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

by Iva Popovic, Lucie A. Bergeron, Yves-Marie Bozec, Ann-Marie Waldvogel, Samantha M. Howitt, Katarina Damjanovic, Frances Patel, Maria G. Cabrera, Gert Wörheide, Sven Uthicke, Cynthia Riginos

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 N_c are found for highly abundant marine invertebrates. Yet, the influences of new mutations on π relative to extrinsic processes such as N_c 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 N_c in Australia’s Great Barrier Reef to jointly examine the determinants of π in populations undergoing extreme N_c 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 N_e (~70,000–180,000) and low N_e/N_c 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 N_e and generation time length, with important implications for explaining high mutational loads and the determinants of genetic diversity in marine invertebrate taxa.