Unexpected collective larval dispersal but little support for sweepstakes reproductive success in the highly dispersive brooding mollusc Crepidula fornicata

Abstract

In many marine invertebrates, long-distance dispersal is achieved during an extended pelagic larval phase. Although such dispersal should result in high gene flow over broad spatial scales, fine-scale genetic structure has often been reported, a pattern attributed to interfamilial variance in reproductive success and limited homogenization during dispersal. To examine this hypothesis, the genetic diversity of dispersing larvae must be compared with the postdispersal stages, that is benthic recruits and adults. Such data remain, however, scarce due to the difficulty to sample and analyse larvae of minute size. Here, we carried out such an investigation using the marine gastropod Crepidula fornicata. Field sampling of three to four larval pools was conducted over the reproductive season and repeated over 3 years. The genetic composition of larval pools, obtained with 16 microsatellite loci, was compared with that of recruits and adults sampled from the same site and years. In contrast to samples of juveniles and adults, large genetic temporal variations between larval pools produced at different times of the same reproductive season were observed. In addition, full- and half-sibs were detected in early larvae and postdispersal juveniles, pointing to correlated dispersal paths between several pairs of individuals. Inbred larvae were also identified. Such collective larval dispersal was unexpected given the long larval duration of the study species. Our results suggest that each larval pool is produced by a small effective number of reproducers but that, over a reproductive season, the whole larval pool is produced by large numbers of reproducers across space and time.

The formation of marine kin structure: effects of dispersal, larval cohesion, and variable reproductive success

“…Therefore, if the “lucky” adults vary over time, reproductive success may be more evenly distributed across the cumulative reproductive season, as evidenced recently in a brooding mollusc (Riquet et al. ). These factors would all weaken the strong effect of variable reproductive success on kinship, which was predicted by our model.…”

“…, Riquet et al. ) research. Generally, collective dispersal refers to correlated dispersal paths without specific reference to kinship.…”

“…Although point estimates have identified putative siblings within a larval pool (Riquet et al. ), combined genetic‐otolith microchemistry analyses revealed that individuals identified as cohesive larvae were not closely related (Ben‐Tzvi et al. ).…”

“…, Riquet et al. ). These findings challenge conventional views of kinship in the sea and raise questions about how kin associations persist despite the potential for dispersal to disrupt them.…”

“…, Riquet et al. ). While there is evidence from otolith microchemistry that some individuals within larval cohorts have shared dispersal pathways for part of the larval phase (Ben‐Tzvi et al.…”