Phenotypic divergence and genomic architecture at two different stages of speciation in a marine snail

Abstract

Speciation typically occurs in a time frame too long to be observed directly. This issue can be over-come by studying pairs of populations at different points in the speciation continuum, ideally within clades so that patterns are not confounded by differences among taxa. Such comparisons are possible in the marine snail Littorina saxatilis because it shows repeated occurrence of ecotypes adapted to either crab predation or wave action that differ in age and environmental context. Here, we explored transects spanning hybrid zones between the crab and wave ecotypes to contrast barriers to gene flow in Spain and Sweden, using low coverage whole genome sequencing, shell features, and behavioural traits. The two countries showed parallel divergence but distinct patterns of differentiation between the ecotypes: a continuous cline in Sweden but two highly genetically and phenotypically divergent, and partly spatially-overlapping clusters in Spain. Spanish early-generation hybrids were not observed but a low level of gene flow still seems to occur. In both countries, highly differentiated loci are clustered in genomic regions covered by chromosomal inversions but also occur in collinear regions. Despite being the same species and showing similar levels of phenotypic divergence, the Spanish ecotypes are closer to full reproductive isolation than the Swedish ecotypes. We discuss potential mechanisms contributing to the evolution of these different levels of reproductive isolation, particularly the age of the population, the strength of selection, the spatial context, and the role of assortative mating.

Chromosome-scale genome assembly of the rough periwinkleLittorina saxatilis

“…Across the species distribution, gene flow is occurring at different rates between the two ecotypes. In Sweden, allelic frequencies present a clinal pattern from crab to wave habitat (Westram et al 2021), while in Spain two distinct genetic clusters are found in upper and lower shore areas (Raffini et al 2023). This particular configuration enables the characterization of genomic, phenotypic, and organismal differences between pairs of populations from the same species at various stages of divergence, making L. saxatilis a most appropriate system to study the speciation process (Johannesson et al 2023).…”