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

Lewontin's paradox, the observation that levels of genetic diversity (pi) do not scale linearly with census population size (N-c) variation, is an evolutionary conundrum. The most extreme mismatches between pi and N-c are found for highly abundant marine invertebrates. Yet, the influences of new mutations on pi relative to extrinsic processes such as N-c fluctuations are unknown. Here, we provide the first germline mutation rate (mu) 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 pi in populations undergoing extreme N-c fluctuations. The A. cf. solaris mean mu 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 (similar to 70,000-180,000) and low N-e/N-c values (0.0047-0.048) indicated weak influences of population outbreaks on long-term pi. Our findings are consistent with elevated mu 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.