1. High germline mutation rates, but not extreme population outbreaks, influence genetic diversity in a keystone coral predator.
- Author
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Popovic, Iva, Bergeron, Lucie A., Bozec, Yves-Marie, Waldvogel, Ann-Marie, Howitt, Samantha M., Damjanovic, Katarina, Patel, Frances, Cabrera, Maria G., Wörheide, Gert, Uthicke, Sven, and Riginos, Cynthia
- Subjects
GENETIC variation ,GENETIC load ,GENETIC drift ,WHOLE genome sequencing ,MARINE invertebrates ,PREDATION ,NUCLEOTIDE sequencing ,CORAL bleaching - Abstract
Lewontin's paradox, the observation that levels of genetic diversity (π) do not scale linearly with census population size (N
c ) 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. Author summary: Understanding how levels of genetic diversity levels are maintained in natural populations and their relationship to species abundance is central to many conservation problems. We address this question in ecologically important crown-of-thorns sea stars to advance our understanding about the determinants of genetic diversity in species undergoing extreme population size fluctuations or outbreaks. In this work, we report the first germline mutation rate estimate for a marine invertebrate using whole-genome sequencing of parent-offspring trios. Our results reveal that unexpectedly high mutational contributions and reduced effective population size (stronger genetic drift than predicted by abundance) shape genetic diversity in this species, despite outbreaking populations sizes exceeding 20–90 million individuals. Our results are consistent with theory on mutation rate evolution, whereby elevated mutation rates evolve in response to reduced effective population size or generation time length. Our findings highlight the potential importance of high mutation rates in maintaining extreme deleterious mutational loads observed in marine invertebrate taxa and moderate genetic diversity levels despite population declines. Such fundamental knowledge advances our understanding about the determinants of genetic diversity in large marine populations and is valuable for testing future hypotheses on mutation rate evolution across diverse animal phyla. [ABSTRACT FROM AUTHOR]- Published
- 2024
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