Male White-shouldered Fairywrens (Malurus alboscapulatus) elevate androgens greater when courting females than during territorial challenges

Boersma, Jordan; Jones, John Anthony; Enbody, Erik D; Welklin, Joseph F.; Ketaloya, Serena; Nason, Doka; Karubian, Jordan; Schwabl, Hubert

doi:10.1016/j.yhbeh.2022.105158

Cited by 10 publications

(15 citation statements)

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“…Populations of White-shouldered Fairywrens with ornamented females, compared to the population with unornamented females, have higher circulating levels of androgens (i.e., testosterone) in females, and the phenotype is associated with greater territorial aggression (Enbody et al 2018;Boersma et al 2020). Importantly, in both populations studied to date, males have much higher androgen levels than do females, and males in the brown population tend to have the highest circulating androgens (Boersma et al 2022), suggesting female androgen levels do not covary with male levels (Enbody et al 2018). Together, variation in territorial behavior among female phenotypes is consistent with the hypothesis that female ornamentation is subject to social selection, as has been hypothesized for females elsewhere (West-Eberhard 1983;Tobias et al 2012), and that androgens (testosterone) are part of the mechanism of the expression of the ornament and its integration with behavior (Boersma et al 2020).…”

Section: Discussionmentioning

confidence: 95%

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The evolutionary history and mechanistic basis of female ornamentation in a tropical songbird

et al. 2022

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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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Section: Discussionmentioning

confidence: 95%

“…Importantly, in both populations studied to date, males have much higher androgen levels than do females, and males in the brown population tend to have the highest circulating androgens (Boersma et al. 2022), suggesting female androgen levels do not covary with male levels (Enbody et al. 2018).…”

Section: Discussionmentioning

confidence: 99%

The evolutionary history and mechanistic basis of female ornamentation in a tropical songbird

et al. 2022

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“…We used this approach to test whether null comparisons across groups were indicative of no meaningful difference in androgens rather than a constraint of small sample sizes obscuring our ability to detect differences. For GnRH-induced androgens we set equivalence bounds according to mean differences across subspecies previously measured in females (Enbody et al, 2018) and males (Boersma et al, 2022a). For simulated territorial intrusion versus flushed androgen sampling comparison in females, we used the previously measured mean difference in males across these same sampling contexts as equivalence bounds (Boersma et al, 2022a).…”

Section: Methodsmentioning

confidence: 99%

“…In the current study, we use GnRH and simulated territorial intrusion challenges to assess whether varying capacity to produce and circulate androgens underlies subspecific variation in female ornamentation, territorial behavior, and baseline androgens. In conjunction with a recent study of male androgens (Boersma et al, 2022a), we also test whether simulated territorial intrusions cause females to elevate androgens relative to flushed controls ("challenge hypothesis" in females; Wingfield et al,1990).…”

Section: Introductionmentioning

confidence: 99%

Does capacity to elevate androgens underlie variation in female ornamentation and territoriality in White-shouldered Fairywren (Malurus alboscapulatus)?

Boersma¹,

Enbody

Ketaloya

et al. 2023

Preprint

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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.

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“…Hormones mediate expression of many morphological and behavioral traits (Ketterson and Nolan 1999, Kaiser et al 2014, Lipshutz et al 2019, and can change rapidly in response to changes in the abiotic (Breuner and Hahn 2003, Lynn et al 2003, Gill et al 2008, Hau et al 2008b, Wingfield et al 2017, Boersma et al 2021) and social environment (Wingfield et al 1990, Goymann et al 2004, Goymann 2009, Boersma et al 2022. Gonadal steroid hormones, such as the androgen testosterone and its metabolites (i.e., estradiol), can mediate transitions between life-history stages (Cawthorn et al 1998, Pärn et al 2008, Wingfield 2008, Gerlach and Ketterson 2013, Rosvall 2013, Hau and Goymann 2015, de Jong et al 2016.…”

Section: Introductionmentioning

confidence: 99%

Drought disrupts year-round breeding readiness in a tropical songbird

Boersma¹,

Enbody²,

Karubian³

et al. 2022

ACE

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Climate change is expected to increase the prevalence and severity of extreme weather events like drought. For many opportunistically breeding tropical bird species, precipitation serves as a primary cue for onset of breeding, and sustained drought can have major impacts on reproductive fitness. The physiological effects of drought are poorly understood, but understanding physiological responses can help resolve the mechanisms underlying effects of drought on population demography. We used physiological data collected on a year-round breeding New Guinea endemic passerine, the White-shouldered Fairywren (Malurus alboscapulatus), during years with persistent rainfall and during the 2015-2016 El Niño drought event to assess patterns of breeding readiness, body condition, and molt. Many males lost their cloacal protuberances, a sperm storage organ they typically maintain year-round, during the drought period. Body molt, which also occurs year-round in this species, was higher in males during the drought period. Using a sliding-window statistical model approach, we identified a critical precipitation window of 0-40 days prior to capture for cloacal protuberance volume and a window of 8-53 days for molt, with lower precipitation associated with smaller cloacal protuberances and greater molt. Plasma androgens were predictive of variation in male cloacal protuberance volume and molt, thus potentially mediating transitions between life-history stages in response to environmental conditions. Female molt, androgens, and male mass varied with photoperiod, with longer but decreasing day lengths characteristic of the austral summer associated with increasing molt and decreasing androgens. Collectively, our results indicate the potential for photoperiod to cue some life-history stages, whereas reduced rainfall impacts male but apparently not female reproductive physiology and readiness to breed. Improving our understanding of environmental regulation of life-history transitions in tropical taxa is essential for identifying which taxa are most at risk under a changing climate. La sécheresse perturbe la préparation à la nidification tout au long de l'année chez un passereau tropicalRÉSUMÉ. On prévoit que les changements climatiques augmenteront la prévalence et la gravité des phénomènes météorologiques extrêmes tels que la sécheresse. Pour de nombreuses espèces d'oiseaux tropicaux qui nichent de façon opportuniste, les précipitations sont le principal indice du début de la nidification, et une sécheresse prolongée peut avoir des répercussions importantes sur la capacité de reproduction. Les effets physiologiques de la sécheresse sont mal connus, mais la compréhension des réponses physiologiques peut aider à résoudre les mécanismes sous-jacents aux effets de la sécheresse sur la démographie des populations. Nous avons utilisé les données physiologiques recueillies chez un passereau endémique de Nouvelle-Guinée se reproduisant toute l'année, le Mérion à épaulettes (Malurus alboscapulatus), au cours d'années avec des précipitations ...

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Male White-shouldered Fairywrens (Malurus alboscapulatus) elevate androgens greater when courting females than during territorial challenges

Cited by 10 publications

References 50 publications

The evolutionary history and mechanistic basis of female ornamentation in a tropical songbird

The evolutionary history and mechanistic basis of female ornamentation in a tropical songbird

Does capacity to elevate androgens underlie variation in female ornamentation and territoriality in White-shouldered Fairywren (Malurus alboscapulatus)?

Drought disrupts year-round breeding readiness in a tropical songbird

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