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An experimental test of temperature-dependent selection on mitochondrial haplotypes in Callosobruchus maculatus seed beetles.

ABSTRACT: Mitochondrial DNA (mtDNA) consists of few but vital maternally inherited genes that interact closely with nuclear genes to produce cellular energy. How important mtDNA polymorphism is for adaptation is still unclear. The assumption in population genetic studies is often that segregating mtDNA variation is selectively neutral. This contrasts with empirical observations of mtDNA haplotypes affecting fitness-related traits and thermal sensitivity, and latitudinal clines in mtDNA haplotype frequencies. Here, we experimentally test whether ambient temperature affects selection on mtDNA variation, and whether such thermal effects are influenced by intergenomic epistasis due to interactions between mitochondrial and nuclear genes, using replicated experimental evolution in Callosobruchus maculatus seed beetle populations seeded with a mixture of different mtDNA haplotypes. We also test for sex-specific consequences of mtDNA evolution on reproductive success, given that mtDNA mutations can have sexually antagonistic fitness effects. Our results demonstrate natural selection on mtDNA haplotypes, with some support for thermal environment influencing mtDNA evolution through mitonuclear epistasis. The changes in male and female reproductive fitness were both aligned with changes in mtDNA haplotype frequencies, suggesting that natural selection on mtDNA is sexually concordant in stressful thermal environments. We discuss the implications of our findings for the evolution of mtDNA.

SUBMITTER: Immonen E

PROVIDER: S-EPMC7593184 | biostudies-literature | 2020 Oct

REPOSITORIES: biostudies-literature

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An experimental test of temperature-dependent selection on mitochondrial haplotypes in <i>Callosobruchus maculatus</i> seed beetles.

Immonen Elina E Berger David D Sayadi Ahmed A Liljestrand-Rönn Johanna J Arnqvist Göran G

Ecology and evolution 20200917 20

Mitochondrial DNA (mtDNA) consists of few but vital maternally inherited genes that interact closely with nuclear genes to produce cellular energy. How important mtDNA polymorphism is for adaptation is still unclear. The assumption in population genetic studies is often that segregating mtDNA variation is selectively neutral. This contrasts with empirical observations of mtDNA haplotypes affecting fitness-related traits and thermal sensitivity, and latitudinal clines in mtDNA haplotype frequenci ...[more]

PMID: 33144972

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Project description:BackgroundThe thermal plasticity of life-history traits receives wide attention in the recent biological literature. Of all the temperature-dependent traits studied, developmental rates of ectotherms are especially often addressed, and yet surprisingly little is known about embryonic responses to temperature, including changes in the thermal thresholds and thermal sensitivity during early development. Even postembryonic development of many cryptically living species is understood superficially at best.ResultsThis study is the first to estimate the exact durations of developmental stages in the cowpea seed beetle C. maculatus from oviposition to adult emergence at five permissive constant temperatures from 20 to 32 °C. Early embryonic development was tracked and documented by means of destructive sampling and subsequent confocal imaging of fluorescently stained specimens. Late embryonic and early larval development was studied with the use of destructive sampling and light microscopy. Well-resolved temporal series based on thousands of embryos allowed precise timing of the following developmental events: formation of the blastoderm; formation, elongation, and retraction of the germ band; dorsal closure; the onset and completion of sclerotization of the cuticle; hatching, and penetration of the first-instar larva into the cowpea seed. Pupation and adult eclosion were observed directly through an incision in the seed coat. The thermal phenotype of C. maculatus was found to vary in the course of ontogeny and different stages scaled disproportionately with temperature, but pitfalls and caveats associated with analyses of relative durations of individual stages are also briefly discussed.ConclusionDisproportionate changes in developmental durations with temperature may have important implications when study design requires a high degree of synchronization among experimental embryos or when the occurrence of particular stages in the field is of interest, as well as in any other cases when development times need to be estimated with precision. This work provides one of the first examples of integration of embryological techniques with ecophysiological concepts and will hopefully motivate similar projects in the future. While experiments with Drosophila continue to be the main source of information on animal development, knowledge on other model species is instrumental to building a broader picture of developmental phenomena.

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.

Dataset Information

An experimental test of temperature-dependent selection on mitochondrial haplotypes in Callosobruchus maculatus seed beetles.

Publications

An experimental test of temperature-dependent selection on mitochondrial haplotypes in <i>Callosobruchus maculatus</i> seed beetles.

Similar Datasets

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