Genomic insights into the vulnerability of sympatric whitefish species flocks

The erosion of habitat heterogeneity can reduce species diversity directly but can also lead to the loss of distinctiveness of sympatric species through speciation reversal. We know little about changes in genomic differentiation during the early stages of these processes, which can be mediated by anthropogenic perturbation. Here, we analyse three sympatric whitefish species (Coregonus spp) sampled across two neighbouring and connected Swiss pre-alpine lakes, which have been differentially affected by anthropogenic eutrophication. Our data set comprises 16,173 loci genotyped across 138 whitefish using restriction-site associated DNA sequencing (RADseq). Our analysis suggests the differential decline of one of the two smaller deeper spawning species in each of the two lakes following a recent period of eutrophication and genomic signatures consistent with hybridisation between sympatric species being more pronounced in the more severely impacted lake. Comparisons between sympatric whitefish species pairs exhibiting similar ecological contrasts reveal genomic differentiation that is largely correlated along the genome, while a correlation is absent when comparing allopatric populations of the same or of ecologically similar species. We identify four genomic loci that provide evidence of parallel divergent adaptation between the shallow water species and two different deep spawning whitefish species. Functional annotations available for two of those loci support the role of ecological contrasts in shaping genomic differentiation. Our genomic analysis indicates the action of divergent natural selection shaping whitefish diversity in pre-alpine lakes and reveals the vulnerability of ecological speciation to anthropogenic alterations of the environment and associated adaptive landscape.