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We document an extreme example of reproductive trait evolution that affects population genetic structure in sister species of Parvulastra cushion stars from Australia. Self-fertilization by hermaphroditic adults and brood protection of benthic larvae causes strong inbreeding and range-wide genetic poverty. Most samples were fixed for a single allele at nearly all nuclear loci; heterozygotes were extremely rare (0.18%); mitochondrial DNA sequences were more variable, but few populations shared haplotypes in common. Isolation-with-migration models suggest that these patterns are caused by population bottlenecks (relative to ancestral population size) and low gene flow. Loss of genetic diversity and low potential for dispersal between high-intertidal habitats may have dire consequences for extinction risk and potential for future adaptive evolution in response to climate and other selective agents.

Patterns of population genetic variation have frequently been understood as consequences of life history covariates such as dispersal ability and breeding systems (e.g. selfing). For example, marine invertebrates show enormous variation in life history traits that are correlated with the extent of gene flow between populations and the magnitude of differentiation among populations at neutral genetic markers (FST). Here we document an unexpected correlation between marine invertebrate life histories and deviation from Hardy-Weinberg equilibrium (non-zero values of FIS, the inbreeding coefficient). FIS values were significantly higher in studies of species with free-spawned planktonic sperm than in studies of species that copulate or have some form of direct sperm transfer to females or benthic egg masses. This result was robust to several different analytical approaches. We note several mechanisms that might contribute to this pattern, and appeal for more studies and ideas that might help to explain our observations.