Testosterone increases display behaviors but does not stimulate growth of adult plumage in male golden-collared manakins (Manacus vitellinus)

In order to attract females, male golden-collared manakins gather in leks and perform a complex display consisting of acrobatics accompanied by loud "wingsnapping". During this display, males show off their yellow beard and yellow, black, and green plumage that is striking in comparison to the dull green plumage of young males and females. We investigated the role of testosterone (T) in activating the display of manakins and in stimulating the growth of the adult male plumage. T regulates song, copulation, and territorial aggression in temperate species. In tropical species, however, T levels can be relatively low year round, which has raised questions about the involvement of T in courtship display and male aggression in these species. In neither temperate nor tropical species has the role of hormones in the shift from juvenile to adult plumage been well studied. Therefore, we implanted green-plumaged birds and adult males with either a T pellet or an inert pellet (controls) and observed the display behaviors of these birds in the field and in captivity. In captive birds, we also plucked feathers from sexually dimorphic regions and observed color and regeneration rate of new feathers. We found that birds implanted with T increased several display behaviors compared to controls. All plucked feathers grew back the same color as prior to treatment; however, we observed some differences in feather growth rate between T-treated birds and controls.     

Synchronizing feather-based measures of corticosterone and carotenoid-dependent signals: what relationships do we expect?

Carotenoids produce many of the red, orange and yellow signal traits of birds, and individuals must trade off utilizing carotenoids for physiological processes versus ornamentation. Proximate mechanisms regulating this trade-off are poorly understood, despite their importance for expression of color signals. Corticosterone (CORT) may play a significant mechanistic role in signal expression because it mobilizes energy substrates and influences foraging behavior. We used a unique feather-based approach to test whether CORT mediates expression of carotenoid-based coloration. First, we investigated relationships between levels of CORT from feathers (CORT_f) and carotenoid-based plumage signals in common redpolls (Acanthis flammea). Then, we determined how the width of growth bars and probability of having fault bars on feathers varied with CORT_f, specifically whether these metrics reflected developmental costs of elevated CORT (“stress” hypothesis) or represented an individual’s quality (“quality” hypothesis). CORT_f correlated positively with the strength of carotenoid signals, but only in adult males. However, also in adult males, CORT_f was positively related to width of feather growth bars and negatively with probability of having fault bars, providing support for the quality hypothesis. Overall, CORT_f was lower in adult males than in females or young males, possibly due to dominance patterns. Our results indicate that CORT may indirectly benefit feather quality, potentially by mediating the expression of carotenoid signals. We place our sex-specific findings into a novel framework that proposes that the influences of CORT in mediating carotenoid-based plumage traits will depend on the extent to which carotenoids are traded off between competing functions.     

EXTRAPAIR MATE CHOICE AND HONEST SIGNALING IN COOPERATIVELY BREEDING SUPERB FAIRY-WRENS

In many species of monogamous birds females copulate with males other than their social mates, resulting in extrapair fertilizations. Little is known about how females choose extrapair mates and whether the traits used to choose them are reliable indicators of male quality. Here we identify a novel male trait associated with extra-group mating success in the superb fairy-wren (Malurus cyaneus), a cooperatively breeding bird with one of the highest known frequencies of extra-group mating. Female fairy-wrens chose extra-group mates that molted earlier into breeding plumage. Males molted up to five months before the breeding season began, and only males that molted at least one month prior to its onset gained any extra-group fertilizations. This conclusion held after controlling statistically for the effect of age and social status on molt date. Once males acquired breeding plumage, they began courtship display to females on other territories. Thus, some males were displaying to females for several months before the breeding season began. This extraordinarily long period of advertisement by males may be facilitated by the long-term ownership of territories. We suggest that early acquisition of breeding plumage or the subsequent display behavior can be reliable cues for mate choice because they are costly to acquire or maintain.     

The multiple signals assessed by female satin bowerbirds: could they be used to narrow down females' choices of mates?

Female choice based on multiple male traits has been documented in many species but the functions of such multiple traits are still under debate. The satin bowerbird has a polygynous mating system in which males attract females to bowers for mating; females choose mates based on multiple aspects of males and their bowers. In this paper, we demonstrate that females use some cues to decide which males to examine closely and other cues to decide which males to mate with. Female visitation rates to bowers were significantly related to male size and the males' 'solitary' display rates, and, to a lesser extent, to the numbers of bower decorations. After controlling for female visitation rates, it was found that a male's mating success was significantly related to his size and the rate at which he 'painted' his bower with saliva and chewed up plant material.     

Species divergence in sexually selected traits: increase in song elaboration is related to decrease in plumage ornamentation in finches

Elaborate plumage and complex songs of male birds are two of the best-known examples of sexually selected traits, yet the interaction between these traits is poorly understood. Theory suggests that among a suite of potential displays, animals will emphasize traits that are most conspicuous, least costly, or best signal condition and reduce display of other traits. Here we examined the relationship between song and plumage elaborations in cardueline finches, songbirds that are highly variable in plumage displays and songs, but that share a similar mating system. We statistically controlled for body mass, habitat characteristics, and phylogenetic relationships and found that across species song complexity was strongly negatively related to elaboration of plumage ornamentation. When plumage coloration was partitioned into carotenoid-based and melanin-based components, song complexity was negatively related to elaboration of male carotenoid-based coloration but unrelated to elaboration of melanin-based coloration. These observations support the idea that, for condition-dependent traits, animal species trade off trait expression in response to changes in the costs or the information content of these traits. We discuss several alternative explanations for the observed pattern.     

Living with the past: nutritional stress in juvenile males has immediate effects on their plumage ornaments and on adult attractiveness in zebra finches

The environmental conditions individuals experience during early development are well known to have fundamental effects on a variety of fitness-relevant traits. Although it is evident that the earliest developmental stages have large effects on fitness, other developmental stages, such as the period when secondary sexual characters develop, might also exert a profound effect on fitness components. Here we show experimentally in male zebra finches, Taeniopygia guttata, that nutritional conditions during this later period have immediate effects on male plumage ornaments and on their attractiveness as adults. Males that had received high quality food during the second month of life, a period when secondary sexual characteristics develop, were significantly more attractive as adults in mate choice tests than siblings supplied with standard food during this period. Preferred males that had experienced better nutritional conditions had larger orange cheek patches when nutritional treatments ended than did unpreferred males. Sexual plumage ornaments of young males thus are honest indicators of nutritional conditions during this period. The mate choice tests with adult birds indicate that nutritional conditions during the period of song learning, brain and gonad development, and moult into adult plumage have persisting effects on male attractiveness. This suggests that the developmental period following nutritional dependence from the parents is just as important in affecting adult attractiveness as are much earlier developmental periods. These findings thus contribute to understanding the origin and consequences of environmentally determined fitness components.     

Early Social Networks Predict Survival in Wild Bottlenose Dolphins

A fundamental question concerning group-living species is what factors influence the evolution of sociality. Although several studies link adult social bonds to fitness, social patterns and relationships are often formed early in life and are also likely to have fitness consequences, particularly in species with lengthy developmental periods, extensive social learning, and early social bond-formation. In a longitudinal study of bottlenose dolphins (Tursiops sp.), calf social network structure, specifically the metric eigenvector centrality, predicted juvenile survival in males. Additionally, male calves that died post-weaning had stronger ties to juvenile males than surviving male calves, suggesting that juvenile males impose fitness costs on their younger counterparts. Our study indicates that selection is acting on social traits early in life and highlights the need to examine the costs and benefits of social bonds during formative life history stages.     

Hormonal differentiation of sexual behavior in Japanese quail

The effect of hormones on the development of Japanese quail during the postembryonic period was examined. First, subcutaneous implants of estradiol monobenzoate (EB) and testosterone propionate (TP) were implanted 6–12 hr after hatching. EB and TP had no effect on the differentiation of sexual behavior in genetic males or females. However, EB had marked feminizing effects on plumage in genetic males. Second, the role of gonadal hormones during development was examined by gonadectomizing males and females 6–12 hr after hatching and treating them intramuscularly with EB or TP as adults. EB-treated adult females displayed sexual behavior typical of the genetic female and developed female plumage. A significant proportion of TP-treated females (57%) displayed male sexual behavior patterns. Cloacal gland development and male-type vocalizations were induced. EB-treated males displayed either male or female sexual patterns depending on the stimulus conditions. Third, to test whether bisexuality in gonadectomized males and females is maintained despite steroid treatment and expression of sexual behavior in adulthood, gonadectomized quail which were originally treated with EB received TP and vice versa. The results indicate that in the absence of gonadal hormones after hatching female quail remain bisexual until exposed to estrogen, whereas gonadectomized male quail retain behavioral bisexuality irrespective of prior estrogen or androgen exposure.     

Supplemental food increases ornamentation of male nestling Eastern Bluebirds

Although the condition‐dependence and signaling function of ornamental plumage coloration among adult males is well studied, less research has focused on the information content of ornamental coloration among juvenile birds. Eastern Bluebird (Sialia sialis) nestlings grow their nuptial plumage while in the nest and dependent on parents for food, making them an ideal species for studying the development and function of elaborate plumage. Previous research suggests that plumage brightness of Eastern Bluebirds functions, in the juvenile stage, in parent–offspring interactions as a sexually selected trait in adults. Using an experimental approach, we tested the effects of supplemental food on the structural plumage coloration (i.e., tips of primary feathers) of Eastern Bluebird nestlings in Watauga County, North Carolina, during the 2011 breeding season. We provided supplemental mealworms daily to breeding pairs from the onset of incubation through the nestling period, and measured plumage brightness, UV chroma, and mass of nestlings (N = 89 males and 71 females). Male nestlings of supplementally fed parents exhibited brighter plumage. The mass and UV chroma of young bluebirds were not significantly affected by food supplementation. However, the relationship between mass and brightness differed between male nestlings in the control and supplementally fed treatments. Males reared in food‐supplemented territories exhibited a positive relationship between color and mass. Nestlings in control territories, however, exhibited a negative relationship between size and brightness, suggesting that reduced food availability results in a tradeoff between allocating resources toward somatic growth and development of bright plumage. Our results suggest that UV‐blue structural plumage in male juvenile Eastern Bluebirds is at least partially condition‐dependent and may help to explain why plumage color can influence social interactions in Eastern Bluebirds.     

Structural plumage colour and parasites in satin bowerbirds Ptilonorhynchus violaceus: implications for sexual selection

We investigated whether variation in structural plumage coloration in satin bowerbirds, Ptilonorhynchus violaceus , could reveal the intensity of infection from parasites, as predicted from models of parasite-mediated sexual selection (PMSS). To do this, we captured adult male, female, and juvenile male satin bowerbirds in Queensland, Australia, and objectively measured individual plumage reflectance from four body regions using a spectrometer. We quantified both ectoparasite load and the intensity of infection from blood parasites. In iridescent blue adult males, plumage reflectance is unimodal, with a single peak in the ultraviolet, while in greenish females and juveniles, plumage reflectance is bimodal, with peaks in both the ultraviolet and green portions of the spectrum. In adult males, the intensity of infection from blood parasites was best predicted by plumage brightness (total reflectance), with brighter males having fewer parasites. Similarly, juvenile males exhibiting greater UV chroma (proportion of reflectance in the UV) had fewer blood parasites. Our findings support a key prediction of PMSS models and provide the first evidence that a structural colour ornament can signal the intensity of infection from blood parasites.     

Asymmetrical expression of transsexual phenotypes in hummingbirds

I present evidence for asymmetry in the expression of transsexual traits in adult hummingbirds. Among females, individuals with male-like plumage are common and define a continuous range of variation. Among males, individuals with female-like plumage are rare and define discontinuous plumage morphs. Quantitative characters also distinguish transsexuals from other members of their sex, but the characters involved differ for male-like females (bill length) and female-like males (bill, wing and tail length). Gonadal development is correlated with transsexuality only in males; female-like males have significantly smaller testes than male-like males. Both sexes demonstrate a significant negative association between plumage brightness and bill length. This association suggests an ecological basis for transsexuality because differences in plumage and bill morphology are associated with differences in foraging behaviour within and between hummingbird species. Morphological differences between transsexuals and non-transsexuals imply that plumage sexual dimorphism is more likely to evolve through changes in the frequency of female, rather than male, transsexual variants.     

Experimental evidence that brighter males sire more extra‐pair young in tree swallows

Across taxa, extra‐pair mating is widespread among socially monogamous species, but few studies have identified male ornamental traits associated with extra‐pair mating success, and even fewer studies have experimentally manipulated male traits to determine whether they are related directly to paternity. As a consequence, there is little experimental evidence to support the widespread hypothesis that females choose more ornamented males as extra‐pair mates. Here, we conducted an experimental study of the relationship between male plumage colour and fertilization success in tree swallows (Tachycineta bicolor), which have one of the highest levels of extra‐pair mating in birds. In this study, we experimentally dulled the bright blue plumage on the back of males (with nontoxic ink markers) early in the breeding season prior to most mating. Compared with control males, dulled males sired fewer extra‐pair young, and, as a result, fewer young overall. Among untreated males, brighter blue males also sired more extra‐pair young, and in paired comparisons, extra‐pair sires had brighter blue plumage than the within‐pair male they cuckolded. These results, together with previous work on tree swallows, suggest that extra‐pair mating behaviour is driven by benefits to both males and females.     

Testosterone and its effects on courtship in golden-collared manakins (Manacus vitellinus): seasonal, sex, and age differences

Male golden-collared manakins gather on leks and perform an acrobatic display to attract females. In temperate breeding species, testosterone (T) activation of courtship displays has been well studied. Few studies have examined T activation of displays in tropical species; even fewer have explored the activational role of T in elaborate courtship displays such as in the manakin. In some tropical species, including manakins, territorial aggression or song behavior are uncoupled from T. We have previously shown that T activates display behavior in manakin males when endogenous T levels are low in the non-courtship season. To understand how T functions in breeding birds, we examined T levels in a large group of manakins sampled during the courtship and non-courtship season. In addition, during the courtship season, we gave T implants to adult males, juvenile males, and females. We found that T levels were low during the non-courtship season and comparatively higher on average during the courtship season. However, T levels were low in many adult males during the courtship season, especially when compared to temperate breeding species. Regardless of initial endogenous T levels during the courtship season, T implants did not increase the display frequency of adult males. T-treated females and juvenile males did display under similar conditions. Our data suggest that the effects of T on manakin display vary with season, sex, and age and that high T is not necessary for display.     

Ontogenetic timing as a condition‐dependent life history trait: High‐condition males develop quickly,peak early,and age fast

Within‐population variation in ageing remains poorly understood. In males, condition‐dependent investment in secondary sexual traits may incur costs that limit ability to invest in somatic maintenance. Moreover, males often express morphological and behavioral secondary sexual traits simultaneously, but the relative effects on ageing of investment in these traits remain unclear. We investigated the condition dependence of male life history in the neriid fly Telostylinus angusticollis. Using a fully factorial design, we manipulated male early‐life condition by varying nutrient content of the larval diet and, subsequently, manipulated opportunity for adult males to interact with rival males. We found that high‐condition males developed more quickly and reached their reproductive peak earlier in life, but also experienced faster reproductive ageing and died sooner than low‐condition males. By contrast, interactions with rival males reduced male lifespan but did not affect male reproductive ageing. High‐condition in early life is therefore associated with rapid ageing in T. angusticollis males, even in the absence of damaging male–male interactions. Our results show that abundant resources during the juvenile phase are used to expedite growth and development and enhance early‐life reproductive performance at the expense of late‐life performance and survival, demonstrating a clear link between male condition and ageing.     

DELAYED MATURATION,NEOTENY, AND SOCIAL SYSTEM DIFFERENCES IN TWO MANAKINS OF THE GENUS CHIROXIPHIA

Long-tailed manakins (Chiroxiphia linearis) and swallow-tailed manakins (C. caudata) are closely related, sexually dichromatic, lek-breeding species in which male mating success is highly skewed. Males of both species delay plumage maturation. Before reaching the definitive state, they wear a sequence of feather coats less conspicuous than that of the adult. Nondefinitive plumages probably enhance male survival in the two species; in C. caudata they may also enhance breeding success of young males, who may be fully reproductively mature their first year. In C. linearis testicular development is retarded along with that of plumage, although males may be physiologically capable of breeding prior to the acquisition of the definitive plumage. This difference probably reflects differences in the social systems of the two species. Five hypotheses have been proposed to explain the evolution of delayed plumage maturation. The sexual-selection, cryptic-breeder, and winter-adaptation hypotheses suggest that it functions primarily to enhance survival of young males. The juvenile- and female-mimicry hypotheses emphasize enhancement of immediate mating success. Support is provided for all but the female-mimicry hypothesis; it is argued that data are more consistent with juvenile mimicry and a neotenic origin of nondefinitive plumages.     

Hybridization cost of delayed maturation of secondary sexual traits in the collared flycatcher

In many species, individuals do not attain their full adult coloration until one or several years after reaching sexual maturity, and this signaling of juvenile status is thought to enable young individuals to avoid aggression from older, dominant conspecifics. We propose that hybridization may be one of several costs and benefits associated with such delayed maturation. We tested this idea in a hybrid zone of collared (Ficedula albicollis) and pied (F. hypoleuca) flycatchers on the Baltic islands of Oland and Gotland. One-year-old (subadult) male collared flycatchers differed from older birds in many plumage traits, and approached male pied flycatchers in phenotype. On both islands, subadult male collared flycatchers hybridized at a higher rate than adults. Mate-choice experiments in aviaries suggest that this difference is at least partly due to female pied flycatchers having a preference for subadults when constrained to choose a heterospecific mate. Because novel morphologies are often derived from changes in ontology, juvenile forms may resemble adults of closely related taxa. When such juveniles are reproductively mature, their phenotypic similarity to the adults of closely related species may increase their risk of hybridization.     

Multiple sexual ornaments in satin bowerbirds: ultraviolet plumage and bowers signal different aspects of male quality

Much attention has been devoted to understanding the evolutionof elaborate male ornaments and how they may signal male quality.However, the evolution of multicomponent sexual signals remainspoorly understood, and past research on this type of signalinghas been largely theoretical. Satin bowerbirds, Ptilonorhynchusviolaceus, are polygynous, are sexually dichromatic, and constructsexually selected display structures (bowers): a model systemfor investigating the evolution and signal function of multiplesexual signals. We studied the interrelationship between bowerfeatures, plumage coloration, and indicators of male qualityin this species. To do this, we located the bowers of male satinbowerbirds in rainforest in Queensland, Australia, and quantifiedbower quality. We captured the male bower owners and used reflectancespectrometry to objectively measure the plumage coloration ofseveral body regions. We measured various indicators of malehealth and condition, including the intensity of infection fromectoparasites and blood parasites. Bower quality and male ultravioletplumage coloration were significantly correlated. By using multipleregression analyses, we show that bower quality predicts ectoparasiteload and body size, whereas ultraviolet plumage coloration predictsthe intensity of infection from blood parasites, feather growthrate, and body size. Our findings support the multiple messageshypothesis of multicomponent signals: Female satin bowerbirdsshould assess both male and bower features to choose the highestquality mates.     

Feather stealing in the satin bowerbird (Ptilonorhynchus violaceus): male competition and the quality of display

Male satin bowerbirds use feathers to decorate their bowers and often steal feathers and other decorations from the bowers of other males. Decorations are a key element in sexual display and tracking their movement between bowers provides the first detailed information about this unique pattern of sexual competition. For two field seasons the movement of marked feathers was followed. Males varied greatly in stealing activity. The most active feather thieves were often from areas where bowers were close together and they were involved in reciprocal stealing with males at adjacent bowers. The rate of stealing by males was significantly correlated with the number of feathers on their bowers. This suggests that stealing is important in determining the level of bower decoration and mating success. Patterns of stealing behaviour support models of sexual selection which suggest that male interactions are important in influencing female choice through their effect on the quality of male display.     

Courts and courtship behaviour of Archbold's Bowerbird Archboldia papuensis in Papua New Guinea

Twelve bowers of Archbold's Bowerbird Archboldia papuensis in the Tari Gap, Southern Highlands, Papua New Guinea, are described. Incomplete courtship displays at four bowers were observed directly and videotaped, and 13 courtship displays culminating in copulation at five bowers were videotaped automatically. Bowers and male advertisement and courtship vocalizations and visual displays are described. Vocalizations included the mimicry of numerous sympatric bird species, calls like those of other bowerbird genera found elsewhere and inanimate sounds of the habitat. Courtships involved two phases. In the first, the male repeatedly chased the female while moving low, close to the surface of the display court. In the second phase, the male prostrated himself below the female and the yellow crest of adult males was presented to females as the male shook and repeatedly raised and lowered his head. Contrary to a previous report, the courtship display of the male Archbold's Bowerbird was assertive and the low position of the male appeared to function in threat reduction.     

Juvenile infection and male display: testing the bright male hypothesis across individual life histories

Current tests of the bright male hypothesis focus on assaysof adult disease resistance and their relation to male traitdevelopment and female choice. We suggest that if parasiteshave significant harmful effects on juvenile stages of a host,then females selecting males that effectively signal juvenileparasite resistance may gain a significant "good genes" benefit.Currently, there is no information on juvenile and adult infectionor resistance in the same male and whether adult male displayssignal juvenile parasite resistance. In the present study, wemeasure infection of the ectoparasitic louse, Myrsidea ptilonorhynchi,in individual male satin bowerbirds (Ptilonorhynchus violaceus)both as juveniles and nine or more years later as adults. Wetest hypotheses that examine the role of juvenile parasite infectionin mediating sexual selection. We found that (1) juvenile infectionis higher than adult infection in the same individuals, (2)adult males able to hold display sites have lower juvenile infection,and (3) juvenile and adult infection in the same individualsare not significantly correlated. In addition, comparisons amonga larger set of individuals from a single year show that bloodand ectoparasite infections are highly correlated, and bothdecrease with male age and are inversely related to male courtshipsuccess. These results, combined with the evidence that femalesmate exclusively with bower-holding males support the hypothesisthat females use adult male display traits to identify maleswith a high level of juvenile disease resistance. We suggestthat effective tests of the bright male hypothesis should include(1) assessment of infection resistance in both subadult andadult life history stages, (2) tests of whether differencesin age-specific resistance are indicated in adult male displays,and (3) tests to determine if females attend to these traitsin mate choice. Although these requirements increase the difficultyof testing the bright male hypothesis, they are necessary fora more accurate assessment of the effects of parasites on maledisplay and female choice.