The genomic landscape of adaptation to a new host plant

Abstract

AbstractAdaptation to novel ecological niches is known to be rapid. However, how ecological divergence translates into reproductive isolation remains a consequential question in speciation research. It is still unclear how coupling of ecological divergence loci and reproductive isolation loci occurs at the genomic level, ultimately enabling the formation of persistent species. Here, we investigate the genomic underpinning colonization of a new niche and formation of two host races inTephritis conurapeacock flies that persist in sympatry. To uncover the genomic differences underlying host plant adaptation, we take advantage of two independent sympatric zones, where host plant specialists using the thistle speciesCirsium heterophyllumandC. oleraceumco-occur, and address what regions of the genome that diverge between the host races in a parallel fashion. Using Population Branch Statistics, dxy and BayPass we identify 2996 and 3107 outlier regions associated with host use among western and eastern Baltic populations, respectively, with 82% overlap. The majority of outliers are located within putative inversions, adding to the growing body of evidence that structural changes to the genome are important for adaptations to persist in face of gene flow. Potentially, the high contents of repetitive elements could have given rise to the inversions, but this remains to be tested. The outlier regions were enriched for genes involved in e.g. metabolism and morphogenesis, potentially due to the selection for processing different metabolites, and changes in size and ovipositor length respectively. In conclusion, this study suggests that structural changes in the genome, and divergence in independent ecological functions may facilitate the formation of persistent host races in face of gene flow.