Sexually Selected Male Plumage Color Is Testosterone Dependent in a Tropical Passerine Bird, the Red-Backed Fairy-Wren (Malurus melanocephalus)

Abstract

BackgroundSexual signals, such as bright plumage coloration in passerine birds, reflect individual quality, and testosterone (T) may play a critical role in maintaining signal honesty. Manipulations of T during molt have yielded mixed effects on passerine plumage color, in most cases delaying molt or leading to production of drab plumage. However, the majority of these studies have been conducted on species that undergo a post-nuptial molt when T is low; the role of T in species that acquire breeding plumage during a pre-nuptial molt remains largely unexplored.Methodology/Principal FindingsWe experimentally tested the effects of increased T on plumage color in second-year male red-backed fairy-wrens (Malurus melanocephalus), a species in which after-second-year males undergo a pre-nuptial molt into red/black (carotenoid and melanin-based) plumage and second-year males either assume red/black or brown breeding plumage. T treatment stimulated a rapid and early onset pre-nuptial molt and resulted in red/black plumage acquisition, bill darkening, and growth of the sperm storage organ, but had no effect on body condition or corticosterone concentrations. Control males molted later and assumed brown plumage. T treated males produced feathers with similar but not identical reflectance parameters to those of unmanipulated after-second-year red/black males; while reflectance spectra of red back and black crown feathers were similar, black breast feathers differed in UV chroma, hue and brightness, indicating a potentially age and plumage patch-dependent response to T for melanin- vs. carotenoid-pigmentation.Conclusions/SignificanceWe show that testosterone is the primary mechanism functioning during the pre-nuptial molt to regulate intrasexually variable plumage color and breeding phenotype in male red-backed fairy-wrens. Our results suggest that the effects of T on plumage coloration may vary with timing of molt (pre- vs. post-nuptial), and that the role of T in mediating plumage signal production may differ across age classes, plumage patches, and between pigment-types.

Testosterone activates sexual dimorphism including male-typical carotenoid but not melanin plumage pigmentation in a female bird

“…80 µl) from the jugular vein, and took a series of morphological measurements. These included measurement of the size of the swelling posterior to the vent or CP (converted to volume using the formula π×depth/2×width×length; see Karubian, 2002;Mulder and Cockburn, 1993), an objective measure of bill color using a color reference chart ranging from 1 (cream colored) to 40 (complete black; Lindsay et al, 2011), the extent of molt based on the number of feathers encased in feather shafts (scored 0-3 across six body regions -head, back, tail, wing, belly and breast -and summed to generate a maximum score of 18; Lindsay et al, 2011), and the percentage of the body showing red/black nuptial coloration [a score of 0-10 given to each of five body regions -head, back, tail, belly and breast -for a cumulative score of 50, converted to percent (×2) following Webster et al, 2008]. We separated plasma from red blood cells via centrifugation and stored samples in liquid nitrogen until transport to Washington State University, where they were kept at −20°C awaiting further analysis.…”

“…We implanted 1-year-old males and females prior to the onset of their pre-nuptial molt with either an empty (control, 'C') or testosterone-filled ('T', crystalline testosterone -Sigma T1500) silastic tube (Dow Corning) between August and October 2007 (T females N=4, T males N=6, C females N=3, C males N=6) (see Lindsay et al 2011 for further details). We recaptured and collected morphological measurements including the length of regrown feathers from birds mid-treatment (17.8 days post-implantation, range=15-24 days) and again approximately 6 weeks postimplantation (mean=45.6 days, range=35-56), at which time implants were removed.…”

“…However, this hypothesis does not take into account the facts that: T-treated female Charadriiform species do not produce all components of the male signal (indicating that other mechanisms may also function; Lank et al, 1999); female Passeriformes can naturally produce some components of the maletypical elaborate plumage (e.g. Morales et al, 2007), which argues against genetic fixation or strict hormonal activation; and variation in male Passeriform coloration can respond to T (Gonzalez et al, 2001;Lindsay et al, 2011;Peters et al, 2000;Roberts et al, 2009), even in species in which sexual dichromatism appears to be LH dependent (e.g. house sparrow, Passer domesticus; Witschi, 1961).…”

“…Male red-backed fairy-wrens express discrete sexually selected (Karubian, 2002;Webster et al, 2008) and T-dependent variation in plumage and bill coloration (Karubian et al, 2011;Lindsay et al, 2011Lindsay et al, , 2009); males with low T titres during the prenuptial molt produce female-typical brown plumage and pale bills, whereas those with high T produce ornamented red/black plumage and black bills (Lindsay et al, 2009). Females can naturally produce some elements of the elaborate male phenotype (red feathers and darkened bill; see Results), though trait elaboration is rare and never reaches levels expressed by males despite elevated and variable T during the breeding season (Schwabl et al, 2014).…”

Glucocorticoids in Mate Choice

“…Testosterone has received by far the most attention in this domain due to evidence for its role in the development of those male traits used to attract females. Among many other traits testosterone is, for example, consistently found to relate to the vitality of sexually selected plumage colouration in birds (see for example [13,14]), the size and strength of antlers in red deer stags (Cervus elaphus; see for example [15,16]) and the intensity and complexity of bird song (see for example [17,18]). In essence, high testosterone results in a strong signal that, in turn, translates into mating success.…”