Massive genome inversion drives coexistence of divergent morphs in common quails

• Published in: Current biology 2022-01, Vol.32 (2), p.462-469.e6
• Main Authors: Sanchez-Donoso, Ines, Ravagni, Sara, Rodríguez-Teijeiro, J. Domingo, Christmas, Matthew J., Huang, Yan, Maldonado-Linares, Andros, Puigcerver, Manel, Jiménez-Blasco, Irene, Andrade, Pedro, Gonçalves, David, Friis, Guillermo, Roig, Ignasi, Webster, Matthew T., Leonard, Jennifer A., Vilà, Carles
• Format: Article
• Language: English
• Subjects: Animals; chromosomal inversion; Chromosome Inversion; Coturnix - genetics; Coturnix coturnix; Female; Gene Flow; Genome; interbreeding; Male; migration; polymorphism; Seasons; stable isotopes; structural variation
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2021.11.019

The presence of population-specific phenotypes often reflects local adaptation or barriers to gene flow. The co-occurrence of phenotypic polymorphisms that are restricted within the range of a highly mobile species is more difficult to explain. An example of such polymorphisms is in the common quail Coturnix coturnix, a small migratory bird that moves widely during the breeding season in search of new mating opportunities, following ephemeral habitats,1,2 and whose females may lay successive clutches at different locations while migrating.3 In spite of this vagility, previous studies reported a higher frequency of heavier males with darker throat coloration in the southwest of the distribution (I. Jiménez-Blasco et al., 2015, Int. Union Game Biol., conference). We used population genomics and cytogenetics to explore the basis of this polymorphism and discovered a large inversion in the genome of the common quail. This inversion extends 115 Mbp in length and encompasses more than 7,000 genes (about 12% of the genome), producing two very different forms. Birds with the inversion are larger, have darker throat coloration and rounder wings, are inferred to have poorer flight efficiency, and are geographically restricted despite the high mobility of the species. Stable isotope analyses confirmed that birds carrying the inversion have shorter migratory distances or do not migrate. However, we found no evidence of pre- or post-zygotic isolation, indicating the two forms commonly interbreed and that the polymorphism remains locally restricted because of the effect on behavior. This illustrates a genomic mechanism underlying maintenance of geographically structured polymorphisms despite interbreeding with a lineage with high mobility. [Display omitted] •A chromosomal inversion of 115 Mbp, 12% of the genome, is found in common quails•Birds with the inversion are darker, heavier, and have rounder wings•These birds do not undertake the characteristic long-distance migration•The sequence in the inversion is highly divergent and originated before speciation Despite the extremely high mobility of common quail Coturnix coturnix, Sanchez-Donoso et al. identify a geographically restricted, very large chromosomal inversion in the darker, heavier common quail of the western edge of the species distribution. This inversion is also associated with reduced dispersal and migration.