Self-fertilization and inbreeding depression in three ascidian species that differ in genetic dispersal potential

Abstract

Although self-fertilization can mitigate the costs of sexual reproduction, many hermaphroditic marine invertebrates avoid selfing, presumably because of inbreeding depression. Eventually, successive generations of inbreeding are expected to reduce genetic load, but selfing cannot evolve for future benefits. Initial inbreeding costs of selfing could be offset by the immediate benefits of local adaptation and mating assurance, both of which are more likely in species with limited gene flow. We compared the likelihood of selfing and the magnitude of inbreeding depression among three ascidian species (Molgula provisionalis, Ciona intestinalis, and Botryllus schlosseri) that were known a priori to differ in larval dispersal potential. Selfing potential exhibited a negative association, and inbreeding depression a positive association with dispersal potential. M. provisionalis, with highly philopatric larvae, had no apparent barrier to self-fertilization and exhibited little evidence of inbreeding depression (ratio of survival of self to outcross progeny 10 weeks after metamorphosis was 0.999). By contrast, C. intestinalis, with highly dispersive larvae, exhibited low levels of self-fertilization in flowing water and high levels of inbreeding depression (survival ratio 14 weeks after metamorphosis of 0.274). B. schlosseri larvae have intermediate dispersal capabilities, yet exhibited low likelihood of self-fertilization and high magnitude of inbreeding depression (survival ratio 10 weeks after metamorphosis of 0.310); however, extremely long-lived sperm contribute to gene flow in B. schlosseri. These results suggest that in marine hermaphrodites, gene flow, self-fertilization, and inbreeding depression should be evaluated as an integrated suite of traits, not independent characters.