Gillespie eco‐evolutionary models (GEMs) reveal the role of heritable trait variation in eco‐evolutionary dynamics

Heritable trait variation is a central and necessary ingredient of evolution. Trait variation also directly affects ecological processes, generating a clear link between evolutionary and ecological dynamics. Despite the changes in variation that occur through selection, drift, mutation, and recombination, current eco‐evolutionary models usually fail to track how variation changes through time. Moreover, eco‐evolutionary models assume fitness functions for each trait and each ecological context, which often do not have empirical validation. We introduce a new type of model, Gillespie eco‐evolutionary models (GEMs), that resolves these concerns by tracking distributions of traits through time as eco‐evolutionary dynamics progress. This is done by allowing change to be driven by the direct fitness consequences of model parameters within the context of the underlying ecological model, without having to assume a particular fitness function. GEMs work by adding a trait distribution component to the standard Gillespie algorithm – an approach that models stochastic systems in nature that are typically approximated through ordinary differential equations. We illustrate GEMs with the Rosenzweig–MacArthur consumer–resource model. We show not only how heritable trait variation fuels trait evolution and influences eco‐evolutionary dynamics, but also how the erosion of variation through time may hinder eco‐evolutionary dynamics in the long run. GEMs can be developed for any parameter in any ordinary differential equation model and, furthermore, can enable modeling of multiple interacting traits at the same time. We expect GEMs will open the door to a new direction in eco‐evolutionary and evolutionary modeling by removing long‐standing modeling barriers, simplifying the link between traits, fitness, and dynamics, and expanding eco‐evolutionary treatment of a greater diversity of ecological interactions. These factors make GEMs much more than a modeling advance, but an important conceptual advance that bridges ecology and evolution through the central concept of heritable trait variation.     

Toward an integration of evolutionary biology and ecosystem science

At present, the disciplines of evolutionary biology and ecosystem science are weakly integrated. As a result, we have a poor understanding of how the ecological and evolutionary processes that create, maintain, and change biological diversity affect the flux of energy and materials in global biogeochemical cycles. The goal of this article was to review several research fields at the interfaces between ecosystem science, community ecology and evolutionary biology, and suggest new ways to integrate evolutionary biology and ecosystem science. In particular, we focus on how phenotypic evolution by natural selection can influence ecosystem functions by affecting processes at the environmental, population and community scale of ecosystem organization. We develop an eco-evolutionary model to illustrate linkages between evolutionary change (e.g. phenotypic evolution of producer), ecological interactions (e.g. consumer grazing) and ecosystem processes (e.g. nutrient cycling). We conclude by proposing experiments to test the ecosystem consequences of evolutionary changes.     

An emerging synthesis between community ecology and evolutionary biology

A synthesis between community ecology and evolutionary biology is emerging that identifies how genetic variation and evolution within one species can shape the ecological properties of entire communities and, in turn, how community context can govern evolutionary processes and patterns. This synthesis incorporates research on the ecology and evolution within communities over short timescales (community genetics and diffuse coevolution), as well as macroevolutionary timescales (community phylogenetics and co-diversification of communities). As we discuss here, preliminary evidence supports the hypothesis that there is a dynamic interplay between ecology and evolution within communities, yet researchers have not yet demonstrated convincingly whether, and under what circumstances, it is important for biologists to bridge community ecology and evolutionary biology. Answering this question will have important implications for both basic and applied problems in biology.     

Integrating animal temperament within ecology and evolution

Temperament describes the idea that individual behavioural differences are repeatable over time and across situations. This common phenomenon covers numerous traits, such as aggressiveness, avoidance of novelty, willingness to take risks, exploration, and sociality. The study of temperament is central to animal psychology, behavioural genetics, pharmacology, and animal husbandry, but relatively few studies have examined the ecology and evolution of temperament traits. This situation is surprising, given that temperament is likely to exert an important influence on many aspects of animal ecology and evolution, and that individual variation in temperament appears to be pervasive amongst animal species. Possible explanations for this neglect of temperament include a perceived irrelevance, an insufficient understanding of the link between temperament traits and fitness, and a lack of coherence in terminology with similar traits often given different names, or different traits given the same name. We propose that temperament can and should be studied within an evolutionary ecology framework and provide a terminology that could be used as a working tool for ecological studies of temperament. Our terminology includes five major temperament trait categories: shyness-boldness, exploration-avoidance, activity, sociability and aggressiveness. This terminology does not make inferences regarding underlying dispositions or psychological processes, which may have restrained ecologists and evolutionary biologists from working on these traits. We present extensive literature reviews that demonstrate that temperament traits are heritable, and linked to fitness and to several other traits of importance to ecology and evolution. Furthermore, we describe ecologically relevant measurement methods and point to several ecological and evolutionary topics that would benefit from considering temperament, such as phenotypic plasticity, conservation biology, population sampling, and invasion biology.     

Eco‐evolutionary partitioning metrics: assessing the importance of ecological and evolutionary contributions to population and community change

Interest in eco‐evolutionary dynamics is rapidly increasing thanks to ground‐breaking research indicating that evolution can occur rapidly and can alter the outcome of ecological processes. A key challenge in this sub‐discipline is establishing how important the contribution of evolutionary and ecological processes and their interactions are to observed shifts in population and community characteristics. Although a variety of metrics to separate and quantify the effects of evolutionary and ecological contributions to observed trait changes have been used, they often allocate fractions of observed changes to ecology and evolution in different ways. We used a mathematical and numerical comparison of two commonly used frameworks – the Price equation and reaction norms – to reveal that the Price equation cannot partition genetic from non‐genetic trait change within lineages, whereas the reaction norm approach cannot partition among‐ from within‐lineage trait change. We developed a new metric that combines the strengths of both Price‐based and reaction norm metrics, extended all metrics to analyse community change and also incorporated extinction and colonisation of species in these metrics. Depending on whether our new metric is applied to populations or communities, it can correctly separate intraspecific, interspecific, evolutionary, non‐evolutionary and interacting eco‐evolutionary contributions to trait change.     

Eco-evolutionary maintenance of diversity in fluctuating environments

Growing evidence suggests that temporally fluctuating environments are important in maintaining variation both within and between species. To date, however, studies of genetic variation within a population have been largely conducted by evolutionary biologists (particularly population geneticists), while population and community ecologists have concentrated more on diversity at the species level. Despite considerable conceptual overlap, the commonalities and differences of these two alternative paradigms have yet to come under close scrutiny. Here, we review theoretical and empirical studies in population genetics and community ecology focusing on the ‘temporal storage effect’ and synthesise theories of diversity maintenance across different levels of biological organisation. Drawing on Chesson's coexistence theory, we explain how temporally fluctuating environments promote the maintenance of genetic variation and species diversity. We propose a further synthesis of the two disciplines by comparing models employing traditional frequency-dependent dynamics and those adopting density-dependent dynamics. We then address how temporal fluctuations promote genetic and species diversity simultaneously via rapid evolution and eco-evolutionary dynamics. Comparing and synthesising ecological and evolutionary approaches will accelerate our understanding of diversity maintenance in nature.     

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.     

Eco-evolutionary feedbacks in community and ecosystem ecology: interactions between the ecological theatre and the evolutionary play

Interactions between natural selection and environmental change are well recognized and sit at the core of ecology and evolutionary biology. Reciprocal interactions between ecology and evolution, eco-evolutionary feedbacks, are less well studied, even though they may be critical for understanding the evolution of biological diversity, the structure of communities and the function of ecosystems. Eco-evolutionary feedbacks require that populations alter their environment (niche construction) and that those changes in the environment feed back to influence the subsequent evolution of the population. There is strong evidence that organisms influence their environment through predation, nutrient excretion and habitat modification, and that populations evolve in response to changes in their environment at time-scales congruent with ecological change (contemporary evolution). Here, we outline how the niche construction and contemporary evolution interact to alter the direction of evolution and the structure and function of communities and ecosystems. We then present five empirical systems that highlight important characteristics of eco-evolutionary feedbacks: rotifer–algae chemostats; alewife–zooplankton interactions in lakes; guppy life-history evolution and nutrient cycling in streams; avian seed predators and plants; and tree leaf chemistry and soil processes. The alewife–zooplankton system provides the most complete evidence for eco-evolutionary feedbacks, but other systems highlight the potential for eco-evolutionary feedbacks in a wide variety of natural systems.     

How fast is fast? Eco‐evolutionary dynamics and rates of change in populations and phenotypes

It is increasingly recognized that evolution may occur in ecological time. It is not clear, however, how fast evolution – or phenotypic change more generally – may be in comparison with the associated ecology, or whether systems with fast ecological dynamics generally have relatively fast rates of phenotypic change. We developed a new dataset on standardized rates of change in population size and phenotypic traits for a wide range of species and taxonomic groups. We show that rates of change in phenotypes are generally no more than 2/3, and on average about 1/4, the concurrent rates of change in population size. There was no relationship between rates of population change and rates of phenotypic change across systems. We also found that the variance of both phenotypic and ecological rates increased with the mean across studies following a power law with an exponent of two, while temporal variation in phenotypic rates was lower than in ecological rates. Our results are consistent with the view that ecology and evolution may occur at similar time scales, but clarify that only rarely do populations change as fast in traits as they do in abundance.     

Adaptive evolution of butterfly wing shape: from morphology to behaviour

Butterflies display extreme variation in wing shape associated with tremendous ecological diversity. Disentangling the role of neutral versus adaptive processes in wing shape diversification remains a challenge for evolutionary biologists. Ascertaining how natural selection influences wing shape evolution requires both functional studies linking morphology to flight performance, and ecological investigations linking performance in the wild with fitness. However, direct links between morphological variation and fitness have rarely been established. The functional morphology of butterfly flight has been investigated but selective forces acting on flight behaviour and associated wing shape have received less attention. Here, we attempt to estimate the ecological relevance of morpho‐functional links established through biomechanical studies in order to understand the evolution of butterfly wing morphology. We survey the evidence for natural and sexual selection driving wing shape evolution in butterflies, and discuss how our functional knowledge may allow identification of the selective forces involved, at both the macro‐ and micro‐evolutionary scales. Our review shows that although correlations between wing shape variation and ecological factors have been established at the macro‐evolutionary level, the underlying selective pressures often remain unclear. We identify the need to investigate flight behaviour in relevant ecological contexts to detect variation in fitness‐related traits. Identifying the selective regime then should guide experimental studies towards the relevant estimates of flight performance. Habitat, predators and sex‐specific behaviours are likely to be major selective forces acting on wing shape evolution in butterflies. Some striking cases of morphological divergence driven by contrasting ecology involve both wing and body morphology, indicating that their interactions should be included in future studies investigating co‐evolution between morphology and flight behaviour.     

Ecophylogenetics: advances and perspectives

Ecophylogenetics can be viewed as an emerging fusion of ecology, biogeography and macroevolution. This new and fast-growing field is promoting the incorporation of evolution and historical contingencies into the ecological research agenda through the widespread use of phylogenetic data. Including phylogeny into ecological thinking represents an opportunity for biologists from different fields to collaborate and has provided promising avenues of research in both theoretical and empirical ecology, towards a better understanding of the assembly of communities, the functioning of ecosystems and their responses to environmental changes. The time is ripe to assess critically the extent to which the integration of phylogeny into these different fields of ecology has delivered on its promise. Here we review how phylogenetic information has been used to identify better the key components of species interactions with their biotic and abiotic environments, to determine the relationships between diversity and ecosystem functioning and ultimately to establish good management practices to protect overall biodiversity in the face of global change. We evaluate the relevance of information provided by phylogenies to ecologists, highlighting current potential weaknesses and needs for future developments. We suggest that despite the strong progress that has been made, a consistent unified framework is still missing to link local ecological dynamics to macroevolution. This is a necessary step in order to interpret observed phylogenetic patterns in a wider ecological context. Beyond the fundamental question of how evolutionary history contributes to shape communities, ecophylogenetics will help ecology to become a better integrative and predictive science.     

Evolutionary rescue beyond the models

Laboratory model systems and mathematical models have shed considerable light on the fundamental properties and processes of evolutionary rescue. But it remains to determine the extent to which these model-based findings can help biologists predict when evolution will fail or succeed in rescuing natural populations that are facing novel conditions that threaten their persistence. In this article, we present a prospectus for transferring our basic understanding of evolutionary rescue to wild and other non-laboratory populations. Current experimental and theoretical results emphasize how the interplay between inheritance processes and absolute fitness in changed environments drive population dynamics and determine prospects of extinction. We discuss the challenge of inferring these elements of the evolutionary rescue process in field and natural settings. Addressing this challenge will contribute to a more comprehensive understanding of population persistence that combines processes of evolutionary rescue with developmental and ecological mechanisms.     

Self-structuring in spatial evolutionary ecology

Spatial self-structuring has been a focus of recent interest among evolutionary ecologists. We review recent developments in the study of the interplay between spatial self-structuring and evolution. We first discuss the relative merits of the various theoretical approaches to spatial modelling in ecology. Second, we synthesize the main theoretical studies of the evolution of cooperation in spatially structured populations. We show that population viscosity is generally beneficial to cooperation, because cooperators can reap additional benefits from being clustered. A similar mechanism can explain the evolution of honest communication and of reduced virulence in host–parasite interactions. We also discuss some recent innovative empirical results that test these theories. Third, we show the relevance of these results to the general field of evolutionary ecology. An important conclusion is that kin selection is the main process that drives evolution of cooperation in viscous populations. Many results of kin selection theory can be recovered as emergent properties of spatial ecological dynamics. We discuss the implications of these results for the study of multilevel selection and evolutionary transitions. We conclude by sketching some perspectives for future research, with a particular emphasis on the topics of evolutionary branching, criticality, spatial fluctuations and experimental tests of theoretical predictions.     

花寿命的进化生态学意义

花寿命 (Floral longevity) 是指一朵花保持开放并具有功能的持续时间, 它作为一种重要的繁殖策略影响着植物的繁殖, 在植物繁殖策略的进化生态学研究中具有非常重要的意义。近年来, 进化生态学家开始重视花寿命的研究, 在传粉与非传粉因素对花寿命的影响、花展示和繁殖成功与花寿命的关系等方面取得了长足的进展。生活史进化模型表明, 最优花寿命取决于开花成本和两性适合度实现速率之间的权衡。大量的实验研究支持此模型。实验研究表明:授粉可导致某些植物的花寿命显著缩短, 但是, 花粉移除对花寿命一般没有显著影响;部分植物的花具有最短花寿命, 这可能是一种保证植物雄性适合度的机制;温度和水分等非传粉因素的变化, 因改变开花成本而影响到花寿命;在花的群体水平上, 植物根据传粉状况和资源状况, 会调节花序上不同花的开放时间, 进而改变花展示的结构和功能;长的花寿命是保障植物繁殖成功的重要机制之一, 但可能要付出一定的适合度代价。该文概述了花寿命进化生态学的理论和实验研究进展, 最后指出:在理论研究上, 雌雄利益冲突为理解花寿命的进化提供了新的视角。在实验研究中, 需要重视植物通过优化花寿命而增强雄性适合度的研究思路。对花寿命的成本-收益分析, 需要考虑单花与花展示的功能关系。     

What processes must we understand to forecast regional-scale population dynamics?

An urgent challenge facing biologists is predicting the regional-scale population dynamics of species facing environmental change. Biologists suggest that we must move beyond predictions based on phenomenological models and instead base predictions on underlying processes. For example, population biologists, evolutionary biologists, community ecologists and ecophysiologists all argue that the respective processes they study are essential. Must our models include processes from all of these fields? We argue that answering this critical question is ultimately an empirical exercise requiring a substantial amount of data that have not been integrated for any system to date. To motivate and facilitate the necessary data collection and integration, we first review the potential importance of each mechanism for skilful prediction. We then develop a conceptual framework based on reaction norms, and propose a hierarchical Bayesian statistical framework to integrate processes affecting reaction norms at different scales. The ambitious research programme we advocate is rapidly becoming feasible due to novel collaborations, datasets and analytical tools.     

Application of ecological and evolutionary theory to microbiome community dynamics across systems

A fundamental aim of microbiome research is to understand the factors that influence the assembly and stability of host-associated microbiomes, and their impact on host phenotype, ecology and evolution. However, ecological and evolutionary theories applied to predict microbiome community dynamics are largely based on macroorganisms and lack microbiome-centric hypotheses that account for unique features of the microbiome. This special feature sets out to drive advancements in the application of eco-evolutionary theory to microbiome community dynamics through the development of microbiome-specific theoretical and conceptual frameworks across plant, human and non-human animal systems. The feature comprises 11 research and review articles that address: (i) the effects of the microbiome on host phenotype, ecology and evolution; (ii) the application and development of ecological and evolutionary theories to investigate microbiome assembly, diversity and stability across broad taxonomic scales; and (iii) general principles that underlie microbiome diversity and dynamics. This cross-disciplinary synthesis of theoretical, conceptual, methodological and analytical approaches to characterizing host–microbiome ecology and evolution across systems addresses key research gaps in the field of microbiome research and highlights future research priorities.     

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.     

Personality-dependent dispersal: characterization, ontogeny and consequences for spatially structured populations

Dispersal is one of the most fundamental components of ecology, and affects processes as diverse as population growth, metapopulation dynamics, gene flow and adaptation. Although the act of moving from one habitat to another entails major costs to the disperser, empirical and theoretical studies suggest that these costs can be reduced by having morphological, physiological or behavioural specializations for dispersal. A few recent studies on different systems showed that individuals exhibit personality-dependent dispersal, meaning that dispersal tendency is associated with boldness, sociability or aggressiveness. Indeed, in several species, dispersers not only develop behavioural differences at the onset of dispersal, but display these behavioural characteristics through their life cycle. While personality-dependent dispersal has been demonstrated in only a few species, we believe that it is a widespread phenomenon with important ecological consequences. Here, we review the evidence for behavioural differences between dispersers and residents, to what extent they constitute personalities. We also examine how a link between personality traits and dispersal behaviours can be produced and how personality-dependent dispersal affects the dynamics of metapopulations and biological invasions. Finally, we suggest future research directions for population biologists, behavioural ecologists and conservation biologists such as how the direction and the strength of the relationship between personality traits and dispersal vary with ecological contexts.     

Integrating across life-history stages: consequences of natal habitat effects on dispersal

Ecological and evolutionary processes are affected by forces acting at both local and regional scales, yet our understanding of how these scales interact has remained limited. These processes are fundamentally linked through individuals that develop as juveniles in one environment and then either remain in the natal habitat or disperse to new environments. Empirical studies in a diverse range of organisms have demonstrated that the conditions experienced in the natal habitat can have profound effects on the adult phenotype. This environmentally induced phenotypic variation can in turn affect the probability that an individual will disperse to a new environment and the ecological and evolutionary impact of that individual in the new environment. We synthesize the literature on this process and propose a framework for exploring the linkage between local developmental environment and dispersal. We then discuss the ecological and evolutionary implications of dispersal asymmetries generated by the effects of natal habitat conditions on individual phenotypes. Our review indicates that the influence of natal habitat conditions on adult phenotypes may be a highly general mechanism affecting the flow of individuals between populations. The wealth of information already gathered on how local conditions affect adult phenotype can and should be integrated into the study of dispersal as a critical force in ecology and evolution.     

Ecological and Evolutionary Effects of Stickleback on Community Structure

Species’ ecology and evolution can have strong effects on communities. Both may change concurrently when species colonize a new ecosystem. We know little, however, about the combined effects of ecological and evolutionary change on community structure. We simultaneously examined the effects of top-predator ecology and evolution on freshwater community parameters using recently evolved generalist and specialist ecotypes of three-spine stickleback (Gasterosteus aculeatus). We used a mesocosm experiment to directly examine the effects of ecological (fish presence and density) and evolutionary (phenotypic diversity and specialization) factors on community structure at lower trophic levels. We evaluated zooplankton biomass and composition, periphyton and phytoplankton chlorophyll-a concentration, and net primary production among treatments containing different densities and diversities of stickleback. Our results showed that both ecological and evolutionary differences in the top-predator affect different aspects of community structure and composition. Community structure, specifically the abundance of organisms at each trophic level, was affected by stickleback presence and density, whereas composition of zooplankton was influenced by stickleback diversity and specialization. Primary productivity, in terms of chlorophyll-a concentration and net primary production was affected by ecological but not evolutionary factors. Our results stress the importance of concurrently evaluating both changes in density and phenotypic diversity on the structure and composition of communities.