A complex copy number variant underlies differences in both colour plumage and cold adaptation in a dimorphic seabird

Abstract

SUMMARYColour morphs associated with different physiological adaptations offer unique opportunities to study the genomic basis of otherwise elusive adaptive traits. These complex balanced polymorphisms are often controlled by groups of tightly linked genes, and understanding how these ‘supergenes’ evolve and are maintained is an active area of research in evolutionary biology (Schwander et al. 2014, Thompson and Jiggins 2014). Within the Atlantic, the common murre (Uria aalge, a colonial seabird) displays a plumage colour dimorphism (‘bridled’ and ‘unbridled’) that seems to be associated with differences in thermal adaptation (Birkhead 1984; Reiertsen et al. 2012). The genes associated with bridling and how these genes affect thermal adaptation are unknown. Using whole genome resequencing, we investigate the genomic basis of differences in colouration and thermal adaptation between the two morphs, and how the association between the two traits is maintained despite random mating. We identify a 60 kb genomic region of high differentiation laying in the intergenic area amongst three candidate genes for colouration and thermal adaptation: retinoic acid receptor beta (RARB), thyroid hormone receptor beta (THRB), and nuclear receptor subfamily 1 group D member 2 (NR1D2 or Rev-erbβ). Differentiation is due to a complex copy number variant (CNV) that suppresses recombination locally. We show that this CNV acts as a ‘supergene’ and maintain association between regulatory elements likely affecting gene expression of one or more of the identified candidate genes. Our analyses also provide insights into the origin of the dimorphism: while copy number proliferation in the unbridled haplotype was potentially mediated by transposable elements (TEs), the bridled haplotype seems to have introgressed from the more cold-adapted sister species, the thick-billed murre (U. lomvia). Our results highlight the role of copy number variants in adaptation, especially when association among traits is maintained in the face of gene flow. They also shed light into the molecular mechanisms of adaptive thermogenesis in birds, which is poorly understood.HighlightsDifferences in plumage colour in Atlantic common murres are associated with different thermal adaptationsA single region is highly differentiated between bridled and unbridled morphsA complex copy number variant in a non-coding region underlies the dimorphismTransposable elements and adaptive introgression from the thick-billed murre seem to explain the origin of the dimorphism