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Dynamic feedback between phenotype and physiology

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Dynamic feedback between phenotype and physiology in sexually selected traitsBirds gone wild: same-sex parenting in albatrossSpeciose versus species-richResearch FocusDynamic feedback between phenotype and physiologyin sexually selected traitsDustin R. Rubenstein1,2and Mark E. Hauber31Department of Integrative Biology and Museum of Vertebrate Zoology, University of California, Berkeley, 3060 Valley LifeSciences Building, Berkeley, CA 94720, USA2Department of Ecology, Evolution and Environmental Biology, Columbia University, Schermerhorn Extension, 10th Floor, 1200Amsterdam Avenue, New York, NY 10027, USA3School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland, New ZealandTheory predicts that physiological costs of producingelaborate phenotypes assure the honesty of sexuallyselected traits. It is generally assumed that these phys-iological processes drive sexually selected displays.However, a recent study by Safran and colleaguesdemonstrates that the manipulation of plumage orna-ments in barn swallows alters the temporal course ofcirculating androgens, thus rejecting the scenario of astatic, unidirectional relationship between physiologyand sexual displays. Instead, these results suggest thatdynamic feedbacks between physiological, morphologi-cal and behavioural costs underlie the development andmaintenance of sexually selected ornaments.Physiology of sexually selected traitsAnimals use elaborate displays in mate attraction andterritorial defence. Honesty of these signals is oftenenforced by costly physiological processes that underliethe production and maintenance of sexually selected traits[1–3]. The proximate control of many such ornamentsrelies on hormones to regulate signal production [4].Specifically, androgens, including testosterone, influencethe expression of many ornamental traits in birds, particu-larly the melanin-based rusty, brown and black coloursthat commonly underlie avian plumage. Melanins are themost common avian pigment, and experimental androgenelevations can enhance melanin-based plumage signalsused in mate attraction and social dominance [5]. Thesepatterns support the theoretical framework that physio-logical traits unidirectionally drive sexually selected dis-plays (Figure 1a) [6].Morphology–hormone feedback in barn swallowsIn a recent paper, Safran and colleagues [7] challenge theprevailing view that the relationship between hormonesand morphological traits is static and unidirectional. Theauthors demonstrate that experimentally enhancing maleplumage coloration in North American barn swallowsHirundo rustica erythrogaster (Figure 2) alters seasonalpatterns of circulating androgens and body mass duringthe breeding season. Rusty ventral plumage in barn swal-lows is a melanin-based [8] sexually selected trait thatinfluences female mate choice, reproductive timing andpaternity allocation [9]. Darker males breed earlier inthe season, have greater paternity and circulate moreandrogens than paler males [7,9]. One week after enhan-cing the ventral coloration of half of the males, experimen-tal males had elevated androgens but decreased bodymass, whereas control males showed the typical seasonaldecline in androgens and increase in body mass.The positive correlation between circulating androgensand coloration in premanipulation males [7] suggests thatandrogens are mechanistically linked to melanogenesisand pigmentation, or that there is an ongoing behaviouralfeedback on androgens related to ventral coloration as asocial cue. Given that the colour manipulations in thisstudy were done outside of the natural moulting periodof barn swallows, it is likely that the increases in andro-gens were the result of behavioural interactions resultingfrom the manipulations. The real surprise of this study,however, is that a phenotypic enhancement led tosuch rapid changes in circulating sex steroids of males.These results demonstrate that the relationship betweenandrogens and ornaments is not fixed (Figure 1a), butrather a dynamic process involving feedback betweenUpdateGlossaryAndrogen: steroid hormones most often associated with masculinisation. Themost common androgen in vertebrates is testosterone.Challenge Hypothesis: hypothesis proposed to explain the social modulationof androgens in males in a seasonal context. It describes how socialinteractions can lead to increased circulating androgens in animals, helpsexplain why androgens in males vary seasonally and predicts how maleandrogen levels relate to social systems.Corticosterone: the primary glucocorticoid in most non-mammalian verte-brates. It is released from the adrenals in response to a variety of social andenvironmental stressors.Glucocorticoid: steroid hormones produced in the adrenals in response tostimulation along the hypothalamic-pituitary-adrenal (HPA) axis. The mostcommon glu cocorticoids in vertebrates are corticosterone and cortisol.Glucocorticoids affect many aspects of vertebrate physiology and behaviourand predominantly regulate energy balance.Hypothalamic-pituitary-adrenal (HPA) axis: describes the hormonal cascaderesulting in glucocorticoid release. Corticotropin-releasing hormone (CFH)secreted from the hypothalamus stimulates the pituitary to secret adrenocorti-cotropic hormone (ACTH), which in turn stimulates glucocorticoid productionin the adrenals.Melanin: the most widespread group of pigments in animals that yield many ofthe black, brown and buff shades seen in plants, fungi and animals.Melanogenesis: the formation of melanin in melanocyte cells.Testosterone: an androgenic steroid primarily secreted from the gonads ofvertebrates. It stimulates seasonal reproductive behaviours such as courtship,sexual behaviours, territorial aggression and song, and plays an important rolein the production of sperm and a variety of secondary sexual characters.Corresponding author: Rubenstein, D.R. ([email protected]).655morphological signals and physiological traits, likelyindirectly via social interactions (Figure 1b).Androgen–morphology interactions: a complex andchanging systemAndrogens have long been known to seasonally modulatevertebrate reproductive behaviours. The Challenge Hy-pothesis formalised the relationship between circulatingandrogen concentrations in male vertebrates and seasonalpatterns of intrasexual aggression [10]; in essence, it wasthe first model of dynamic feedback between androgensand sexually selected traits. It sought to not only explainseasonal androgen


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