Measuring the contribution of evolution to community trait structure in freshwater zooplankton

There are currently few predictions about when evolutionary processes are likely to play an important role in structuring community features. Determining predictors that indicate when evolution is expected to impact ecological processes in natural landscapes can help researchers identify eco-evolutionary ‘hotspots', where eco-evolutionary interactions are more likely to occur. Using data collected from a survey in freshwater cladoceran communities, landscape population genetic data and phenotypic trait data measured in a common garden, we applied a Bayesian linear model to assess whether the impact of local trait evolution in the keystone species Daphnia magna on cladoceran community trait values could be predicted by population genetic properties (within-population genetic diversity, genetic distance among populations), ecological properties (Simpson's diversity, phenotypic divergence) or environmental divergence. We found that the impact of local trait evolution varied among communities. Moreover, community diversity and phenotypic divergence were found to be better predictors of the contribution of evolution to community trait values than environmental features or genetic properties of the evolving species. Our results thus indicate the importance of ecological context for the impact of evolution on community features. Our study also demonstrates one way to detect signatures of eco-evolutionary interactions in communities inhabiting heterogeneous landscapes using survey data of contemporary ecological and evolutionary structure.     

Ecological opportunity and the origin of adaptive radiations

Ecological opportunity – through entry into a new environment, the origin of a key innovation or extinction of antagonists – is widely thought to link ecological population dynamics to evolutionary diversification. The population‐level processes arising from ecological opportunity are well documented under the concept of ecological release. However, there is little consensus as to how these processes promote phenotypic diversification, rapid speciation and adaptive radiation. We propose that ecological opportunity could promote adaptive radiation by generating specific changes to the selective regimes acting on natural populations, both by relaxing effective stabilizing selection and by creating conditions that ultimately generate diversifying selection. We assess theoretical and empirical evidence for these effects of ecological opportunity and review emerging phylogenetic approaches that attempt to detect the signature of ecological opportunity across geological time. Finally, we evaluate the evidence for the evolutionary effects of ecological opportunity in the diversification of Caribbean Anolis lizards. Some of the processes that could link ecological opportunity to adaptive radiation are well documented, but others remain unsupported. We suggest that more study is required to characterize the form of natural selection acting on natural populations and to better describe the relationship between ecological opportunity and speciation rates.     

Beyond simple adaptation: Incorporating other evolutionary processes and concepts into eco-evolutionary dynamics

Studies of eco-evolutionary dynamics have integrated evolution with ecological processes at multiple scales (populations, communities and ecosystems) and with multiple interspecific interactions (antagonistic, mutualistic and competitive). However, evolution has often been conceptualised as a simple process: short-term directional adaptation that increases population growth. Here we argue that diverse other evolutionary processes, well studied in population genetics and evolutionary ecology, should also be considered to explore the full spectrum of feedback between ecological and evolutionary processes. Relevant but underappreciated processes include (1) drift and mutation, (2) disruptive selection causing lineage diversification or speciation reversal and (3) evolution driven by relative fitness differences that may decrease population growth. Because eco-evolutionary dynamics have often been studied by population and community ecologists, it will be important to incorporate a variety of concepts in population genetics and evolutionary ecology to better understand and predict eco-evolutionary dynamics in nature.     

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.     

Molecular ecological approaches to studying the evolutionary impact of selective harvesting in wildlife

Harvesting of wildlife populations by humans is usually targeted by sex, age or phenotypic criteria, and is therefore selective. Selective harvesting has the potential to elicit a genetic response from the target populations in several ways. First, selective harvesting may affect population demographic structure (age structure, sex ratio), which in turn may have consequences for effective population size and hence genetic diversity. Second, wildlife-harvesting regimes that use selective criteria based on phenotypic characteristics (e.g. minimum body size, horn length or antler size) have the potential to impose artificial selection on harvested populations. If there is heritable genetic variation for the target characteristic and harvesting occurs before the age of maturity, then an evolutionary response over time may ensue. Molecular ecological techniques offer ways to predict and detect genetic change in harvested populations, and therefore have great utility for effective wildlife management. Molecular markers can be used to assess the genetic structure of wildlife populations, and thereby assist in the prediction of genetic impacts by delineating evolutionarily meaningful management units. Genetic markers can be used for monitoring genetic diversity and changes in effective population size and breeding systems. Tracking evolutionary change at the phenotypic level in the wild through quantitative genetic analysis can be made possible by genetically determined pedigrees. Finally, advances in genome sequencing and bioinformatics offer the opportunity to study the molecular basis of phenotypic variation through trait mapping and candidate gene approaches. With this understanding, it could be possible to monitor the selective impacts of harvesting at a molecular level in the future. Effective wildlife management practice needs to consider more than the direct impact of harvesting on population dynamics. Programs that utilize molecular genetic tools will be better positioned to assess the long-term evolutionary impact of artificial selection on the evolutionary trajectory and viability of harvested populations.     

Demographic variability and heterogeneity among individuals within and among clonal bacteria strains

Identifying what drives individual heterogeneity has been of long interest to ecologists, evolutionary biologists and biodemographers, because only such identification provides deeper understanding of ecological and evolutionary population dynamics. In natural populations one is challenged to accurately decompose the drivers of heterogeneity among individuals as genetically fixed or selectively neutral. Rather than working on wild populations we present here data from a simple bacterial system in the lab, Escherichia coli. Our system, based on cutting‐edge microfluidic techniques, provides high control over the genotype and the environment. It therefore allows to unambiguously decompose and quantify fixed genetic variability and dynamic stochastic variability among individuals. We show that within clonal individual variability (dynamic heterogeneity) in lifespan and lifetime reproduction is dominating at about 90–92%, over the 8–10% genetically (adaptive fixed) driven differences. The genetic differences among the clonal strains still lead to substantial variability in population growth rates (fitness), but, as well understood based on foundational work in population genetics, the within strain neutral variability slows adaptive change, by enhancing genetic drift, and lowering overall population growth. We also revealed a surprising diversity in senescence patterns among the clonal strains, which indicates diverse underlying cell‐intrinsic processes that shape these demographic patterns. Such diversity is surprising since all cells belong to the same bacteria species, E. coli, and still exhibit patterns such as classical senescence, non‐senescence, or negative senescence. We end by discussing whether similar levels of non‐genetic variability might be detected in other systems and close by stating the open questions how such heterogeneity is maintained, how it has evolved, and whether it is adaptive.     

Rapid evolution and the convergence of ecological and evolutionary time

Recent studies have documented rates of evolution of ecologically important phenotypes sufficiently fast that they have the potential to impact the outcome of ecological interactions while they are underway. Observations of this type go against accepted wisdom that ecological and evolutionary dynamics occur at very different time scales. While some authors have evaluated the rapidity of a measured evolutionary rate by comparing it to the overall distribution of measured evolutionary rates, we believe that ecologists are mainly interested in rapid evolution because of its potential to impinge on ecological processes. We therefore propose that rapid evolution be defined as a genetic change occurring rapidly enough to have a measurable impact on simultaneous ecological change. Using this definition we propose a framework for decomposing rates of ecological change into components driven by simultaneous evolutionary change and by change in a non‐evolutionary factor (e.g. density dependent population dynamics, abiotic environmental change). Evolution is judged to be rapid in this ecological context if its contribution to ecological change is large relative to the contribution of other factors. We provide a worked example of this approach based on a theoretical predator–prey interaction [ Abrams, P. & Matsuda, H. (1997) . Evolution, 51, 1740], and find that in this system the impact of prey evolution on predator per capita growth rate is 63% that of internal ecological dynamics. We then propose analytical methods for measuring these contributions in field situations, and apply them to two long‐term data sets for which suitable ecological and evolutionary data exist. For both data sets relatively high rates of evolutionary change have been found when measured as character change in standard deviations per generation (haldanes). For Darwin's finches evolving in response to fluctuating rainfall [ Grant, P.R. & Grant, B.R. (2002) . Science, 296, 707], we estimate that evolutionary change has been more rapid than ecological change by a factor of 2.2. For a population of freshwater copepods whose life history evolves in response to fluctuating fish predation [ Hairston, N.G. Jr & Dillon, T.A. (1990) . Evolution, 44, 1796], we find that evolutionary change has been about one quarter the rate of ecological change – less than in the finch example, but nevertheless substantial. These analyses support the view that in order to understand temporal dynamics in ecological processes it is critical to consider the extent to which the attributes of the system under investigation are simultaneously changing as a result of rapid evolution.     

The evolutionary ecology of the major histocompatibility complex

The major histocompatibility complex (MHC) has become a paradigm for how selection can act to maintain adaptively important genetic diversity in natural populations. Here, we review the contribution of studies on the MHC in non-model species to our understanding of how selection affects MHC diversity, emphasising how ecological and ethological processes influence the tempo and mode of evolution at the MHC, and conversely, how variability at the MHC affects individual fitness, population dynamics and viability. We focus on three main areas: the types of information that have been used to detect the action of selection on MHC genes; the relative contributions of parasite-mediated and sexual selection on the maintenance of MHC diversity; and possible future lines of research that may help resolve some of the unanswered issues associated with MHC evolution.     

Detecting and managing fisheries-induced evolution

Exploitation of fish populations can induce evolutionary responses in life histories. For example, fisheries targeting large individuals are expected to select for early maturation at smaller sizes, leading to reduced fecundity and thus also reduced fisheries yield. These predicted phenotypic shifts have been observed in several fish stocks, but disentangling the environmental and genetic causes behind them has proved difficult. Here, we review recent studies investigating phenotypic shifts in exploited populations and strategies for minimizing fisheries-induced evolution. Responses to selective harvesting will depend on species-specific life-history traits, and on community-level and environmental processes. Therefore, the detection of fisheries-induced evolution and successful fish stock management requires routine population monitoring, and a good understanding of genetics, relevant ecological processes and changing environmental conditions.     

The role of migration in the evolution of phenotypic switching

Stochastic switching is an example of phenotypic bet hedging, where an individual can switch between different phenotypic states in a fluctuating environment. Although the evolution of stochastic switching has been studied when the environment varies temporally, there has been little theoretical work on the evolution of phenotypic switching under both spatially and temporally fluctuating selection pressures. Here, we explore the interaction of temporal and spatial change in determining the evolutionary dynamics of phenotypic switching. We find that spatial variation in selection is important; when selection pressures are similar across space, migration can decrease the rate of switching, but when selection pressures differ spatially, increasing migration between demes can facilitate the evolution of higher rates of switching. These results may help explain the diverse array of non-genetic contributions to phenotypic variability and phenotypic inheritance observed in both wild and experimental populations.     

Predator-induced plasticity does not alter the pathway from evolution to ecology among locally adapted populations of <Emphasis Type="Italic">Daphnia</Emphasis>

In the growing field of eco-evolutionary dynamics, evidence for an influence of rapid shifts in phenotype on ecological processes is accumulating, yet, the contributions of phenotypic plasticity versus genetic change to these observed ecological changes are unclear. In one of the best studied ecosystems in terms of eco-evolutionary dynamics, landlocked versus anadromous alewife (Alosa pseudoharengus) have caused strong evolutionary divergence in their key zooplankton prey (Daphnia ambigua). We previously showed that such evolutionary differences have cascading ecological effects on consumer-resource dynamics and primary production. Yet, these locally adapted populations of Daphnia also differ in trait plasticity, which may, in turn, modify the pathway from evolution to ecology. Here we compared Daphnia from lakes with landlocked versus anadromous alewife for differences in rates of population growth in the presence and absence of predator cues over the course of a 39-day experiment. We predicted that predator-induced shifts in life history traits would facilitate faster rates of population growth. Contrary to our expectations, predator cue exposure did not alter rates of population growth. We instead found that Daphnia from lakes with landlocked alewife ultimately attained higher population densities (and exhibited faster population growth) when compared with Daphnia from lakes with anadromous alewife. Based on our previous work, these population level responses were unexpected, as Daphnia from lakes with landlocked alewife exhibit slower rates of somatic growth and delayed maturation. We discuss our results in lieu of the known differences in plasticity and how the population growth patterns may be influenced by resource limitation.     

Zooplankton research: the contribution of limnology to general ecological paradigms

Biotic interactions and density dependent processes are particularly important in the pelagic zone of a lake. Plankton has numerous properties (e.g., short life cycles, size structure) that makes them suitable objects for testing hypotheses and developing concepts relevant for general ecology. Zooplankton being in the center of aquatic food webs and influenced strongly by both bottom-up and top-down processes have often been used as models for ecological paradigms. The trophic-dynamic concept, the theory of population dynamics, and the analysis of predator-prey relationships are examples of successful contributions of zooplankton research. In recent years, zooplankton research has developed new ideas in community, population and evolutionary ecology. This is illustrated by studies on mechanisms of seasonal succession, competition and phenotypic plasticity. The new concept of physiological ecology is explained with copepod diapause behaviour. The blending of ideas from ecology and evolutionary genetics, which is undergoing a rapid development of new tools, will create new paradigms in the future, and zooplankton research will play an important part in this process.     

The contributions of age and sex to variation in common tern population growth rate

1. The decomposition of population growth rate into contributions from different demographic rates has many applications, ranging from evolutionary biology to conservation and management. Demographic rates with low variance may be pivotal for population persistence, but variable rates can have a dramatic influence on population growth rate. 2. In this study, the mean and variance in population growth rate (lambda) is decomposed into contributions from different ages and demographic rates using prospective and retrospective matrix analyses for male and female components of an increasing common tern (Sterna hirundo) population. 3. Three main results emerged: (1) subadult return was highly influential in prospective and retrospective analyses; (2) different age-classes made different contributions to variation in lambda: older age classes consistently produced offspring whereas young adults performed well only in high quality years; and (3) demographic rate covariation explained a significant proportion of variation in both sexes. A large contribution to lambda did not imply a large contribution to its variation. 4. This decomposition strengthens the argument that the relationship between variation in demographic rates and variation in lambda is complex. Understanding this relationship and its consequences for population persistence and evolutionary change demands closer examination of the lives, and deaths, of the individuals within populations within species.     

Lessons learned from the dog genome

Extensive genetic resources and a high-quality genome sequence position the dog as an important model species for understanding genome evolution, population genetics and genes underlying complex phenotypic traits. Newly developed genomic resources have expanded our understanding of canine evolutionary history and dog origins. Domestication involved genetic contributions from multiple populations of gray wolves probably through backcrossing. More recently, the advent of controlled breeding practices has segregated genetic variability into distinct dog breeds that possess specific phenotypic traits. Consequently, genome-wide association and selective sweep scans now allow the discovery of genes underlying breed-specific characteristics. The dog is finally emerging as a novel resource for studying the genetic basis of complex traits, including behavior.     

The role of environment and core‐margin effects on range‐wide phenotypic variation in a montane grasshopper

The integration of genetic information with ecological and phenotypic data constitutes an effective approach to gain insight into the mechanisms determining interpopulation variability and the evolutionary processes underlying local adaptation and incipient speciation. Here, we use the Pyrenean Morales grasshopper (Chorthippus saulcyi moralesi) as study system to (i) analyse the relative role of genetic drift and selection in range‐wide patterns of phenotypic differentiation and (ii) identify the potential selective agents (environment, elevation) responsible for variation. We also test the hypothesis that (iii) the development of dispersal‐related traits is associated with different parameters related to population persistence/turnover, including habitat suitability stability over the last 120 000 years, distance to the species distribution core and population genetic variability. Our results indicate that selection shaped phenotypic differentiation across all the studied morphological traits (body size, forewing length and shape). Subsequent analyses revealed that among‐population differentiation in forewing length was significantly explained by a temperature gradient, suggesting an adaptive response to thermoregulation or flight performance under contrasting temperature regimes. We found support for our hypothesis predicting a positive association between the distance to the species distribution core and the development of dispersal‐related morphology, which suggests an increased dispersal capability in populations located at range edges that, in turn, exhibit lower levels of genetic variability. Overall, our results indicate that range‐wide patterns of phenotypic variation are partially explained by adaptation in response to local environmental conditions and differences in habitat persistence between core and peripheral populations.     

Which evolutionary processes influence natural genetic variation for phenotypic traits?

Although many studies provide examples of evolutionary processes such as adaptive evolution, balancing selection, deleterious variation and genetic drift, the relative importance of these selective and stochastic processes for phenotypic variation within and among populations is unclear. Theoretical and empirical studies from humans as well as natural animal and plant populations have made progress in examining the role of these evolutionary forces within species. Tentative generalizations about evolutionary processes across species are beginning to emerge, as well as contrasting patterns that characterize different groups of organisms. Furthermore, recent technical advances now allow the combination of ecological measurements of selection in natural environments with population genetic analysis of cloned QTLs, promising advances in identifying the evolutionary processes that influence natural genetic variation.     

The role of changes in environmental quality in multitrait plastic responses to environmental and social change in the model microalga Chlamydomonas reinhardtii

Intraspecific variation plays a key role in species'' responses to environmental change; however, little is known about the role of changes in environmental quality (the population growth rate an environment supports) on intraspecific trait variation. Here, we hypothesize that intraspecific trait variation will be higher in ameliorated environments than in degraded ones. We first measure the range of multitrait phenotypes over a range of environmental qualities for three strains and two evolutionary histories of Chlamydomonas reinhardtii in laboratory conditions. We then explore how environmental quality and trait variation affect the predictability of lineage frequencies when lineage pairs are grown in indirect co‐culture. Our results show that environmental quality has the potential to affect intraspecific variability both in terms of the variation in expressed trait values, and in terms of the genotype composition of rapidly growing populations. We found low phenotypic variability in degraded or same‐quality environments and high phenotypic variability in ameliorated conditions. This variation can affect population composition, as monoculture growth rate is a less reliable predictor of lineage frequencies in ameliorated environments. Our study highlights that understanding whether populations experience environmental change as an increase or a decrease in quality relative to their recent history affects the changes in trait variation during plastic responses, including growth responses to the presence of conspecifics. This points toward a fundamental role for changes in overall environmental quality in driving phenotypic variation within closely related populations, with implications for microevolution.     

Neutral markers, ecologically relevant traits, and the structure of genetic variation in Daphnia

Zooplankton, Daphnia in particular, are increasingly used as model organisms to investigate general evolutionary biological questions. I here discuss some recent insights into the patterns and processes determining genetic diversity within and genetic differentiation among natural populations of cyclically parthenogenetic Daphnia. I focus on three aspects: (1) the interplay of phenotypic plasticity and genetic polymorphism in explaining variability in ecologically relevant traits, (2) the patterns of genetic variation revealed by neutral markers and ecologically relevant traits, and (3) the evolutionary ecological importance of hybridization events in Daphnia. The need for studies on the evolutionary ecology of sexual reproduction and dispersal via ephippial eggs in Daphnia is stressed.     

The Rediscovery of a Long Described Species Reveals Additional Complexity in Speciation Patterns of Poeciliid Fishes in Sulfide Springs

The process of ecological speciation drives the evolution of locally adapted and reproductively isolated populations in response to divergent natural selection. In Southern Mexico, several lineages of the freshwater fish species of the genus Poecilia have independently colonized toxic, hydrogen sulfide-rich springs. Even though ecological speciation processes are increasingly well understood in this system, aligning the taxonomy of these fish with evolutionary processes has lagged behind. While some sulfide spring populations are classified as ecotypes of Poecilia mexicana, others, like P. sulphuraria, have been described as highly endemic species. Our study particularly focused on elucidating the taxonomy of the long described sulfide spring endemic, Poecilia thermalis Steindachner 1863, and investigates if similar evolutionary patterns of phenotypic trait divergence and reproductive isolation are present as observed in other sulfidic species of Poecilia. We applied a geometric morphometric approach to assess body shape similarity to other sulfidic and non-sulfidic fish of the genus Poecilia. We also conducted phylogenetic and population genetic analyses to establish the phylogenetic relationships of P. thermalis and used a population genetic approach to determine levels of gene flow among Poecilia from sulfidic and non-sulfidic sites. Our results indicate that P. thermalis'' body shape has evolved in convergence with other sulfide spring populations in the genus. Phylogenetic analyses placed P. thermalis as most closely related to one population of P. sulphuraria, and population genetic analyses demonstrated that P. thermalis is genetically isolated from both P. mexicana ecotypes and P. sulphuraria. Based on these findings, we make taxonomic recommendations for P. thermalis. Overall, our study verifies the role of hydrogen sulfide as a main factor shaping convergent, phenotypic evolution and the emergence of reproductive isolation between Poecilia populations residing in adjacent sulfidic and non-sulfidic environments.