How reproductive isolation barriers accumulate between nascent species remains a long-standing question in speciation research. Recently, chromosomal inversions have been proposed as strong candidates to generate barriers to gene flow due to their reduced recombination rate, which helps to maintain high linkage disequilibrium between arrangements and loci under divergent selection. However, little is still known about the complete evolutionary history of inversions, i.e., the determinants of their appearance within genomes and how selection, gene flux, mutation load, and recombination shape genetic divergence between arrangements.
In this seminar, I will present the origin and fates of chromosomal inversions and their impact on speciation in 166 whole-genome sequences of 8 different species of Littorina marine snails, whose 2 (L. saxatilis and L. fabalis) are split into different ecotypes that have different shell phenotypes, behavior, and habitat preferences. We first confirmed the presence of more than 30 polymorphic inversions longer than 1 megabase pair; most inversions separating ecotypes were found to be private to either L. fabalis or L. saxatilis. By combining Hi-C contact maps and synteny approaches, we found that chromosomal inversions are preferentially found in repeat-rich, gene-poor regions and nearby telomeres. Most inversions were found to be old, but we found no evidence that associative overdominance generating by the differential accumulation of deleterious mutation in both arrangements can explain their maintenance as polymorphism. Despite finding presence of gene flux between arrangements, we did not find elevated differentiation around inversion’s breakpoints (i.e., suspension bridge patterns) for most inversions, suggesting that gene flux is occurring mostly via gene conversion rather than double cross over. We argue that this is a powerful system to improve our understanding of the evolutionary history of chromosomal inversions and their role in the evolution of barriers to gene flow in multiple closely related species. Notably, it paves the way to understand how chromosomal inversions have shaped the divergence at a deeper timescale across species of the Littorina genus and to determine whether some polymorphic inversions might have a single origin between distant Littorina species and thus might be sieved to be re-used to accumulate barrier to gene flow in distant lineages.
