No 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.

The White-shouldered Fairywren (Malurus alboscapulatus) is a tropical passerine bird distributed across much of New Guinea. White-shouldered Fairywrens are among few species of fairywren with exclusively tropical distributions and differ from better studied congeners in Australia because subspecies vary by female, but not male, coloration and morphology. As with many bird species in New Guinea, basic demographic, social, morphological, and breeding data are limited. From 2011 to 2018 we documented the basic biology of two subspecies representing extremes of the female ornamentation spectrum. Both subspecies form groups having an even operational sex ratio and appear to breed year-round. Extra-pair paternity occurs in the subspecies with female ornamentation; comparable data are lacking for the subspecies having unornamented females, but the greater scaled cloacal protuberance volume of males suggests similar or higher extra-pair paternity rates. Females of the ornamented subspecies are generally larger than those lacking ornamentation, but exhibit reduced tail lengths, which is thought to serve as a signal of social dominance in other fairywrens. After first achieving adult-like plumage, males and ornamented females retain ornamented plumage year-round; however, only males in the subspecies with unornamented females appear to exhibit delayed plumage maturation. Our discussion highlights similarities and differences between White-shouldered Fairywren life histories and those of better studied Australian Malurus species; we focus on tropical vs. temperate environments and variable female ornamentation, and we identify priorities for future research.

We know little of the proximate mechanisms underlying the expression of signaling traits in female vertebrates. Across males, the expression of sexual and competitive traits, including ornamentation and aggressive behavior, is often mediated by testosterone. In the white-shouldered fairywren (Malurus alboscapulatus) of New Guinea, females of different subspecies differ in the presence or absence of white shoulder patches and melanic plumage, whereas males are uniformly ornamented. Previous work has shown that ornamented females circulate more testosterone and exhibit more territorial aggression than do unornamented females. We investigated the degree to which testosterone regulates the expression of ornamental plumage and territorial behavior by implanting free-living unornamented females with testosterone. Every testosterone-treated female produced a male-like cloacal protuberance, and 15 of 20 replaced experimentally plucked brown with white shoulder patch feathers but did not typically produce melanic plumage characteristic of ornamented females. Testosterone treatment did not elevate territorial behavior prior to the production of the plumage ornament or during the active life of the implant. However, females with experimentally induced ornamentation, but exhausted implants, increased the vocal components of territory defense relative to the pretreatment period and also to testosterone-implanted females that did not produce ornamentation. Our results suggest that testosterone induces partial acquisition of the ornamental female plumage phenotype and that ornament expression, rather than testosterone alone, results in elevations of some territorial behaviors.

Ornamentation, such as the showy plumage of birds, is widespread among female vertebrates, yet the evolutionary pressures shaping female ornamentation remain uncertain. In part this is due to a poor understanding of the mechanistic route to ornamentation in females. To address this issue, we evaluated the evolutionary history of ornament expression in a tropical passerine bird, the White-shouldered Fairywren, whose females, but not males, strongly vary between populations in occurrence of ornamented black-and-white plumage. We first use phylogenomic analysis to demonstrate that female ornamentation is derived and that female ornamentation evolves independently of changes in male plumage. We then use exogenous testosterone in a field experiment to induce partial ornamentation in naturally unornamented females. By sequencing the transcriptome of experimentally induced ornamented and natural feathers, we identify genes expressed during ornament production and evaluate the degree to which female ornamentation in this system is associated with elevated testosterone, as is common in males. We reveal that some ornamentation in females is linked to testosterone and that sexes differ in ornament-linked gene expression. Lastly, using genomic outlier analysis we identify a candidate melanogenesis gene that lies in a region of high genomic divergence among populations that is also differentially expressed in feather follicles of different female plumages. Taken together, these findings are consistent with sex-specific selection favoring the evolution of female ornaments and demonstrate a key role for testosterone in generating population divergence in female ornamentation through gene regulation. More broadly, our work highlights similarities and differences in how ornamentation evolves in the sexes.