affects the evolutionary outcome of sexual selection.     

Plant domestication slows pest evolution

Agricultural practices such as breeding resistant varieties and pesticide use can cause rapid evolution of pest species, but it remains unknown how plant domestication itself impacts pest contemporary evolution. Using experimental evolution on a comparative phylogenetic scale, we compared the evolutionary dynamics of a globally important economic pest – the green peach aphid (Myzus persicae) – growing on 34 plant taxa, represented by 17 crop species and their wild relatives. Domestication slowed aphid evolution by 13.5%, maintained 10.4% greater aphid genotypic diversity and 5.6% higher genotypic richness. The direction of evolution (i.e. which genotypes increased in frequency) differed among independent domestication events but was correlated with specific plant traits. Individual‐based simulation models suggested that domestication affects aphid evolution directly by reducing the strength of selection and indirectly by increasing aphid density and thus weakening genetic drift. Our results suggest that phenotypic changes during domestication can alter pest evolutionary dynamics.     

Eco‐evolutionary dynamics in restored communities and ecosystems

Recent ecological studies have revealed that rapid evolution within populations can have significant impacts on the ecological dynamics of communities and ecosystems. These eco‐evolutionary dynamics (EED) are likely to have substantial and quantifiable effects in restored habitats over timescales that are relevant for the conservation and restoration of small populations and threatened communities. Restored habitats may serve as “hotspots” for EED due to mismatches between transplanted genotypes and the restored environment, and novel interactions among lineages that do not share a coevolutionary history, both of which can generate strong selection for rapid evolutionary change that has immediate demographic consequences. Rapid evolution that influences population dynamics and community processes is likely to have particularly large effects during the establishment phase of restoration efforts. Finally, restoration activities and their associated long‐term monitoring programs provide outstanding opportunities for using eco‐evolutionary experimental approaches. Results from such studies will address questions about the effects of rapid evolutionary change on the ecological dynamics of populations and interacting species, while simultaneously providing critical, but currently overlooked, information for conservation practices.     

Socially flexible female choice differs among populations of the Pacific field cricket: geographical variation in the interaction coefficient psi (Ψ)

Indirect genetic effects (IGEs) occur when genes expressed in one individual affect the phenotype of a conspecific. Theoretical models indicate that the evolutionary consequences of IGEs critically depend on the genetic architecture of interacting traits, and on the strength and direction of phenotypic effects arising from social interactions, which can be quantified by the interaction coefficient Ψ. In the context of sexually selected traits, strong positive Ψ tends to exaggerate evolutionary change, whereas negative Ψ impedes sexual trait elaboration. Despite its theoretical importance, whether and how Ψ varies among geographically distinct populations is unknown. Such information is necessary to evaluate the potential for IGEs to contribute to divergence among isolated or semi-isolated populations. Here, we report substantial variation in Ψ for a behavioural trait involved in sexual selection in the field cricket Teleogryllus oceanicus: female choosiness. Both the strength and direction of Ψ varied among geographically isolated populations. Ψ also changed over time. In a contemporary population of crickets from Kauai, experience of male song increased female choosiness. In contrast, experience of male song decreased choosiness in an ancestral population from the same location. This rapid change corroborates studies examining the evolvability of Ψ and demonstrates how interpopulation variation in the interaction coefficient might influence sexual selection and accelerate divergence of traits influenced by IGEs that contribute to reproductive isolation in nascent species or subspecies.     

Population divergence along lines of genetic variance and covariance in the invasive plant Lythrum salicaria in eastern North America

Evolution during biological invasion may occur over contemporary timescales, but the rate of evolutionary change may be inhibited by a lack of standing genetic variation for ecologically relevant traits and by fitness trade-offs among them. The extent to which these genetic constraints limit the evolution of local adaptation during biological invasion has rarely been examined. To investigate genetic constraints on life-history traits, we measured standing genetic variance and covariance in 20 populations of the invasive plant purple loosestrife (Lythrum salicaria) sampled along a latitudinal climatic gradient in eastern North America and grown under uniform conditions in a glasshouse. Genetic variances within and among populations were significant for all traits; however, strong intercorrelations among measurements of seedling growth rate, time to reproductive maturity and adult size suggested that fitness trade-offs have constrained population divergence. Evidence to support this hypothesis was obtained from the genetic variance-covariance matrix (G) and the matrix of (co)variance among population means (D), which were 79.8% (95% C.I. 77.7-82.9%) similar. These results suggest that population divergence during invasive spread of L. salicaria in eastern North America has been constrained by strong genetic correlations among life-history traits, despite large amounts of standing genetic variation for individual traits.     

The probability of parallel genetic evolution from standing genetic variation

Parallel evolution is often assumed to result from repeated adaptation to novel, yet ecologically similar, environments. Here, we develop and analyse a mathematical model that predicts the probability of parallel genetic evolution from standing genetic variation as a function of the strength of phenotypic selection and constraints imposed by genetic architecture. Our results show that the probability of parallel genetic evolution increases with the strength of natural selection and effective population size and is particularly likely to occur for genes with large phenotypic effects. Building on these results, we develop a Bayesian framework for estimating the strength of parallel phenotypic selection from genetic data. Using extensive individual‐based simulations, we show that our estimator is robust across a wide range of genetic and evolutionary scenarios and provides a useful tool for rigorously testing the hypothesis that parallel genetic evolution is the result of adaptive evolution. An important result that emerges from our analyses is that existing studies of parallel genetic evolution frequently rely on data that is insufficient for distinguishing between adaptive evolution and neutral evolution driven by random genetic drift. Overcoming this challenge will require sampling more populations and the inclusion of larger numbers of loci.     

Evolutionary history shapes the association between developmental instability and population‐level genetic variation in three‐spined sticklebacks

Developmental instability (DI) is the sensitivity of a developing trait to random noise and can be measured by degrees of directionally random asymmetry [fluctuating asymmetry (FA)]. FA has been shown to increase with loss of genetic variation and inbreeding as measures of genetic stress, but associations vary among studies. Directional selection and evolutionary change of traits have been hypothesized to increase the average levels of FA of these traits and to increase the association strength between FA and population‐level genetic variation. We test these two hypotheses in three‐spined stickleback (Gasterosteus aculeatus L.) populations that recently colonized the freshwater habitat. Some traits, like lateral bone plates, length of the pelvic spine, frontal gill rakers and eye size, evolved in response to selection regimes during colonization. Other traits, like distal gill rakers and number of pelvic fin rays, did not show such phenotypic shifts. Contrary to a priori predictions, average FA did not systematically increase in traits that were under presumed directional selection, and the increases observed in a few traits were likely to be attributable to other factors. However, traits under directional selection did show a weak but significantly stronger negative association between FA and selectively neutral genetic variation at the population level compared with the traits that did not show an evolutionary change during colonization. These results support our second prediction, providing evidence that selection history can shape associations between DI and population‐level genetic variation at neutral markers, which potentially reflect genetic stress. We argue that this might explain at least some of the observed heterogeneities in the patterns of asymmetry.     

The genomic basis of eco‐evolutionary dynamics

Recent recognition that ecological and evolutionary processes can operate on similar timescales has led to a rapid increase in theoretical and empirical studies on eco‐evolutionary dynamics. Progress in the fields of evolutionary biology, genomics and ecology is greatly enhancing our understanding of rapid adaptive processes, the predictability of adaptation and the genetics of ecologically important traits. However, progress in these fields has proceeded largely independently of one another. In an attempt to better integrate these fields, the centre for ‘Adaptation to a Changing Environment’ organized a conference entitled ‘The genomic basis of eco‐evolutionary change’ and brought together experts in ecological genomics and eco‐evolutionary dynamics. In this review, we use the work of the invited speakers to summarize eco‐evolutionary dynamics and discuss how they are relevant for understanding and predicting responses to contemporary environmental change. Then, we show how recent advances in genomics are contributing to our understanding of eco‐evolutionary dynamics. Finally, we highlight the gaps in our understanding of eco‐evolutionary dynamics and recommend future avenues of research in eco‐evolutionary dynamics.     

Evolutionary potential of morphological traits across different life‐history stages

Despite accumulating examples of selection acting on heritable traits in the wild, predicted evolutionary responses are often different from observed phenotypic trends. Various explanations have been suggested for these mismatches. These include within‐individual changes across lifespan that can create important variation in genetic architecture of traits and selection acting on them, but also potential problems with the methodological approach used to predict evolutionary responses of traits. Here, we used an 8‐year data set on tree swallow (Tachycineta bicolor) to first assess the effects of differences among three nestling life‐history stages on the genetic (co)variances of two morphological traits (body mass and primary feather length) and the selection acting on them over three generations. We then estimated the evolutionary potential of these traits by predicting their evolutionary responses using the breeder's equation and the secondary theorem of selection approaches. Our results showed variation in strength and direction of selection and slight changes in trait variance across ages. Predicted evolutionary responses differed importantly between both approaches for half of the trait–age combinations we studied, suggesting the presence of environmentally induced correlations between focal traits and fitness possibly biasing breeder's equation predictions. Our results emphasize that predictions of evolutionary potential for morphological traits are likely to be highly variable, both in strength and direction, depending on the life stage and method used, thus mitigating our capacity to predict adaptation and persistence of wild populations.