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.

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.

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Historic bias toward study of male sex hormones and sexual signals currently constrains our perspective of hormone-behavior-phenotype relationships. Resolving how ornamented female phenotypes evolve is particularly important for understanding the diversity of social signals across taxa. Studies of both males and females in taxa with variable female phenotypes are needed to establish whether sexes share mechanisms underlying expression of signaling phenotypes and behavior. White-shouldered Fairywren (Malurus alboscapulatus) subspecies vary in female ornamentation, baseline circulating androgens, and response to territorial intrusion. The moretoni ornamented female subspecies show higher female, but lower male androgens, and a stronger pair territorial response relative to pairs from the lorentzi unornamented female subspecies. Here we address whether subspecific differences in female ornamentation, baseline androgens, and pair territoriality are associated with ability to elevate androgens following gonadotropin releasing hormone (GnRH) challenge and in response to simulated territorial intrusion. We find that subspecies do not differ in their capacity to circulate androgens in either sex following GnRH or territorial intrusion challenges. Whereas pre-GnRH androgens were somewhat predictive of degree of response to territorial intrusions, higher androgens were associated with lower territorial aggression. Post-GnRH androgens were not predictive of response to simulated intruders, nor did females sampled during intrusion elevate androgens relative to flushed controls, suggesting that increased androgens are not necessary for the expression of territorial defense behaviors. Collectively, our results suggest that capacity to produce and circulate androgens does not underlie subspecific patterns of female ornamentation, territoriality, and baseline androgens.