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

Abstract

AbstractSpeciation 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 snailLittorina saxatilisbecause 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.