Predation risk determines pigmentation phenotype in nuthatches by melanin‐related gene expression effects

Abstract

Pigments determine the appearance of organisms. However, pigment production can be associated with physiological constraints as in the case of pheomelanin, the sulphurated form of melanin whose synthesis in melanocytes consumes cysteine and consequently reduces the availability of glutathione (GSH) to exert antioxidant protection. Pheomelanogenesis may thus increase the susceptibility to suffer chronic oxidative stress. I investigated the possibility that environmental lability in the expression of genes regulating pheomelanogenesis protects from oxidative stress, a situation in which GSH is most required. By broadcasting adult alarm calls, I manipulated the perception of predation risk, a natural source of oxidative stress, in free‐living Eurasian nuthatch Sitta europaea nestlings developing pheomelanin‐pigmented flank feathers. The manipulation affected the consumption of GSH that resulted from the expression of two genes (Slc7a11 and Slc45a2) influencing cysteine/GSH availability in cells, as these genes were down‐regulated in the feather melanocytes of the nestlings with lowest intracellular antioxidant capacity (i.e. lowest GSH levels). Systemic oxidative damage increased with Slc7a11 expression in feather melanocytes, suggesting that the observed down‐regulation was physiologically advantageous. The nestlings exposed to an increased perception of predation risk developed flank feathers of reduced colour intensity. These results indicate that perceived predation risk can determine the pigmentation phenotype by (probably epigenetic) effects on gene expression that protect from physiological constraints imposed by pheomelanin production.

Exposure to a competitive social environment activates an epigenetic mechanism that limits pheomelanin synthesis in zebra finches

“…This indeed resulted in a decrease in the intensity of pheomelanin-based plumage coloration (Galván, 2018). The present study confirms those results and shows that Slc7a11 downregulation also occurs as a response to another natural source of stress: a competitive social environment.…”

“…Consequently, Slc7a11 expression also affects cellular oxidative stress, as cysteine consumed during pheomelanin synthesis is no longer available for antioxidant protection as a constituent of GSH (Pavel, Smit, & Pizinger, ). Slc7a11 downregulation in melanocytes of growing feathers has previously been observed in male zebra finches exposed to an exogenous pro‐oxidant substance (Galván, Moraleda, Otero, Álvarez, & Inácio, ) and in the Eurasian nuthatch ( Sitta europaea ) exposed to a natural source of environmental stress (predation risk; Galván, ). This indeed resulted in a decrease in the intensity of pheomelanin‐based plumage coloration (Galván, ).…”

“…Slc7a11 downregulation in melanocytes of growing feathers has previously been observed in male zebra finches exposed to an exogenous pro‐oxidant substance (Galván, Moraleda, Otero, Álvarez, & Inácio, ) and in the Eurasian nuthatch ( Sitta europaea ) exposed to a natural source of environmental stress (predation risk; Galván, ). This indeed resulted in a decrease in the intensity of pheomelanin‐based plumage coloration (Galván, ). The present study confirms those results and shows that Slc7a11 downregulation also occurs as a response to another natural source of stress: a competitive social environment.…”

“…Values before (initial) and after (final) experimental treatments are shown. Higher ΔC t final values for males housed in groups indicate lower gene expression ( 2 1 = 5.749; p = .016) ∆ observed in male zebra finches exposed to an exogenous pro-oxidant substance (Galván, Moraleda, Otero, Álvarez, & Inácio, 2017) and in the Eurasian nuthatch (Sitta europaea) exposed to a natural source of environmental stress (predation risk; Galván, 2018).…”

“…The underlying mechanisms may be represented by changes in DNA methylation (Champagne, 2010;Weaver et al, 2004;Zhang & Meaney, 2010), as oxidative stress modulates the activity of enzymes responsible for DNA demethylation (Niu, DesMarais, Tong, Yao, & Costa, 2015). As changes in DNA methylation can be influenced by the social context and hormone levels (Dhiman, Attwood, Campbell, & Smiraglia, 2015;Weaver et al, 2004), a similar adaptive response to that observed in response to predation risk (Galván, 2018) could be expected from competitive environments that promote high testosterone levels and increase the susceptibility to oxidative stress.…”