The genetic basis of color-related local adaptation in a ring-like colonization around the Mediterranean

Abstract

Uncovering the genetic basis of phenotypic variation and the population history under which it established is key to understand the trajectories along which local adaptation evolves. Here, we investigated the genetic basis and evolutionary history of a clinal plumage color polymorphism in European barn owls (Tyto alba). Our results suggest that barn owls colonized the Western Palearctic in a ring-like manner around the Mediterranean and meet in secondary contact in Greece. Rufous coloration appears to be linked to a recently evolved nonsynonymous-derived variant of the melanocortin 1 receptor (MC1R) gene, which according to quantitative genetic analyses evolved under local adaptation during or following the colonization of Central Europe. Admixture patterns and linkage disequilibrium between the neutral genetic background and color found exclusively within the secondary contact zone suggest limited introgression at secondary contact. These results from a system reminiscent of ring species provide a striking example of how local adaptation can evolve from derived genetic variation.

Beyond mean allelic effects: A locus at the major color geneMC1Rassociates also with differing levels of phenotypic and genetic (co)variance for coloration in barn owls

“…S1). This is congruent with previous findings suggesting a lack of genetic structure in relation to plumage coloration in European barn owls (Burri et al 2016) and a low proportion of assortative pairing in relation to the MC1R (about 9%, Ducret et al 2016). Coincident with a higher variance, measurements of plumage coloration in MC1R WW and MC1R RW were significantly less repeatable than in MC1R RR individuals.…”

“…Here, we showed that a MC1R locus affecting coloration in the barn owl (San-Jose et al 2015;Burri et al 2016) and other bird species (Johnson et al 2012;Zhan et al 2012;Yu et al 2013) is also associated with substantial differences in the variance of three plumage traits: plumage rufous coloration and the number and size of ventral black spots. As a general trend, the rufous MC1R allele was associated with lower variance for plumage coloration, and spot number and size.…”

“…Although less parsimonious, this scenario is possible given that the rufous allele seems to derive from the white allele (Burri et al 2016), and has expanded through Europe favored by natural selection (Antoniazza et al 2010(Antoniazza et al , 2014. In such a scenario, we would expect these putative sites to be less polymorphic when co-occurring with the rufous allele to explain the lower variance associated with this allele.…”

“…This might have reduced genetic variation in the vicinity of the MC1R rufous allele owing to the hitchhiking effect of selection on the rufous allele, which has been observed in the MC1R of two populations of lizard species that evolved blanched colorations to adapt to the light soil of the White Sands ecosystem of New Mexico (Laurent et al 2016). The fact that the barn owl colonized Europe after the last glaciation (ß20,000 years before present; Antoniazza et al 2014) and that there exists substantial gene flow between color forms in Europe (Antoniazza et al 2010;Burri et al 2016) renders this assumption unlikely in our opinion, but specific studies to accurately date the origin of the rufous allele would still be needed to better assess the likelihood of this scenario. This scenario also assumes that there has not been enough time for recombination to erase the effect of hitchhiking, which would have homogenized the genetic backgrounds in the surroundings of the white and rufous alleles (e.g., Domingues et al 2012).…”

“…Color traits are highly heritable in the barn owl (plumage coloration: 0.84 ± 0.02, spot size: 0.67 ± 0.02, and spot number: 0.57 ± 0.03) and moderate to strongly genetically correlated (between 0.2 ± 0.04 and 0.93 ± 0.04: Roulin and Jensen 2015). Homozygotes for the valine allele (hereafter referred to as the white allele) have whiter plumage coloration, homozygotes for the isoleucine allele (hereafter referred to as the rufous allele) have a rufous plumage coloration, and heterozygotes exhibit an intermediate phenotype (San-Jose et al 2015;Burri et al 2016). Homozygotes for the valine allele (hereafter referred to as the white allele) have whiter plumage coloration, homozygotes for the isoleucine allele (hereafter referred to as the rufous allele) have a rufous plumage coloration, and heterozygotes exhibit an intermediate phenotype (San-Jose et al 2015;Burri et al 2016).…”