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High germline mutation rates, but not extreme population outbreaks, influence genetic diversity in a keystone coral predator.

ABSTRACT: Lewontin's paradox, the observation that levels of genetic diversity (π) do not scale linearly with census population size (Nc) variation, is an evolutionary conundrum. The most extreme mismatches between π and Nc are found for highly abundant marine invertebrates. Yet, the influences of new mutations on π relative to extrinsic processes such as Nc fluctuations are unknown. Here, we provide the first germline mutation rate (μ) estimate for a marine invertebrate in corallivorous crown-of-thorns sea stars (Acanthaster cf. solaris). We use high-coverage whole-genome sequencing of 14 parent-offspring trios alongside empirical estimates of Nc in Australia's Great Barrier Reef to jointly examine the determinants of π in populations undergoing extreme Nc fluctuations. The A. cf. solaris mean μ was 9.13 x 10-09 mutations per-site per-generation (95% CI: 6.51 x 10-09 to 1.18 x 10-08), exceeding estimates for other invertebrates and showing greater concordance with vertebrate mutation rates. Lower-than-expected Ne (~70,000-180,000) and low Ne/Nc values (0.0047-0.048) indicated weak influences of population outbreaks on long-term π. Our findings are consistent with elevated μ evolving in response to reduced Ne and generation time length, with important implications for explaining high mutational loads and the determinants of genetic diversity in marine invertebrate taxa.

SUBMITTER: Popovic I

PROVIDER: S-EPMC10861045 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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High germline mutation rates, but not extreme population outbreaks, influence genetic diversity in a keystone coral predator.

Popovic Iva I Bergeron Lucie A LA Bozec Yves-Marie YM Waldvogel Ann-Marie AM Howitt Samantha M SM Damjanovic Katarina K Patel Frances F Cabrera Maria G MG Wörheide Gert G Uthicke Sven S Riginos Cynthia C

PLoS genetics 20240212 2

Lewontin's paradox, the observation that levels of genetic diversity (π) do not scale linearly with census population size (Nc) variation, is an evolutionary conundrum. The most extreme mismatches between π and Nc are found for highly abundant marine invertebrates. Yet, the influences of new mutations on π relative to extrinsic processes such as Nc fluctuations are unknown. Here, we provide the first germline mutation rate (μ) estimate for a marine invertebrate in corallivorous crown-of-thorns s ...[more]

PMID: 38346089

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Project description:The importance of trait variation has long been recognized in ecological and evolutionary research. The divergence of sexually dimorphic traits (e.g., body size, morphology, behavior, etc.) is primarily attributed to sexual selection, and sexual dimorphism can have consequences for diets and habitat use. Recent evidence for one aquatic predator species (adult newts; Notophthalmus viridescens) suggests that trait differences and habitat partitioning between the sexes may be important in structuring zooplankton communities. However, newts are known to increase amphibian diversity within pond communities via keystone predation. Yet, no data are available on differentiating potentially sexually dimorphic effects of newts on larval amphibian communities. Thus, we conducted a series of mesocosm experiments to determine the effects of sexual dimorphism of adult newts on larval amphibian communities. Based on previous work with newts and zooplankton, we hypothesized that male and female newts would have differing effects on prey communities. We found that female newts consumed one prey species more than male newts did and no newt treatments. There were no differences between the sexes in prey consumption of another prey species. Size at metamorphosis was greater in the presence of newts (either male or female) for wood frogs and in the presence of female newts for spotted salamanders in comparison with no newt treatments. Our findings indicate that sexual dimorphism within a known keystone predator can have differential effects on prey. Indeed, our results indicate that while the effects of predators on one response (survival) can differ between sexes, the impacts on another response (prey fitness; measured as size at metamorphosis) were similar. Our research to understand the effects of sexual dimorphism is timely as sex ratios of predators may become skewed in nature due to anthropogenic change. If intraspecific differences exist via top-down effects, then downstream impacts on prey communities may go unnoticed.

Dataset Information

High germline mutation rates, but not extreme population outbreaks, influence genetic diversity in a keystone coral predator.

Publications

High germline mutation rates, but not extreme population outbreaks, influence genetic diversity in a keystone coral predator.

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