Pleiotropy in the melanocortin system: expression levels of this system are associated with melanogenesis and pigmentation in the tawny owl (Strix aluco)

Abstract

The adaptive function of melanin-based coloration is a long-standing debate. A recent genetic model suggested that pleiotropy could account for covariations between pigmentation, behaviour, morphology, physiology and life history traits. We explored whether the expression levels of genes belonging to the melanocortin system (MC1R, POMC, PC1/3, PC2 and the antagonist ASIP), which have many pleiotropic effects, are associated with melanogenesis (through variation in the expression of the genes MITF, SLC7A11, TYR, TYRP1) and in turn melanin-based coloration. We considered the tawny owl (Strix aluco) because individuals vary continuously from light to dark reddish, and thus, colour variation is likely to stem from differences in the levels of gene expression. We measured gene expression in feather bases collected in nestlings at the time of melanin production. As expected, the melanocortin system was associated with the expression of melanogenic genes and pigmentation. Offspring of darker reddish fathers expressed PC1/3 to lower levels but tended to express PC2 to higher levels. The convertase enzyme PC1/3 cleaves the POMC prohormone to obtain ACTH, while the convertase enzyme PC2 cleaves ACTH to produce α-melanin-stimulating hormone (α-MSH). ACTH regulates glucocorticoids, hormones that modulate stress responses, while α-MSH induces eumelanogenesis. We therefore conclude that the melanocortin system, through the convertase enzymes PC1/3 and PC2, may account for part of the interindividual variation in melanin-based coloration in nestling tawny owls. Pleiotropy may thus account for the covariation between phenotypic traits involved in social interactions (here pigmentation) and life history, morphology, behaviour and physiology.

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

“…Consequently, the association between colour traits and the melanocortin system, as shown in several species (Emaresi et al . ; Monti et al . ; Ducrest et al .…”

Sex- and melanic-specific variations in the oxidative status of adult tawny owls in response to manipulated reproductive effort

“…Secondly, tawny owls show continuous variation in melaninbased plumage coloration (from light to dark reddish; for pictures, see Da Silva et al, 2013), the expression of which is strongly genetically controlled and not sensitive, or only weakly so, to environmental conditions (Brommer et al, 2005;Gasparini et al, 2009;Emaresi et al, 2013). Interestingly, differently coloured adult males display alternative trade-off resolution and life histories (Emaresi et al, , 2014.…”

Plumage colour and the expression of stress‐related genes in gull chicks

“…Interestingly, the feather melanic colouration was associated with sex, irrespective of the egg laying order. Sex‐related genetic factors may influence the different regulation, expression or deposition of melanins between males and females (Emaresi et al , San‐Jose et al , ). In birds, embryos show sex‐specific development with contrasting physiological machinery (Balthazart and Adkins‐Regan ), as revealed by sex‐biased gene expression (Mank et al ), organ development (Nielsen and Torday ) and survival (Pérez et al ) in avian embryos.…”