Elevated oxidative stress in pied flycatcher nestlings of eumelanic foster fathers under low rearing temperatures

Abstract

Striking variation in melanin coloration within natural populations is likely due to the different fitness outcomes of alternative phenotypes in varying environmental conditions. There are two types of melanin: eumelanins yield blackish hues, whereas pheomelanins yield reddish hues. The production of eumelanins requires low levels of glutathione (GSH), which is the most important intracellular antioxidant, whereas the production of pheomelanins requires high levels of GSH. We investigated the oxidative status of male pied flycatchers (Ficedula hypoleuca) with different degrees of melanin coloration under different temperatures during the nestling period. Moreover, we assessed the oxidative status of offspring in relation to their biological or foster father's melanin coloration and ambient temperature. To separate offspring genotype effects and paternal effects in different temperatures, we used a partial cross-foster design. The temperature differently affected the oxidative status of differently colored male pied flycatchers and their foster offspring. When the weather was relatively cold, black males had higher glutathione S-transferase levels compared with brown males, indicating enhanced stress in black males. Foster offspring of black males had a lower ratio between reduced and oxidized GSH followed by higher total amount of GSH than foster offspring of brown males. Thus, foster offspring of black males seem to suffer from oxidative stress under relatively cold weather compared with those of brown males, and vice versa under relatively warm weather. Although differently colored males experienced changes in their oxidative status under different temperatures, the link between paternal melanin coloration and offspring oxidative stress appears to be environmentally induced.

Pigment molecular composition reveals significant information for visual communication

“…The percentage of black feather colour (vs. grey colour) in the dorsal plumage of males was estimated by eye from 0% to 100% to the nearest 1% (Järvistö et al, 2015; Figure 1). The repeatability of this estimation has been reported as high ( r = 0.88, F 1,33 = 24.96, p < 0.001) on the basis of assessments made by two different observers (Teerikorpi et al, 2019). Among the 51 males included in this study, dorsal plumage blackness ranged from 5 to 99% (mean = 59.3%, SD = 33.7%; Figure 1).…”

“…Although the eumelanin DHICA:DHI ratio predicted plumage blackness variation in males, the correlation coefficient (0.36) indicated that a high proportion of variance remains unexplained. This may be the reason why different studies have not found clear associations between plumage blackness and oxidative stress markers in male pied flycatchers (López‐Arrabé et al, 2014; Moreno et al, 2011; Teerikorpi et al, 2019) and other species with eumelanin‐based mating signals (Henschen et al, 2018), as the eumelanin DHICA:DHI ratio of black feathers may be a trait that more directly reveals the physiological status of birds.…”

“…However, the signalling function of this trait, that is why females preferentially mate with blacker male pied flycatchers, is unknown. In fact, associations between dorsal plumage blackness and systemic markers of oxidative stress and damage have been shown to be absent (López‐Arrabé et al, 2014; Moreno et al, 2011) or dependent on environmental factors such as temperature (Teerikorpi et al, 2019), which makes their interpretation difficult.…”

Adaptive coloration in pied flycatchers (Ficedula hypoleuca)—The devil is in the detail

“…It has been shown experimentally that it is the melanin coloration of the foster parent and not the genetic parent that matters during the rearing period (Järvistö, 2015). Further, it has been shown that foster offspring of black males seem to suffer from oxidative stress under relatively cold weather compared with those of brown males (Teerikorpi et al., 2019). Taken together, these results show that temperature‐dependent variation in reproductive success mainly is explained by differences in parental behaviors, which in turn are associated with variation in melanin coloration (Järvistö, 2015; Sirkiä et al., 2010; Teerikorpi et al., 2019).…”

“…Further, it has been shown that foster offspring of black males seem to suffer from oxidative stress under relatively cold weather compared with those of brown males (Teerikorpi et al., 2019). Taken together, these results show that temperature‐dependent variation in reproductive success mainly is explained by differences in parental behaviors, which in turn are associated with variation in melanin coloration (Järvistö, 2015; Sirkiä et al., 2010; Teerikorpi et al., 2019). These findings are compatible with the idea of pleiotropic effects of genes regulating the synthesis of melanins being the key links between climatic adaptations and eumelanin‐based plumage coloration (Roulin, 2004).…”