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Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations.

ABSTRACT: Predicting the rate of adaptation to environmental change in wild populations is important for understanding evolutionary change. However, predictions may be unreliable if the two key variables affecting the rate of evolutionary change-heritability and selection-are both affected by the same environmental variable. To determine how general such an environmentally induced coupling of heritability and selection is, and how this may influence the rate of adaptation, we made use of freely accessible, open data on pedigreed wild populations to answer this question at the broadest possible scale. Using 16 populations from 10 vertebrate species, which provided data on 50 traits (relating to body mass, morphology, physiology, behaviour and life history), we found evidence for an environmentally induced relationship between heritability and selection in only 6 cases, with weak evidence that this resulted in an increase or decrease in the expected selection response. We conclude that such a coupling of heritability and selection is unlikely to strongly affect evolutionary change, even though both heritability and selection are commonly postulated to be dependent on the environment.

SUBMITTER: Ramakers JJC

PROVIDER: S-EPMC6027994 | biostudies-literature | 2018 Jul

REPOSITORIES: biostudies-literature

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Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations.

Ramakers Jip J C JJC Culina Antica A Visser Marcel E ME Gienapp Phillip P

Nature ecology & evolution 20180618 7

Predicting the rate of adaptation to environmental change in wild populations is important for understanding evolutionary change. However, predictions may be unreliable if the two key variables affecting the rate of evolutionary change-heritability and selection-are both affected by the same environmental variable. To determine how general such an environmentally induced coupling of heritability and selection is, and how this may influence the rate of adaptation, we made use of freely accessible ...[more]

PMID: 29915341

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Project description:Whether sexual selection impedes or aids adaptation has become an outstanding question in times of rapid environmental change and parallels the debate about how the evolution of individual traits impacts on population dynamics. The net effect of sexual selection on population viability results from a balance between genetic benefits of "good-genes" effects and costs of sexual conflict. Depending on how these facets of sexual selection are affected under environmental change, extinction of maladapted populations could be either avoided or accelerated. Here, we evolved seed beetles under three alternative mating regimes to disentangle the contributions of sexual selection, fecundity selection, and male-female coevolution to individual reproductive success and population fitness. We compared these contributions between the ancestral environment and two stressful environments (elevated temperature and a host plant shift). We found evidence that sexual selection on males had positive genetic effects on female fitness components across environments, supporting good-genes sexual selection. Interestingly, however, when males evolved under sexual selection with fecundity selection removed, they became more robust to both temperature and host plant stress compared to their conspecific females and males from the other evolution regimes that applied fecundity selection. We quantified the population-level consequences of this sex-specific adaptation and found evidence that the cost of sociosexual interactions in terms of reduced offspring production was higher in the regime applying only sexual selection to males. Moreover, the cost tended to be more pronounced at the elevated temperature to which males from the regime were more robust compared to their conspecific females. These results illustrate the tension between individual-level adaptation and population-level viability in sexually reproducing species and suggest that the relative efficacies of sexual selection and fecundity selection can cause inherent sex differences in environmental robustness that may impact demography of maladapted populations.

Project description:BACKGROUND: Insights into the micro-evolutionary patterns of morphological traits require an assessment of the natural variation of the trait within and between populations and closely related species. The mouse mandible is a particularly suitable morphological trait for such an analysis, since it has long been used as a model to study the quantitative genetics of shape. In addition, many distinct populations, sub-species and closely related species are known for the house mouse. However, morphological comparisons among wild caught animals require an assessment in how far environmental and technical factors could interfere with the shape change measurements. RESULTS: Using geometric morphometrics, we have surveyed mandible shapes in 15 natural populations of the genus Mus, with a focus on the subspecies Mus musculus domesticus. In parallel we have carefully assessed possibly confounding technical and biological factors. We find that there are distinct differences on average between populations, subspecies and species, but these differences are smaller than differences between individuals within populations. Populations from summer-dry regions, although more ancestral, are less distinct from each other than are populations from the more recently colonized northern areas. Populations with especially distinct shapes occur in an area of sympatry of M. m. domesticus and M. spretus and on recently colonized sub-antarctic islands. We have also studied a number of inbred strains to assess in how far their mandible shapes resemble those from the wild. We find that they fall indeed into the shape space of natural variation between individuals in populations. CONCLUSIONS: Although mandible shapes in natural populations can be influenced by environmental variables, these influences are insufficient to explain the average extent of shape differences between populations, such that evolutionary processes must be invoked to explain this level of diversity. We discuss that adaptive evolution may contribute to shape changes between populations, in particular in newly colonized areas. A comparison between inbred strains and wild mice suggests that the laboratory environment has no major systematic effect on the mandible shape and that such strains can be used as representatives of the natural shape differences between individuals.

Dataset Information

Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations.

Publications

Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations.

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