Condition-dependence of pheomelanin-based coloration in nuthatches Sitta europaea suggests a detoxifying function: implications for the evolution of juvenile plumage patterns

Galván, Ismael

doi:10.1038/s41598-017-09771-4

Cited by 19 publications

(37 citation statements)

References 45 publications

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“…This is particularly relevant for species showing sexual dichromatism, which often plays a role in gender‐biased sexual selection (Heinsohn et al ., ). In my population, adult male nuthatches with flank feathers of low colour intensity achieve a higher mating success than males with more intense flank feather colour, probably because nestlings in poor body condition develop feathers of more intense colour (Galván, ). Thus, males that experienced good conditions early in life may be preferred by females during adulthood if colour expression was correlated across years as birds age (i.e.…”

Section: Discussionmentioning

confidence: 99%

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

Galván

2018

J of Evolutionary Biology

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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.

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Section: Discussionmentioning

confidence: 99%

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

Galván

2018

J of Evolutionary Biology

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“…When pheomelanin is synthesized, this may constrain physiological performance because it consumes glutathione (GSH), which is the most important intracellular antioxidant (Panzella et al 2014). On the other hand, melanin pheomelanin production may help remove excess cysteine, which is toxic (Galván 2017). The predominance of pheomelanin in the plumage of female birds in the Western Palearctic may respond to sex-biased physiologies in these species, and comparative studies with melanized but monomorphic species is therefore warranted.…”

Section: Discussionmentioning

confidence: 99%

Melanin‐based sexual dichromatism in the Western Palearctic avifauna implies darker males and lighter females

Negro

Figueroa-Luque

Galván

2018

Journal of Avian Biology

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Melanins are the most common pigments providing coloration in the plumage and bare skin of birds and other vertebrates. Numerous species are dichromatic in the adult or definitive plumage, but the direction of this type of sexual dichromatism (i.e. whether one sex tends to be darker than the other) has not been thoroughly investigated. Using color plates, we analysed the presence of melanin‐based color patches in 666 species belonging to 69 families regularly breeding in the Western Palearctic. Sexual dichromatism based on melanins in at least one integumentary part involved 205 (30.7%) species. The body parts contributing more frequently to dichromatism were the dorsal areas, head and breast, whereas the less dichromatic body parts were the belly and the exposed integumentary parts (i.e. bill and legs). Regarding the phylogenetic spread of dichromatisms, 37 (53.6%) families contained at least one species with melanin‐based sexual dimorphism in the definitive adult plumage. As for the direction of the color difference, males are darker than females in a majority of species, meaning that males tend to produce more eumelanin and females tend to synthesize more pheomelanin. This survey has revealed the high prevalence of melanins in the emergence of sexual dichromatism in birds, at least in the Western Palearctic. Whether the described pattern is due to sexual selection promoting more conspicuous males or to natural selection for more cryptic females remains to be determined. Given that pheomelanin synthesis concurrently consumes the antioxidant glutathione but may also reduces toxic cysteine, sex‐biased physiological factors should also be given consideration in the evolution of bird plumages.

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“…On the other hand, we investigated the effect of the experimental treatment on the physical, body condition of nuthatch nestlings, a predictor of survival prospects in the species (Matthysen, ). For this, we used body mass corrected by (i.e., independent of) body size, as this measure is a good indicator of subcutaneous fat content in nuthatches and other birds (Galván, ). This was analysed by linear mixed‐effects models with body mass as a response variable and tarsus length as a covariate (see Section 2.11).…”

Section: Methodsmentioning

confidence: 99%

“…If such a function is physiologically advantageous, we hypothesize that melanocytes would favour pheomelanin synthesis under an increase in cysteine availability. Here we investigate this possibility by experimentally increasing the dietary uptake of cysteine to developing Eurasian nuthatches Sitta europaea , a passerine bird that deposits large amounts of pheomelanin in flank feathers (Galván, ). Specifically, we tested if melanocytes from growing pheomelanin‐pigmented feathers show epigenetic lability and respond to the increase in cysteine availability by favouring pheomelanin synthesis.…”

Section: Introductionmentioning

confidence: 99%

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confidence: 99%

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Changes in melanocyte RNA and DNA methylation favour pheomelanin synthesis and may avoid systemic oxidative stress after dietary cysteine supplementation in birds

et al. 2019

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Cysteine plays essential biological roles, but excessive amounts produce cellular oxidative stress. Cysteine metabolism is mainly mediated by the enzymes cysteine dioxygenase and γ‐glutamylcysteine synthetase, respectively coded by the genes CDO1 and GCLC. Here we test a new hypothesis posing that the synthesis of the pigment pheomelanin also contributes to cysteine homeostasis in melanocytes, where cysteine can enter the pheomelanogenesis pathway. We conducted an experiment with the Eurasian nuthatch Sitta europaea, a bird producing large amounts of pheomelanin for feather pigmentation, to investigate if melanocytes show epigenetic lability under exposure to excess cysteine. We increased systemic cysteine levels in nuthatches by supplementing them with dietary cysteine during growth. In feather melanocytes this led to the downregulation of genes involved in intracellular cysteine metabolism (GCLC), cysteine transport to the cytosol from the extracellular medium (Slc7a11) and from melanosomes (CTNS), and regulation of tyrosinase activity (MC1R and ASIP). These changes were mediated by increases in DNA m5C in all genes except Slc7a11, which experienced RNA m6A depletion. Birds supplemented with cysteine synthesized more pheomelanin than controls, but did not suffer higher systemic oxidative stress. These results suggest that excess cysteine activates an epigenetic mechanism that favours pheomelanin synthesis and may protect against oxidative stress.

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Condition-dependence of pheomelanin-based coloration in nuthatches Sitta europaea suggests a detoxifying function: implications for the evolution of juvenile plumage patterns

Cited by 19 publications

References 45 publications

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

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

Melanin‐based sexual dichromatism in the Western Palearctic avifauna implies darker males and lighter females

Changes in melanocyte RNA and DNA methylation favour pheomelanin synthesis and may avoid systemic oxidative stress after dietary cysteine supplementation in birds

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