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

• Published in: PLoS genetics Vol. 20; no. 2; p. e1011129
• Main Authors: 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, Riginos, Cynthia
• Format: Journal Article
• Language: English
• Published: United States Public Library of Science 12.02.2024; Public Library of Science (PLoS)
• Subjects: Analysis; Animal reproduction; Animals; Anthozoa - genetics; Biological diversity; Biology and Life Sciences; Censuses; Confidence intervals; Coral Reefs; Crown-of-thorns starfish; Earth Sciences; Ecology and Environmental Sciences; Evolution; Gene mutations; Genetic aspects; Genetic diversity; Genomes; Genomics; Germ-Line Mutation - genetics; Hypotheses; Identification and classification; Invertebrates; Mutation; Mutation Rate; Mutation rates; Polymorphism; Population; Population Density; Population genetics; Reefs; Starfish - genetics; Whole genome sequencing; Australia
• ISSN: 1553-7404; 1553-7390; 1553-7404
• DOI: 10.1371/journal.pgen.1011129

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.