Evolutionary trade-off between naturally- and sexually-selected melanin-based colour traits in worldwide barn owls and allies

Natural selection typically constrains the evolution of sexually-selected characters. The evolution of naturally- and sexually-selected traits can be intertwined if they share part of their genetic machinery or if sex traits impair foraging success or increase the risk of depredation. The present study investigated phenotypic correlations between naturally- and sexually-selected plumage traits in the Tytonidae (barn owls, grass owls, and masked owls). Phenotypic correlations indicate the extent to which selection on one trait will indirectly influence the evolution of another trait. In this group of birds, the ventral body side varies from white to dark reddish, a naturally- selected pheomelanin-based colour trait with important roles in predator-prey interactions. Owls also exhibit eumelanin-based black spots, for which number and size signal different aspects of individual quality and are used in mate choice. These three plumage traits are strongly heritable and sexually dimorphic, with females being on average darker reddish and more spotted than males. Phenotypic correlations were measured between these three plumage traits in 3958 free-living barn owls in Switzerland and 10 670 skin specimens from 34 Tyto taxa preserved in museums. Across Tyto taxa, the sexually-selected plumage spottiness was positively correlated with the naturally- selected reddish coloration, with redder birds being more heavily spotted. This suggests that they are genetically constrained or that natural and sexual selection are not antagonistically exerted on plumage traits. In a large sample of Swiss nestlings and within 34 Tyto taxa, the three plumage traits were positively correlated. The production of melanin pigments for one plumage trait is therefore not traded off against the production of melanin pigments for another plumage trait. Only in the most heavily-spotted Tyto taxa do larger-spotted individuals display fewer spots. This indicates that, at some threshold value, the evolution of many spots constrains the evolution of large spots. These analyses raise the possibility that different combinations of melanin-based plumage traits may not be selectively equivalent