High germline mutation rates but not extreme population size outbreaks influence genetic diversity in crown-of-thorns sea stars

Lewontins paradox, the observation that levels of genetic diversity ({pi}) among animals do not scale linearly with variation in census population sizes (Nc), is an evolutionary conundrum, where the most extreme mismatches between {pi} and Nc are found for highly abundant marine invertebrates. Yet, whether new mutations influence {pi} relative to extrinsic processes remains unknown for most taxa. Here, we provide the first direct germline mutation rate () estimate for a marine invertebrate, using high-coverage (60x) whole-genome sequencing of wild-caught Acanthaster cf. solaris crown-of-thorns sea stars (Echinodermata). We also provide empirical estimates of adult Nc in Australias Great Barrier Reef to jointly examine the determinants of {pi}. Based on direct observations of 63 de novo mutations across 14 parent-offspring trios, the A. cf. solaris mean was 9.13 x 10-09 mutations per-site per-generation (95% CI: 6.51 x 10-09 to 1.18 x 10-08). This value exceeds estimates for other invertebrates, showing greater concordance with reported vertebrate germline mutation rates. Lower-than-expected Ne ([~]70,000-180,000) and low Ne/Nc values (0.0047-0.048) indicated significant genetic drift and weak influences of contemporary population outbreaks on long-term {pi}. Our findings of elevated and low Ne in A. cf. solaris may help explain high mutational loads and extreme polymorphism levels observed in some marine invertebrate taxa and are consistent with evolving in response to Ne (drift-barrier hypothesis). This study advances our understanding of the processes controlling levels of natural genetic variation and provides new data valuable for further testing hypotheses about mutation rate evolution across animal phyla.