TY - JOUR

T1 - High germline mutation rates, but not extreme population outbreaks, influence genetic diversity in a keystone coral predator

AU - Popovic, Iva

AU - Bergeron, Lucie A.

AU - Bozec, Yves Marie

AU - Waldvogel, Ann Marie

AU - Howitt, Samantha M.

AU - Damjanovic, Katarina

AU - Patel, Frances

AU - Cabrera, Maria G.

AU - Wörheide, Gert

AU - Uthicke, Sven

AU - Riginos, Cynthia

N1 - Publisher Copyright: © 2024 Popovic et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2024

Y1 - 2024

N2 - 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.

AB - 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.

U2 - 10.1371/journal.pgen.1011129

DO - 10.1371/journal.pgen.1011129

M3 - Journal article

C2 - 38346089

AN - SCOPUS:85184884861

VL - 20

JO - P L o S Genetics

JF - P L o S Genetics

SN - 1553-7390

IS - 2

M1 - e1011129

ER -