Rapid genomic convergent evolution in experimental populations of Trinidadian guppies (Poecilia reticulata)

This is the final version. Available on open access from Wiley via the DOI in this recordData archiving: The data that support these findings are openly available at: European Nucleotide Archive (https://www.ebi.ac.uk/ena/ browser/home)—reference numbers: PRJEB42705 (all introduction populations) and PRJEB10680 (GHP). All scripts and associated data are available on Github repository: mapping and SNP calling (https://github.com/josieparis/gatk-snp-calling); population genomics and haplotype scans (https://github.com/ bfraser-commits/Rapid_genomic_adaptation_guppies); the software for multivariate AF analyses (AF-vapeR) (https://github. com/JimWhiting91/afvaper); and simulation analyses (https:// github.com/JimWhiting91/fibr_simulations).Although rapid phenotypic evolution has been documented often, the genomic basis of rapid adaptation to natural environments is largely unknown in multicellular organisms. Population genomic studies of experimental populations of Trinidadian guppies (Poecilia reticulata) provide a unique opportunity to study this phenomenon. Guppy populations that were transplanted from high-predation (HP) to low-predation (LP) environments have been shown to evolve toward the phenotypes of naturally colonized LP populations in as few as eight generations. These changes persist in common garden experiments, indicating that they have a genetic basis. Here, we report results of whole genome variation in four experimental populations colonizing LP sites along with the corresponding HP source population. We examined genome-wide patterns of genetic variation to estimate past demography and used a combination of genome scans, forward simulations, and a novel analysis of allele frequency change vectors to uncover the signature of selection. We detected clear signals of population growth and bottlenecks at the genome-wide level that matched the known history of population numbers. We found a region on chromosome 15 under strong selection in three of the four populations and with our multivariate approach revealing subtle parallel changes in allele frequency in all four populations across this region. Investigating patterns of genome-wide selection in this uniquely replicated experiment offers remarkable insight into the mechanisms underlying rapid adaptation, providing a basis for comparison with other species and populations experiencing rapidly changing environments.Max Planck SocietyEuropean Research Council (ERC)Natural Environment Research Council (NERC)University of SussexUniversity of ExeterNational Science Foundation (NSF

Does Intraspecific Size Variation in a Predator Affect Its Diet Diversity and Top-Down Control of Prey?

It has long been known that intraspecific variation impacts evolutionary processes, but only recently have its potential ecological effects received much attention. Theoretical models predict that genetic or phenotypic variance within species can alter interspecific interactions, and experiments have shown that genotypic diversity in clonal species can impact a wide range of ecological processes. To extend these studies to quantitative trait variation within populations, we experimentally manipulated the variance in body size of threespine stickleback in enclosures in a natural lake environment. We found that body size of stickleback in the lake is correlated with prey size and (to a lesser extent) composition, and that stickleback can exert top-down control on their benthic prey in enclosures. However, a six-fold contrast in body size variance had no effect on the degree of diet variation among individuals, or on the abundance or composition of benthic or pelagic prey. Interestingly, post-hoc analyses revealed suggestive correlations between the degree of diet variation and the strength of top-down control by stickleback. Our negative results indicate that, unless the correlation between morphology and diet is very strong, ecological variation among individuals may be largely decoupled from morphological variance. Consequently we should be cautious in our interpretation both of theoretical models that assume perfect correlations between morphology and diet, and of empirical studies that use morphological variation as a proxy for resource use diversity

Double trouble at high density::Cross-level test of ressource-related adaptive plasticity and crowding-related fitness.

Population size is often regulated by negative feedback between population density and individual fitness. At high population densities, animals run into double trouble: they might concurrently suffer from overexploitation of resources and also from negative interference among individuals regardless of resource availability, referred to as crowding. Animals are able to adapt to resource shortages by exhibiting a repertoire of life history and physiological plasticities. In addition to resource-related plasticity, crowding might lead to reduced fitness, with consequences for individual life history. We explored how different mechanisms behind resource-related plasticity and crowding-related fitness act independently or together, using the water flea Daphnia magna as a case study. For testing hypotheses related to mechanisms of plasticity and crowding stress across different biological levels, we used an individual-based population model that is based on dynamic energy budget theory. Each of the hypotheses, represented by a sub-model, is based on specific assumptions on how the uptake and allocation of energy are altered under conditions of resource shortage or crowding. For cross-level testing of different hypotheses, we explored how well the sub-models fit individual level data and also how well they predict population dynamics under different conditions of resource availability. Only operating resource-related and crowding-related hypotheses together enabled accurate model predictions of D. magna population dynamics and size structure. Whereas this study showed that various mechanisms might play a role in the negative feedback between population density and individual life history, it also indicated that different density levels might instigate the onset of the different mechanisms. This study provides an example of how the integration of dynamic energy budget theory and individual-based modelling can facilitate the exploration of mechanisms behind the regulation of population size. Such understanding is important for assessment, management and the conservation of populations and thereby biodiversity in ecosystems

Integrating ecology and evolutionary theory. A game changer for biodiversity conservation?

Currently, one of the central arguments in favour of biodiversity conservation is that it is essential for the maintenance of ecosystem services, that is, the benefits that people receive from ecosystems. However, the relationship between ecosystem services and biodiversity is contested and needs clarification. The goal of this chapter is to spell out the interaction and reciprocal influences between conservation science, evolutionary biology, and ecology, in order to understand whether a stronger integration of evolutionary and ecological studies might help clarify the interaction between biodiversity and ecosystem functioning as well as influence biodiversity conservation practices. To this end, the eco-evolutionary feedback theory proposed by David Post and Eric Palkovacs is analysed, arguing that it helps operationalise niche construction theory and develop a more sophisticated understanding of the relationship between ecosystem functioning and biodiversity. Finally, it is proposed that by deepening the integration of ecological and evolutionary factors in our understanding of ecosystem functioning, the eco-evolutionary feedback theory is supportive of an “evolutionary-enlightened management” of biodiversity within the ecosystem services approach.info:eu-repo/semantics/publishedVersio

Common garden experiments in the genomic era : new perspectives and opportunities

PdV was supported by a doctoral studentship from the French Ministère de la Recherche et de l’Enseignement Supérieur. OEG was supported by the Marine Alliance for Science and Technology for Scotland (MASTS)The study of local adaptation is rendered difficult by many evolutionary confounding phenomena (e.g. genetic drift and demographic history). When complex traits are involved in local adaptation, phenomena such as phenotypic plasticity further hamper evolutionary biologists to study the complex relationships between phenotype, genotype and environment. In this perspective paper, we suggest that the common garden experiment, specifically designed to deal with phenotypic plasticity has a clear role to play in the study of local adaptation, even (if not specifically) in the genomic era. After a quick review of some high-throughput genotyping protocols relevant in the context of a common garden, we explore how to improve common garden analyses with dense marker panel data and recent statistical methods. We then show how combining approaches from population genomics and genome-wide association studies with the settings of a common garden can yield to a very efficient, thorough and integrative study of local adaptation. Especially, evidence from genomic (e.g. genome scan) and phenotypic origins constitute independent insights into the possibility of local adaptation scenarios, and genome-wide association studies in the context of a common garden experiment allow to decipher the genetic bases of adaptive traits.PostprintPeer reviewe

Size-dependent intraguild predation, cannibalism, and resource allocation determine the outcome of species coexistence

Intraguild predation (IGP), a system in which species compete for resources and prey upon each other, is more common than existing theory predicts. In theory, an IG predator and its prey can coexist if the IG predator is a weaker competitor for a shared resource and the predator directly benefits from consuming the prey. However, many species that are IG predators also consume members of their own species (cannibalism). Here we ask whether cannibalism can help resolve the paradox of IGP systems. Our approach differs from previous work on IGP and cannibalism by explicitly considering the size-dependence of predatory interactions and how the benefits of predation are allocated to survival, growth, and fecundity of the predator or cannibal. Our results show that cannibalism facilitates coexistence under conditions that are opposite of those predicted by standard IGP theory: species can coexist when the cannibal is a better competitor on the shared resources, directly benefits little from consuming conspecifics, and allocates resources from predation more towards growth and fecundity over survival. Because the effects IGP and cannibalism are opposite, when an IGP predator is also a cannibal, coexistence between the IGP predator and its prey is not possible and instead depends on the operation of other coexistence mechanisms (e.g. resource partitioning). These results point to the importance of understanding the relative rates of IGP and cannibalism as well as the resource allocation strategy of the IG predator in determining the likelihood of species coexistence

Competitive asymmetry and local adaptation in Trinidadian guppies

1. The outcome of competition between individuals often depends on body size. These competitive asymmetries can drive variation in demographic rates, influencing the ecology and evolution of life histories. The magnitude and direction of such asymmetries differ among taxa, yet little is known empirically about how adaptation to resource limitation alters competitive asymmetries. 2. Here, we investigate the relationship between size‐dependent competitive ability and adaptation to resource limitation. 3. We examined size‐dependent competition in two ecotypes of Trinidadian guppy, adapted to high or low levels of resource competition. Using aquaria‐based competition experiments, we describe how the size and ecotype of competitors influence somatic growth rate, whilst controlling for the confounding effect of niche differentiation. We replicated our study across two independent evolutionary origins of the “competitive” ecotype. 4. The two “competitive” ecotypes differed markedly in size‐dependent asymmetry, indicating that adaptation to resource limitation alone is insufficient to explain changes in size‐dependent competitive asymmetry. For one origin, the ecotype adapted to resource limitation was a superior competitor over a wide range of size pairings. 5. The equivalence of competitors varied over fivefold, dependent on size and ecotype; in three of four populations, larger individuals had a competitive advantage. 6. Our results demonstrate that competitive asymmetry has strong effects on somatic growth. Because somatic growth contributes to demographic parameters, intraspecific trait variation is likely to play a key role in regulating demographic rates. Our findings imply that the evolution of size‐dependent asymmetries under conditions of intense competition is likely to be constrained by niche availability, although further research is needed to verify this

Competitive asymmetry and local adaptation in Trinidadian guppies

1. The outcome of competition between individuals often depends on body size. These competitive asymmetries can drive variation in demographic rates, influencing the ecology and evolution of life histories. The magnitude and direction of such asymmetries differ among taxa, yet little is known empirically about how adaptation to resource limitation alters competitive asymmetries. 2. Here, we investigate the relationship between size‐dependent competitive ability and adaptation to resource limitation. 3. We examined size‐dependent competition in two ecotypes of Trinidadian guppy, adapted to high or low levels of resource competition. Using aquaria‐based competition experiments, we describe how the size and ecotype of competitors influence somatic growth rate, whilst controlling for the confounding effect of niche differentiation. We replicated our study across two independent evolutionary origins of the “competitive” ecotype. 4. The two “competitive” ecotypes differed markedly in size‐dependent asymmetry, indicating that adaptation to resource limitation alone is insufficient to explain changes in size‐dependent competitive asymmetry. For one origin, the ecotype adapted to resource limitation was a superior competitor over a wide range of size pairings. 5. The equivalence of competitors varied over fivefold, dependent on size and ecotype; in three of four populations, larger individuals had a competitive advantage. 6. Our results demonstrate that competitive asymmetry has strong effects on somatic growth. Because somatic growth contributes to demographic parameters, intraspecific trait variation is likely to play a key role in regulating demographic rates. Our findings imply that the evolution of size‐dependent asymmetries under conditions of intense competition is likely to be constrained by niche availability, although further research is needed to verify this

The effects of asymmetric competition on the life history of Trinidadian guppies.

The effects of asymmetric interactions on population dynamics has been widely investigated, but there has been little work aimed at understanding how life history parameters like generation time, life expectancy and the variance in lifetime reproductive success are impacted by different types of competition. We develop a new framework for incorporating trait-mediated density-dependence into size-structured models and use Trinidadian guppies to show how different types of competitive interactions impact life history parameters. Our results show the degree of symmetry in competitive interactions can have dramatic effects on the speed of the life history. For some vital rates, shifting the competitive superiority from small to large individuals resulted in a doubling of the generation time. Such large influences of competitive symmetry on the timescale of demographic processes, and hence evolution, highlights the interwoven nature of ecological and evolutionary processes and the importance of density-dependence in understanding eco-evolutionary dynamics

Novel parasite invasion leads to rapid demographic compensation and recovery in an experimental population of guppies (Poecilia reticulata)

The global movement of pathogens is altering populations and communities through a variety of direct and indirect ecological pathways. The direct effect of a pathogen on a host is reduced survival, which can lead to decreased population densities. However, theory also suggests that increased mortality can lead to no change or even increases in the density of the host. This paradoxical result can occur in a regulated population when the pathogen’s negative effect on survival is countered by increased reproduction at the lower density. Here, we analyze data from a long-term capture–mark–recapture experiment of Trinidadian guppies (Poecilia reticulata) that were recently infected with a nematode parasite (Camallanus cotti). By comparing the newly infected population with a control population that was not infected, we show that decreases in the density of the infected guppy population were transient. The guppy population compensated for the decreased survival by a density-dependent increase in recruitment of new individuals into the population, without any change in the underlying recruitment function. Increased recruitment was related to an increase in the somatic growth of uninfected fish. Twenty months into the new invasion, the population had fully recovered to preinvasion densities even though the prevalence of infection of fish in the population remained high (72%). These results show that density-mediated indirect effects of novel parasites can be positive, not negative, which makes it difficult to extrapolate to how pathogens will affect species interactions in communities. We discuss possible hypotheses for the rapid recovery