Historical imprints on genetic population structure in direct-developing beach whelks (Bullia digitalis)

Abstract

Marine organisms often show deep genetic divergence between lineages that are characterized by shallow population structure. The distinction of historical and contemporary demographic forces in creating and maintaining these genetic patterns is crucial for management and conservation. In this study, we examined the genetic population structure of Bullia digitalis, a lecithotrophic sandy beach whelk that lacks a pelagic larval phase and is thus expected to show limited connectivity between populations. Mitochondrial (mt)DNA cytochrome c oxidase subunit I (COI; 540 bp, n = 214) and a reanalysis of allozyme data (14 loci, n = 735) among populations along the cool southeast Atlantic (west) and warm-temperate southwest Indian Ocean (south) coasts of southern Africa showed a strong phylogeographic break across Cape Point with mtDNA (ΦRT = 0.6, p < 0.001), but a weak break with allozymes (FRT = 0.002, p = 0.004). MtDNA gene flow occurred asymmetrically from the west to the south coast. Although there was no mtDNA differentiation between populations on either side of that break (ΦSR = 0.0), there was weak but significant isolation by distance (IBD) among south coast samples (r2 = 0.20, p = 0.039). In contrast, significant allozyme differentiation was detected on small spatial scales but without overall IBD. MtDNA mismatch analysis indicated a recent range expansion, suggesting historic population expansions, most likely during periods of lower sea levels and greater habitat continuity along southern African shores. Thus, the apparent mtDNA connectivity among populations of beach whelks likely reflects historic, rather than contemporary, gene flow.