Sex‐specific allelic transmission bias suggests sexual conflict at MC1R

Abstract

Sexual conflict arises when selection in one sex causes the displacement of the other sex from its phenotypic optimum, leading to an inevitable tension within the genome - called intralocus sexual conflict. Although the autosomal melanocortin-1-receptor gene (MC1R) can generate colour variation in sexually dichromatic species, most previous studies have not considered the possibility that MC1R may be subject to sexual conflict. In the barn owl (Tyto alba), the allele MC1RWHITE is associated with whitish plumage coloration, typical of males, and the allele MC1RRUFOUS is associated with dark rufous coloration, typical of females, although each sex can express any phenotype. Because each colour variant is adapted to specific environmental conditions, the allele MC1RWHITE may be more strongly selected in males and the allele MC1RRUFOUS in females. We therefore investigated whether MC1R genotypes are in excess or deficit in male and female fledglings compared with the expected Hardy-Weinberg proportions. Our results show an overall deficit of 7.5% in the proportion of heterozygotes in males and of 12.9% in females. In males, interannual variation in assortative pairing with respect to MC1R explained the year-specific deviations from Hardy-Weinberg proportions, whereas in females, the deficit was better explained by the interannual variation in the probability of inheriting the MC1RWHITE or MC1RRUFOUS allele. Additionally, we observed that sons inherit the MC1RRUFOUS allele from their fathers on average slightly less often than expected under the first Mendelian law. Transmission ratio distortion may be adaptive in this sexually dichromatic species if males and females are, respectively, selected to display white and rufous plumages.

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.…”

“…Thus, differences between genotypes were not the spurious result of population stratification associated to variation at the MC1R, for instance, owing to MC1R alleles representing different admixed populations, or driving assortative pairing (Hernández-Sánchez et al 2003;Gratten et al 2008). 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). Given the results discussed above, we argue that the encountered variance differences are more likely to arise through an interaction between the MC1R genotypes with other loci and/or the environment.…”

“…The analyses were based on a wild social pedigree built using paternities assessed from field behavioral observations of parental care (Pemberton 2008, see Supporting Information). The extra-pair paternity rate is exceptionally low in the barn owl (about 1%, Henry et al 2013, see also Ducret et al 2016) and biases in model estimates owing to missassigned paternities are expected to be negligible (Charmantier and Réale 2005). The full pedigree consisted of 7705 individuals (of which 1202 were breeding adults with unknown ancestors and considered as founders in the pedigree).…”

MC1R variants affect the expression of melanocortin and melanogenic genes and the association between melanocortin genes and coloration

“…It is surprising that between‐genotypes differences in ASIP expression could arise from population stratification associated with MC1R genotypes, given that assortative pairing with respect to MC1R genotype is rare (Ducret et al . ) and the absence of genetic differentiation between MC1R genotypes in the barn owl (L.M. San‐Jose, unpublished data; Burri et al .…”

“…2) may occur because MC1R activity (expected to be higher in this group) can promote the transactivation of the MC1R gene through a positive feedback loop via MITF (Aoki & Moro 2002). It is surprising that between-genotypes differences in ASIP expression could arise from population stratification associated with MC1R genotypes, given that assortative pairing with respect to MC1R genotype is rare (Ducret et al 2016) and the absence of genetic differentiation between MC1R genotypes in the barn owl (L.M. San-Jose, unpublished data; Burri et al 2016).…”