The genomic signature of ecological divergence along the benthic-limnetic axis in allopatric and sympatric threespine stickleback.

Abstract

The repeated occurrence of similar phenotypes in independent lineages (i.e., parallel evolution) in response to similar ecological conditions can provide compelling insights into the process of adaptive evolution. An intriguing question is to what extent repeated phenotypic changes are underlain by repeated changes at the genomic level and whether patterns of genomic divergence differ with the geographic context in which populations evolve. Here, we combined genomic, morphological and ecological data sets to investigate the genomic signatures of divergence across populations of threespine stickleback (Gasterosteus aculeatus) that adapted to contrasting ecological niches (benthic or limnetic) in either sympatry or allopatry. We found that genome-wide differentiation (FST ) was an order of magnitude higher and substantially more repeatable for sympatric benthic and limnetic specialists compared to allopatric populations with similar levels of ecological divergence. We identified genomic regions consistently differentiated between sympatric ecotypes that were also differentiated between or associated with benthic vs. limnetic niche in allopatric populations. These candidate regions were enriched on three chromosomes known to be involved in the benthic-limnetic divergence of threespine stickleback. Some candidate regions overlapped with QTL for body shape and trophic traits such as gill raker number, traits that strongly differ between benthic and limnetic ecotypes. In summary, our study shows that magnitude and repeatability of genomic signatures of ecological divergence in threespine stickleback highly depend on the geographic context. The identified candidate regions provide starting points to identify functionally important genes for the adaptation to benthic and limnetic niches.