PAJOT-Basile/Evolving_inversions

Replicated local hybrid zones between ecotypes established over environmental gradients provide an opportunity to study the genomic architecture of local adaptation and barriers to gene flow. The marine snail Littorina fabalis segregates locally into a dwarf and a large ecotypes over wave exposure gradients in northwestern European shores. Previous work focusing on a local hybrid zone in Sweden revealed strong genetic differentiation between the ecotypes, concentrated in 12 putative chromosomal inversions. Here we compare the phenotypic and genetic composition of two hybrid zone, one from Sweden and one from France, both distributed over wave exposure gradients. Our aim is to investigate if similar genomic architectures (e.g., the same inversions) contribute to adaptation to parallel environmental gradients. Remarkably, we found that the shell size cline is reversed in France compared to in Sweden, with small individuals occupying the sheltered end of the environmental gradient in Sweden but the 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 at both sites. Most of the differences are clustered in 15 shared inversions that showed overlapping arrangement clines in both hybrid zones. In addition, these inversions showed a high number of private clines specific to one hybrid zone, and also reversed cline patterns between zones. Genome-wide association studies (GWAS) detected significant associations between genomic regions within inversions and shell size, but only in Sweden, while inversions and colour in France. These findings suggest that some site-specific phenotypic and genetic differences between ecotypes may be adaptive. Our results show that while the same inversions can be generally crucial to maintain ecotype differences and local adaptation, the content of the inversion arrangements can be shaped by local needs to enhance adaptive potential under site-specific environmental conditions.