Inversions support both parallel and location-specific adaptations in snail ecotypes

Abstract

Replicated hybrid zones between ecotypes established over within shore environmental gradients provide an opportunity to study the genomic architecture of barriers to gene flow. The marine snail Littorina fabalis segregates locally into dwarf and large ecotypes over wave-exposure gradients on northwestern European shores. Previous work focusing on a hybrid zone in Sweden revealed strong genetic differentiation between the ecotypes, concentrated in 12 putative chromosomal inversions. Here we compare the Swedish hybrid zone with samples from France distributed across a similar wave-exposed gradient. Our aims were to test if similar exposure gradients promote parallel ecotype distributions and hybrid zones, and if similar genomic architectures contribute to divergence and adaptation across the gradients. Unpredictably, we found that the shell size cline was reversed in France compared to Sweden, with small individuals occupying the more-sheltered end of the environmental gradient in Sweden but the more-exposed end in France. We also observed a cline in shell colour in France, whereas nearly all Swedish snails were yellow. Using whole-genome sequencing, we found similar levels of genetic differentiation between ecotypes in both places. Most of the differences were accounted for by the same 15 inversions, and the arrangement clines showed similar associations to the wave-exposure gradient in both hybrid zones. These inversions were enriched in SNPs differentiating the ecotypes that were either specific to one hybrid zone or showed reversed cline patterns between zones. Genome-wide association studies (GWAS) detected significant associations between genomic regions within inversions and shell size in Sweden, while one inversion was associated with colour in France. Our results show that the same inversions play a dual role: they support ecotype differences across similar environmental gradients in distant locations, while also contribute site-specific variation contributing to local adaptation.