The genomic landscape of adaptation to a new host plant

Adaptation to novel ecological niches is known to be rapid. However, how the loci underlying ecological divergence are coupled to traits reproductively isolating populations, ultimately enabling the formation of persistent species, remains a consequential question in speciation research. Here, we investigated the genomic differences underpinning colonization of a new niche and formation of two partly sympatric host races of Tephritis conura peacock flies. We took advantage of two independent sympatric zones west and east of the Baltic Sea, where host plant specialists using the thistle species Cirsium heterophyllum and C. oleraceum co-occur, and address what regions of the genome maintain the host races in parallel. Using genome-wide association, differentiation and divergence statistics, we identified a large, highly divergent region associated with host use among western and eastern populations. Within this region, we identified unique haplotypes associated with each host race, indicative of a large inversion, adding to the growing body of evidence that structural changes to the genome are important for adaptations to persist in the face of gene flow. We further showed strong signatures of selection in this region, especially in populations of the derived C. oleraceum specialist host race. The region also had reduced introgression, especially in western populations, while the rest of the genome showed signs of extensive gene flow. Genes within highly differentiated windows within the putative inversion were not only enriched for functions involved in host adaptation, including phenology and metabolic responses to different metabolites in the two host plants, but also enriched for gametogenesis, fertilization and embryological development, all of which suggest sequence divergence could have large consequences on reproductive isolation between the host races. In conclusion, this study suggests that structural changes in the genome may facilitate the formation of persistent host races, and ultimately speciation, in face of gene flow.