The expression of melanin-based plumage is separately modulated by exogenous oxidative stress and a melanocortin

Abstract

Melanin-based traits involved in animal communication have been traditionally viewed as occurring under strict genetic control. However, it is generally accepted that both genetic and environmental factors influence melanin production. Medical studies suggest that, among environmental factors influencing melanization, oxidative stress could play a relevant role. On the other hand, genetic control would be exerted by the melanocortin system, and particularly by the alpha-melanocyte-stimulating hormone (a-MSH), which triggers the production of eumelanins (black pigments). To determine how the melanocortin system and an exogenous source of oxidative stress interact in the expression of melanin-based plumage, developing red-legged partridges (Alectoris rufa) were manipulated. Some partridges were injected with a-MSH, while other birds received a pro-oxidant molecule (diquat) in drinking water. Controls and birds receiving both treatments were also studied. Both a-MSH-and diquat-treated individuals presented larger eumelanin-based traits than controls, but a-MSHþdiquat-treated birds showed the largest traits, suggesting that oxidative stress and melanocortins promote additive but independent effects. Diquat also induced a decline in the level of a key intracellular antioxidant (glutathione), which is associated with high expression of eumelanin-based signals in other bird species. Some scenarios for the evolution of melanin-based traits in relation to oxidative stress are proposed.

The Level of an Intracellular Antioxidant during Development Determines the Adult Phenotype in a Bird Species: A Potential Organizer Role for Glutathione

“…Among them, the subject of the study was related to the present work in only two cases. In Galván and Alonso-Alvarez (2008), wild nestling great tits injected with similar BSO amounts showed higher, rather than lower, PLAOX values than controls. The disagreement in results could be explained by interactions with factors differing between studies, such as environmental conditions (captive vs. wild), dietary antioxidant levels, or phylogenetic distance (different species).…”

“…To our knowledge, only four avian studies have used BSO and effectively decreased tGSH values (Galvani et al 1998;Marchionatti et al 2001;Galván and Alonso-Alvarez 2008;Horak et al 2010). Among them, the subject of the study was related to the present work in only two cases.…”

Female plumage colour influences seasonal oxidative damage and testosterone profiles in a songbird

“…Existing hypotheses to explain signal-physiology links focus predominantly on consistent individual differences in physiology or phenotypic condition that constrain the development or display of signal traits [2][3][4]. For example, melanin-based traits like the ventral plumage of barn swallows have been proposed to signal resistance to oxidative stress though several mechanisms, including the direct suppression of melanization by oxidative stress, or an allocation trade-off between antioxidant defence and signal development [14,15,19]. While our results support the role of melanin-based plumage as a reliable indicator of susceptibility to oxidative stress [2,20], they implicate an alternative driver of this relationship: the display of darker plumage resulted in a decrease in both ROMs and testosterone during the breeding season.…”

“…In Hirundo rustica erythrogaster, birds of both sexes with darker melanin-based ventral colour have higher reproductive success independent of age [10], and experimentally darkened males gain more paternity [11]. Although melanin-based plumage has a strong heritable component [12], its elaboration can also be influenced by social status and physiological state during moult, including circulating testosterone and oxidative stress [13][14][15].…”

Yolk testosterone shapes the expression of a melanin-based signal in great tits: an antioxidant-mediated mechanism?

“…However, environmental factors such as the availability of certain metals and melanin precursors seem to affect melanin production (McGraw, 2008). Recently, exogenous oxidative stress has been highlighted as an important factor modulating plumage melanization (Galván and Alonso-Alvarez, 2009). Moreover, melanin synthesis (Slominski et al, 2004) is regulated by a number of different hormones that could potentially be sensitive to environmental influences.…”