Acquisition of breeding coloration depends on badge size in male house sparrows Passer domesticus

Summary The black throat badge of the male house sparrow Passer domesticus, which functions as a status signal of dominance rank, changes in size during late winter because light feather tips gradually wear off. Males change the size of their visible badge earlier if their final badge size is large. The differential timing of the change from winter to breeding coloration in relation to badge size is partially controlled by the behaviour of the individual male. Feather abrasion of the badge is mainly due to preening and dust bathing. During late winter, male house sparrows preen the badge area more than females preen the homologous area, and males with large badges preen more than males with small badges. The seasonal change in size of the visible badge of male house sparrows may reflect the balance of different selection pressures. A large badge size signals dominance status in autumn and winter while predation by visually searching avian predators may constitute the main opposing selection pressure. Sexual selection causes a stronger selection pressure for a large badge in spring and summer. Correspondence to: A.P. Moller     

Badge size in the house sparrow Passer domesticus

Summary I studied female mate choice in house sparrows Passer domesticus in relation to the size of the black throat patch of males (badge size), which is a signal of dominance status, and to territory quality. Males with large badges obtained a mate earlier in spring than males with small badges. Males which remained unmated during the entire breeding season had smaller badges than mated males, even when controlling for the effect of other morphological traits and age. Largebadged males had territories with more breeding sites than small-badged males. Territories defended by males with large badges primarily had hole nest sites, which were safe from predators, and nestlings rarely fell from hole nests. Females were implanted with estradiol to induce copulation solicitation displays. Females responded more strongly to a male taxidermic mount and song than to song alone, and they responded more strongly and frequently to male mounts with large badges. Female house sparrows chose mates on the basis of male badges and perhaps on the basis of the quality of the nesting territories offered.     

Bill color, not badge size, indicates testosterone-related information in house sparrows

The honesty of ornamental signals of quality is often argued to be enforced via costs associated with testosterone. It is still poorly understood, however, how seasonal variation of testosterone within individuals is related to the timing and extent of ornament development. Here, we studied inter- and intra-individual variability of plasma testosterone levels in a population of 150 captive male house sparrows (Passer domesticus) through the course of a full year. We further analyzed the relationship between plasma testosterone levels and two sexually dimorphic ornaments: badge size and bill coloration. Also, because of a known negative relation between molt and circulating testosterone levels, we analyzed the relationship between ornamentation and molt status during the fall. We found that testosterone levels increased towards the breeding season and decreased before the onset of annual molt. However, within individuals, relative testosterone titers demonstrated low repeatability between seasons. Plasma testosterone levels were not correlated with badge size in any season but were correlated strongly with bill coloration during all periods, except the breeding season when variation in bill color was low. Finally, we found that bill coloration strongly correlated with molt status during fall. Our results indicate that bill coloration, not badge size, is the best ornamental indicator of a “running average” of male testosterone in house sparrows and therefore the best potential indicator of qualities and/or behavioral strategies associated with testosterone.     

Ectoparasites of house sparrows (Passer domesticus): an experimental test of the immunocompetence handicap hypothesis and a new model

Conspicuous secondary sexual traits may have evolved as handicap-revealing signals or as badges of status. We present results of an experiment using males of the sexually dimorphic house sparrow (Passer domesticus), that support the idea that the male-specific bib can be both a handicap-revealing signal and a reliable badge indicating the physical condition of the bird. In a test of the immunocompetence handicap hypothesis, wild-caught adult male house sparrows were studied in captivity. Birds implanted with elevated doses of testosterone were more dominant, had higher circulating levels of both testosterone and corticosterone and they also harboured relatively larger ectoparasite loads. Higher parasite loads were also associated with individuals showing lower immunocompetence and larger changes in bib size. A new model for immunocompetence effects in sexual selection is introduced, integrating actions that the hypothalamopituitary axis exerts on gonads, adrenals and the thyroid gland. The ”integrated immunocompetence model” synthesizes both the ”handicap” (i.e. survival-decreasing) and ”badge of status” (i.e. survival- enhancing) models for evolution of secondary sexual traits. Received: 15 May 1999 / Received in revised form: 2 November 1999 / Accepted: 6 November 1999     

Seasonal variation in the relationship between cellular immune response and badge size in male house sparrows (Passer domesticus)

The immunocompetence handicap hypothesis postulates that secondary sexual traits are honest signals of male quality because steroid hormones (such as corticosteroids and sex steroids), which are supposed to favor the development of secondary sexual traits, may also have immunosuppressive effects. Certain secondary sexual traits are not only used as mate choice signals but also play a role as badges of status. In the house sparrow (Passer domesticus), males have a bib of black feathers which is used both as a signal of social status in male-male interactions and by females when choosing a mate. We investigated the relationships between bib size and cellular immune response in male house sparrows during and outside the reproductive season. Males with large badges were found to have lower levels of immunocompetence, as assessed using a T-cell-mediated immunity assay, during the reproductive season, as predicted by the immunocompetence handicap hypothesis. Conversely, in November, the correlation between badge size and cellular immune response was positive, possibly reflecting the better access to trophic resources of large-badged dominant males in winter flocks. Received: 24 September 1998 / Received in revised form: 2 February 1999 / Accepted: 14 February 1999     

Sexual ornamentation,condition, and immune defence in the house sparrow Passer domesticus

Female mate preferences for extreme male ornaments may arise and be maintained because males signal their ability to raise an immune defence against parasites by the size of their ornaments. The bursa of Fabricius is an organ involved in antibody synthesis in young birds, but regresses before sexual maturity. The relationship between badge size, condition, and immune defence was investigated in male house sparrows, Passer domesticus, which have a bib of black feathers under their beak, a secondary sexual character currently subject to a directional female mate preference. The size of the bursa of Fabricius decreased during the first year of life in house sparrows. Males with large secondary sexual characters had a smaller bursa than males with small badges. Individuals with a large directional asymmetry in relative testis size had a larger bursa. The abundance of one parasite (a mallophagan) was positively related to bursa size. There was a positive relationship between relative volume of bursa of Fabricius and the number of fault bars on feathers, which is a measure of body condition. These results suggest that males with large badges have lower current levels of immune response than males with small badges, and that males in good body condition, as evidenced from the absence of fault bars, had a relatively small bursa of Fabricius. Received: 6 October 1995/Accepted after revision: 2 June 1996     

Digit ratios (2D:4D), secondary sexual characters and cell-mediated immunity in house sparrows <Emphasis Type="Italic">Passer domesticus</Emphasis>

Homeobox genes regulate development of digits, and it has been suggested that the ratio of length of second to length of fourth digit reflects such genetic effects in a sex-specific manner. We show that digit ratios in the sexually dichromatic house sparrow Passer domesticus differ between sexes, with males having higher ratios than females, and that individuals produce consistent ratios on the two feet. If Homeobox or other genes had pleiotropic effects on development of digits, behavior, and physiology of males and females, we would expect secondary sexual characters and immunity to be related to digit ratio in a sex-specific manner. The size of the visible part of the black badge in February (a secondary sexual character), but not total badge size, was positively correlated with digit ratios, suggesting that males with more male-like digit ratios had larger visible badges. Because of sex-specific effects of development on secondary sexual characters and immunity, we predicted sex-specific differences in immune response to be related to digit ratio. House sparrows with large digit ratios had weaker T cell-mediated immune response than individuals with small digit ratios, particularly in females, implying that females with more male-like digit ratios had weak immune responses. These findings are consistent with the hypothesis that early development, as reflected by digit ratios, and genetics affect the expression of adult characters that are supposedly strongly contributing to fitness.     

Yolk testosterone organizes behavior and male plumage coloration in house sparrows (<Emphasis Type="Italic">Passer domesticus</Emphasis>)

Vertebrate eggs contain maternal steroid hormones in their yolks; and in avian species the concentration of these steroids vary within and among clutches. The organizational actions of these variable doses of maternal steroids in the avian egg, analogous to those regulating the development of sexually dimorphic traits, are little explored. In this study, we examined the organizational effects of yolk testosterone in the house sparrow, Passer domesticus, a sexually dichromatic passerine bird in which males are characterized by the presence of a throat patch or badge of black feathers that varies in size among males. We injected a physiological dose of testosterone or vehicle into eggs in the field, removed nestlings, and hand-raised them in the laboratory. At 5 months of age, we investigated treatment effects on plumage and behavior. Males that hatched from testosterone-injected eggs developed a larger badge than males that hatched from vehicle-injected (control) eggs. However, testosterone did not induce the expression of a badge in females. In staged dyadic encounters, both males and females hatched from testosterone-injected eggs were more successful at obtaining and defending a food source than individuals of the same sex hatched from control eggs. The results suggest that variable concentrations of maternal testosterone in the eggs of the house sparrow organize the expression of a plumage trait in males and behavior in both sexes.Communicated by J. Graves     

Sex-specific nest defense in house sparrows (Passer domesticus) varies with badge size of males

According to indicator models of sexual selection, females can benefit from choosing males with above average epigamic traits, but empirical evidence for such benefits is scarce. Here, we report results from an experiment with 29 pairs of house sparrows (Passer domesticus) where the intensity of nest defense against a mounted mustelid predator was related to the size of the black throat and breast patch (“badge”) in males. Using principal components analysis (PCA), original response variables of both sexes were reduced to two factors: “Approach” to the predator and “Distant warning”. “Approach”, the more risky behavior, increased from small- through medium- to large-badged males and decreased in their females. Since large-badged males have a higher certainty of paternity (i.e. greater benefits from defense) and may be older and more experienced (i.e. incur lower costs), the most likely explanation for male defense intensity increasing with badge size is an improving benefit/cost ratio. The resulting optimal response of their females and evolutionarily stable participation in joint parental care is illustrated by a graphical model. It shows that females would, indeed, benefit directly from choosing large-badged males. This, however, is no proof of a direct evolutionary tie between badge size and paternal behavior, as assumed by indicator models of sexual selection. It may simply represent a spurious relationship, originating from the correlation of badge size and defense with confidence of paternity. Received: 22 September 1997 / Accepted after revision: 3 November 1997     

Permanent exposure versus facultative concealment of sexual traits: an experimental study in the house sparrow

In many bird species the cryptic winter plumage is due to the presence of light feather tips that conceal conspicuous colorations. The gradual abrasion of these tips that makes sexual traits visible has been interpreted as a strategy to improve mating success (here referred as the permanent exhibition hypothesis). However, under some circumstances, the maintenance of a full plumage that facultatively enables the bird to exhibit or cover aggression-inducing traits has proved to be advantageous (the coverable badge hypothesis). In a population of house sparrows where black throat patches (here called badges) are used in intrasexual competition, the degree of abrasion of dull feather tips that conceal bright colour early in the breeding season correlated neither with badge size nor with traits indicating morphology and body condition. These results are only in accordance with predictions of the coverable badge hypothesis. In 1992 experimental clipping of badge feather tips, which forced permanent exposure of badges, negatively affected birds with the largest badges in terms of nest acquisition, but an opposite trend was indicated for birds with the smallest badges. In 1993, when more novel birds in the study area were competing for nesting sites than in 1992, only badge size, but not the experimental manipulation, affected nesting success. These results suggest that the loss of the ability to conceal badges was disadvantageous, and more so if most competing individuals had already been resident in the colony in previous years and the larger their badges were. There is a striking contrast between the results reported for this study population, where badges mainly signal fighting ability, and those reported for another house sparrow population, where badges are mainly used in mate choice. In this last population, tip abrasion is advantageous for dominant individuals showing the largest badges. This suggests that the trade-off between conserving versus wearing off the feathers that conceal ornaments could have different optimal resolutions depending on the relative importance of inter and intrasexual selection on indicator traits. Received: 29 September 1995/Accepted after revision: 14 July 1996     

Testosterone,dominance signalling and immunosuppression in the house sparrow,<Emphasis Type="Italic"> Passer domesticus</Emphasis>

The immunocompetence handicap hypothesis (ICHH) suggests that dominance signals are costly because their development is controlled by testosterone, which is immunosuppressive. Signal control therefore links an increased disease risk with a high quality signal. The chest bib of the house sparrow, Passer domesticus, is a signal known to be related to dominance and under control of testosterone levels. We experimentally manipulated testosterone in male sparrows during the breeding season and again independently during the post-breeding period to test whether variation in levels of testosterone could cause variation in levels of immunocompetence. There was no effect of testosterone manipulation on the cell-mediated response of birds to phytohaemagglutinin injection, nor did testosterone levels appear to affect either white blood cell ratios or red blood cell counts. In contrast, both breeding season and post-breeding season testosterone levels had significant effects upon the humoral response of the birds to sheep red blood cell injections. However, whilst testosterone during the breeding season appeared to act immunosuppressively, the role of post-breeding levels is less clear. In concordance with a previous study, there was an indication that corticosterone is involved in mediating the immunosuppressive effects of testosterone. The strength of the secondary humoral response and the cell-mediated response were negatively related suggesting the possibility of a trade-off between the different arms of the immune system. These results provide some support for the ICHH as a mechanism promoting the evolution of costly badges of status, although the results question whether the immunosuppressive cost can be mediated by testosterone at the time of badge development.Communicated by W.A.Searcy     

Sexual behavior is related to badge size in the house sparrow Passer domesticus

Summary Badge size, which functions as a signal of dominance status in male house sparrows Passer domesticus, was significantly related to their sexual behavior. Males with large badges participated in communal displays (multi-male chases directed towards single females) more often than males with small badges, irrespective of whether the female involved was the male's mate or not. Experimentally released females were more often chased if they were fertile than if they were nonfertile. Estradiol-implanted females were chased more often than control females without a hormone implant, and males with large badges chased estradiol-implanted females more often than did males with small badges. Both forced extra-pair copulations during communal displays and unforced extra-pair copulations were more often achieved by males with large than small badges. Male house sparrows with large badges also copulated with their mates at a higher rate than did males with small badges. A higher certainty of paternity therefore is hypothetized to accrue to male house sparrows with large badges.     

Testosterone is involved in acquisition and maintenance of sexually selected male plumage in superb fairy-wrens, Malurus cyaneus

Testosterone has been proposed as a physiological link between the level of sexual signalling and male condition. Bright plumage is one of the most noticeable sexual signals and is often used by females as a basis for mate choice. Yet bright male plumage is not necessarily testosterone dependent. We investigated the role of testosterone in the moult into seasonal nuptial plumage in male superb fairy-wrens. Early pre-nuptial moult is under intense intersexual selection and males can acquire the bright plumage any time between autumn and the next spring. Testosterone was always undetectable or very low in males in dull eclipse plumage. During the pre-nuptial moult, both the number of males with detectable testosterone and average testosterone levels increased sharply. High testosterone was more correlated with nuptial plumage than with presence of the cloacal protuberance (indicative of sperm storage). Subcutaneous testosterone implants always induced the pre-nuptial moult within 2–3 weeks after implantation, even well outside the natural time range of moulting. Moreover, removal of the implants before the nuptial plumage was completed, arrested the moult process. The evidence suggests that development of the nuptial plumage is testosterone dependent, although we cannot exclude that testosterone exerts its action after conversion to a metabolite such as oestrogen. Once the nuptial plumage was completed, all males maintained substantially elevated testosterone, sometimes months before the onset of breeding. These high levels could be necessary to maintain the plumage, and/or are involved in courtship displays. The results are discussed with respect to potential costs involved in acquiring and maintaining the nuptial plumage. Received: 17 January 2000 / Received in revised form: 24 February 2000 / Accepted: 25 February 2000     

Ectoparasite loads in free-ranging northern fence lizards, Sceloporus undulatus hyacinthinus: effects of testosterone and sex

More knowledge of the proximate factors that influence parasite loads would help us understand the selective pressures faced by hosts and host-parasite evolution. Testosterone has been associated with increased parasite loads in vertebrates. Here we asked whether experimentally elevated testosterone affected ectoparasite loads in free-ranging northern fence lizards (Sceloporus undulatus hyacinthinus). Males were captured, given testosterone or sham implants, and released. In 2 consecutive years, testosterone-implanted males had significantly more ectoparasites at recapture than did controls. Additionally, ectoparasite loads were positively correlated with testosterone concentrations in unmanipulated males, and males had significantly more ectoparasites than did females. The results are consistent with an effect of testosterone on parasite loads. However, rather than elevated testosterone increasing mite loads in experimental males, it appeared that high testosterone inhibited a natural seasonal decline in mite loads. Testosterone-implanted males also lost body mass whereas controls gained mass. Among controls, those retaining the most ectoparasites over the course of the experiment experienced the smallest gains in body mass, suggesting that the mites are costly.     

Social environment during molt and the expression of melanin-based plumage pigmentation in male house sparrows (<Emphasis Type="Italic">Passer domesticus</Emphasis>)

Evolutionary biologists have shown much recent interest in the costliness and signal content of colorful plumage displays in birds. Although many studies suggest that both carotenoid- and structurally-based plumage colors are condition-dependent indicators of health and nutritional state at the time ornamental feathers are grown, there is little experimental evidence supporting the idea that melanin pigmentation is a reliable signal of condition during molt. Instead, melanin-based ornamental coloration often reveals the competitive ability and dominance of individuals throughout the year. However, this work does not indicate which proximate environmental factors shape the expression of melanin pigmentation at the time of feather growth. Because of the link between melanin coloration and the social environment, it is possible that the development of brightly colored plumage may be associated with aggressive social interactions during feather molt. Here, we show that melanin-based ornamental coloration in male house sparrows (Passer domesticus) is correlated with the degree to which individuals interact aggressively with conspecifics during molt. Males that were dominant (beta, but not alpha) within captive social groups during molt grew larger badges than subordinates. Groups of males that had higher rates of aggression during molt grew larger badges than less aggressive triads. To our knowledge, this is the first demonstration that melanin pigmentation and plumage-based status badges are related to the competitive history of individuals during feather development. By coupling badge size directly with aggressive experiences during molt, birds can use their status signal to honestly indicate their likelihood of winning agonistic encounters throughout the year.     

The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus)

Many bird species have patches of colour in their plumage, contrasting with their basic coloration, which are used to display and signal status to conspecifics. These are called ’badges of status’, because they are believed to be low-cost signals of social status. For a signalling system to be evolutionarily stable, cheating must be controlled. The conventional view is that there is frequent testing, which uncovers cheats. Recently, the immunocompetence handicap hypothesis (ICHH) suggested that signals may be dependent on testosterone for their development, with a cost being imposed through immune suppression. We report experiments on house sparrows (Passer domesticus) which show that testosterone significantly influences the size of the bib (a ’badge of status’). The ultimate effect of the testosterone manipulation was to impair antibody production, as predicted by the ICHH. However, testosterone manipulations also changed the levels of the ’stress hormone’ corticosterone. The level of corticosterone was also related to the degree of immunosuppression. After controlling for the effect of corticosterone, testosterone enhanced the birds’ ability to produce antibodies, counter to the ICHH. The hypothesis therefore must be modified. We suggest that testosterone has a dual effect: it leads to immunosuppression through a mechanism involving corticosterone but, conversely, leads to increased immunocompetence probably via dominance influencing access to resources. Received: 5 March 1999 / Received in revised form: 1 October 1999 / Accepted: 16 October 1999     

Achromatic color variation in black-capped chickadees,Poecile atricapilla: black and white signals of sex and rank

Sexual dichromatism and phenotypic variation in elaborate male traits are common products of sexual selection. The spectral properties of carotenoid and structurally-based plumage colors and the patch sizes of melanin-based plumage colors have received considerable attention as sexual signals in birds. However, the importance of variation in achromatic plumage colors (white, gray and black) remains virtually unexplored, despite their widespread occurrence. We investigated a potential signal function of the achromatic black and white plumage of black-capped chickadees (Poecile atricapilla). We captured and color-banded 178 free-living chickadees and assessed winter flock dominance hierarchies by tabulating pairwise interactions at feeders. We recaptured 73 of these birds and measured plumage coloration for six body regions using a reflectance spectrometer and the area of melanin-based plumage patches from standardized photographs. We found extensive individual variation in chickadee plumage traits and considerable sexual dichromatism. Male black-capped chickadees have significantly brighter white plumage than females, larger black patches, and greater plumage contrast between adjacent white and black plumage regions. We also found rank differences in the plumage reflectance of males; high-ranking males, who are preferred by females as both social and extra-pair partners, exhibit significantly darker black plumage and grow their feathers more rapidly than low-ranking males. This variation among individuals reveals a potential signal function for achromatic plumage coloration in birds.     

Extrapair paternity in the swamp sparrow, <Emphasis Type="Italic">Melospiza georgiana</Emphasis>: male access or female preference?

Over the past two decades, the combination of molecular and field methods has revealed considerable variation in the level of extrapair fertilizations among socially monogamous birds. Models predicting extrapair young range in scale from a single population to multiple Orders, and there is no single, unifying theory for these reproductive tactics. We investigated proximate explanations of extrapair fertilizations in two subspecies of the swamp sparrow, Melospiza georgiana georgiana and Melospiza georgiana nigrescens, across a range of social and environmental conditions. The presence of extrapair young was best predicted by the size of two male plumage badges (one correlated with parental care and one with territorial aggression) relative to the badge size of their immediate neighbors, the interaction of these two measures, mean territory size, and the maximum size of the aggression badge among neighbors. The size of the male’s parental care badge (relative to neighbors) was negatively correlated with the probability of lost paternity. The relative size of the aggression badge was positively correlated with the presence of extrapair young when the parental care badge was small and negatively correlated when the badge was large. Controlling for these crown measures, males with larger territories were less likely to suffer losses in paternity. There was no effect of breeding density, breeding synchrony, their interaction, subspecies, or weather during the fertile period on the presence of extrapair young. These results suggest that female preference for males that provide more parental care (or preference for genes that convey this trait) plays a dominant role in extrapair interactions among swamp sparrows. Models based on female assessments of relative mate quality offer a promising explanation of patterns in extrapair fertilizations among bird species.     

Song output and stimulation of the female in white-throated sparrows

Summary We investigated the importance of song length and singing rate in stimulating female white-throated sparrows, Zonotrichia albicollis. In November 1988 ten female and one male white-throated sparrow were captured during the fall migration. To enhance the expression of sexual receptivity, the females were implanted with 17-beta-estradiol silastic pellets. Using the visual stimulus of a non-singing male to further enhance the expression of sexual receptivity in the females, we found that females gave a greater response, in the form of copulation displays, to a five-note versus a two-note version of a typical male white-throated sparrow song. Each version was played back at four songs per minute. In May 1990 birds were captured and treated as before, except that the two-note song was played at ten songs per minute and the five-note song at four songs per minute. Therefore, each female heard twenty notes per minute. In the second experiment, the females did not show a statistical difference in response to the two- and five-note song playbacks. We interpret the results of the second experiment as indicating the song rate as well as song length is important in stimulating female white-throated sparrows because increasing the rate of the two-note song brought the response up to the level of response we obtained to the five-note song played at the slower rate. We conclude that in white-throated sparrows, song output is important for female stimulation.     

Testosterone treatment suppresses paternal care in superb fairy-wrens, Malurus cyaneus, despite their concurrent investment in courtship

Courtship displays and paternal care in male birds are generally thought to be mutually exclusive, because testosterone, necessary for stimulation of sexual behaviours, suppresses paternal behaviours. Superb fairy-wrens, Malurus cyaneus, are unusual in that males concurrently engage in courtship and paternal care. Fairy-wrens live in stable socially monogamous pairs with 0-4 subordinate male helpers. Both helper and dominant males provide care whenever it is required but continue courtship throughout the period of care as most fertilisations are extra-group and females are multi-brooded. To examine the role of testosterone in this trade-off, we compared testosterone levels in males of different social status, while they had dependent nestlings, and determined the effect of testosterone treatment on provisioning rates of pairs. Testosterone levels were lower in subordinate helpers, although these do not provide more paternal care than dominant males. Conversely, testosterone levels were similar in dominant males with or without helpers, although as the number of helpers increases males invest substantially less in nestling care and more in extra-group courtship. Although testosterone levels are high, irrespective of paternal duties, experimental testosterone treatment of males resulted in a large (65%) reduction in nestling feeding rates. Surprisingly, there was no indication that females compensated for this reduction in provisioning, suggesting that females might assume a constant male contribution to offspring care. We conclude that during nestling provisioning, male fairy-wrens maintain testosterone at an individual level that does not interfere with parental duties, while allowing high investment in extra-group courtship.