Abstract
Carotenoid pigments produce most red, orange and yellow colours in vertebrates. This coloration can serve as an honest signal of quality that mediates social and mating interactions, but our understanding of the underlying mechanisms that control carotenoid signal production, including how different physiological pathways interact to shape and maintain these signals, remains incomplete. We investigated the role of testosterone in mediating gene expression associated with a red plumage sexual signal in red-backed fairywrens (Malurus melanocephalus). In this species, males within a single population can flexibly produce either red/black nuptial plumage or female-like brown plumage. Combining correlational analyses with a field-based testosterone implant experiment and quantitative polymerase chain reaction, we show that testosterone mediates expression of carotenoid-based plumage in part by regulating expression of CYP2J19, a ketolase gene associated with ketocarotenoid metabolism and pigmentation in birds. This is, to our knowledge, the first time that hormonal regulation of a specific genetic locus has been linked to carotenoid production in a natural context, revealing how endocrine mechanisms produce sexual signals that shape reproductive success.
Highlights
Carotenoid pigments, which provide many of the vivid red, orange and yellow colours observed in vertebrates, have long captured the attention of behavioural ecologists interested in the evolution of social signals
By combining field-based observational and experimental investigations with gene expression and biochemical analyses, we found that testosterone regulates gene expression implicated in the production of sexually selected red plumage in male red-backed fairywrens
Carotenoid metabolism is an endogenous process, and the ketolase enzyme encoded by CYP2J19 has previously been demonstrated to convert dietary carotenoids into red ketocarotenoids in birds [14,15]
Summary
Carotenoid pigments, which provide many of the vivid red, orange and yellow colours observed in vertebrates, have long captured the attention of behavioural ecologists interested in the evolution of social signals. Testosterone treatment of females can induce some red plumage coloration in normally brown females that would otherwise have low circulating androgens [60] Revealing how these endocrine processes may regulate gene expression associated with sexually selected carotenoid coloration has the potential to advance our understanding of the evolutionary origins and trajectories of carotenoid ornaments. We first use high-performance liquid chromatography (HPLC) to determine circulating carotenoid levels of ornamented red/black males, unornamented brown males, and females to identify the degree to which variation in metabolized ketocarotenoid circulation explains differences in carotenoid-based signal expression among these phenotypes. Implanted birds were recaptured 10–12 days post-implantation for liver sample collection, a time period that allowed for growth of pin feathers in the plucked plumage patches (red pins in testosterone-implanted males, and a mix of red and brown pins in the sham-implanted males, consistent with what had been observed in another feather-plucking study in this species [59]). We tested for statistical differences in liver CYP2J19 expression (log fold change) between phenotypes with an ANOVA, using the aov function in R, followed by a Tukey’s posthoc test using the Tukey HSD function in R
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