Phylogenetic evidence of the re-evolution of planktotrophy in Australian periwinkles

Abstract

The mode of development of marine invertebrates has major effects on dispersal and population structure. Species without a feeding larval stage (direct developers) are generally more genetically subdivided than species with planktotrophic (swimming and feeding) development. Evidence of the re-evolution of planktotrophy from a direct-developing ancestor has been accumulating within marine invertebrates. However, it remains unclear whether such evolutionary transitions are rare or common. The Bembicium genus (Gastropoda: Littorinidae) provides an additional opportunity to examine the re-evolution of planktotrophy. The genus includes two species with planktotrophic development (Bembicium auratum and Bembicium nanum) and three species with direct development (Bembicium vittatum, Bembicium melanostoma and Bembicium flavescens). Phylogenetic analyses based on sequences of two mitochondrial markers (COI and 16S rRNA) and one nuclear marker (ANT) provide evidence for a switch from direct development back to planktotrophy. Also, pairwise genetic distances between haplotypes reveal that the two planktotrophic species have greater genetic diversity (at the species level) than the direct developers, and the three direct-developing species are genetically structured based on geographical distance. Our study adds to growing evidence for the re-evolution of planktotrophy and suggests that the genetic basis for a switch between modes of development might be simple in marine snails.

Multigenerational hybridisation results in heterosis and facilitates adaptive introgression, with no evidence of outbreeding depression in a pair of marine gastropods

“…There were also no signi cant mtDNA haplotype or cyto-nuclear interaction effects on growth. The failure to detect outbreeding depression in the Fremantle admixed population was surprising, given the frequency it is referred to in the literature as one of the greatest risks of mixing divergent sources ( The evolution of planktotrophy from direct development has occurred more than once in Bembicium, including between the sister species studied here (Cummins et al, 2022), suggesting mode of development in these snails is controlled by relatively few genes or genes in close proximity. This perhaps reduces the potential for recombination to break up co-adapted gene complexes and limits negative genetic effects.…”

“…We were also unable con dently to link outlier loci in either species with patterns of allele frequency change consistent with adaptive introgression. This may be partly due to the di culty of identifying outlier loci when there is strong population structure and relatively low gene ow between populations, as is the case for B. vittatum (Cummins et al, 2022;Johnson and Black, 2006), because it reduces the power of genome scans to detect 'outliers' (Beaumont and Nichols, 1996). The lack of associations between individual SNP loci and growth rate and the small number of annotated, assembled mollusc genomes further limited the conclusions we could draw from the data.…”

“…Bembicium vittatum was translocated outside its natural range of occurrence (Parsons, 1997) to Fremantle, Western Australia, resulting in multigenerational hybridisation with a native congener, B. auratum (Cummins et al, 2023). Initially, hybridisation following the translocation was unexpected due to differing modes of development between these sister species (Kennington et al, 2012), plus the occurrence of B. auratum and B. vittatum sympatrically elsewhere, with no evidence of hybridisation (Cummins et al, 2022;Johnson and Black, 2006;Reid, 1988). B. auratum develops indirectly, from egg to planktotrophic larva to adult (Anderson, 1962;Johnson and Black, 2006; Quoy and Gaimard, 1834), while B. vittatum is a direct developer, hatching from the egg as a crawling juvenile (Black et al, 1994;Johnson and Black, 2006;Philippi, 1846;Reid, 1988).…”