Tests of association between the humoral immune response of red-winged blackbirds (<Emphasis Type="Italic">Agelaius phoeniceus</Emphasis>) and male plumage,testosterone, or reproductive success

We explored the potential relationships between male traits, reproductive success, testosterone levels in the breeding season, and humoral immunocompetence in male red-winged blackbirds (Agelaius phoeniceus). Males responded to a single injection of diphtheria-tetanus vaccine by producing antibodies to both antigens. The primary responses to each antigen were positively correlated with each other, but the relationship was clearly non-linear. No male responded strongly to diphtheria without also responding strongly to tetanus, but many males had strong responses to tetanus and weak responses to diphtheria. Response to tetanus was positively associated with hormone levels, whereas the relationship between testosterone and the response to diphtheria was weakly and nonsignificantly negative. We found no convincing relationships between immune responses and male morphological traits (epaulet size, body blackness, and body size), male success in male-male competition (territory size and tenure), or male reproductive success (number of mates, average clutch size, proportion of offspring sired, or proportion of young fledged). These results do not support testosterone acting as a constraint on immunity. Testosterone could be mediating a condition-dependent trade-off between sexual ornaments and the immune system, but the evidence for this was weak, as neither any male sexual trait nor any measure of performance was associated with immune responses. We could not eliminate the possibility that male sexual traits advertise other aspects of immunity that are not dependent upon condition or hormones.     

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     

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     

Exposing males to female scent increases the cost of controlling <Emphasis Type="Italic">Salmonella</Emphasis> infection in wild house mice

Secondary sexual characters often provide indicators of a male’s resistance to infectious diseases to rivals and potential mates, but it is unclear why. It is often suggested that males honestly signal their health due to energetic and other physiological trade-offs between investing into secondary sexual traits vs resistance to infectious diseases. Our aim was to determine whether such a trade-off exists using wild-derived male house mice (Mus domesticus). We exposed male mice to female scent, a manipulation that induces elevations in testosterone concentration and the expression of a variety of testosterone-mediated secondary sexual traits, and tested whether this sexual stimulation impaired the males’ ability to resolve or cope with an experimental infection (Salmonella enterica). We kept the males on a controlled diet to prevent them from compensating by eating more food. We found that sexually stimulated males were able to control bacterial growth as effectively as sham-stimulated controls; however, to do so, they lost more body mass during infection compared to the controls. In contrast, we found no evidence that sexual stimulation reduced the body mass of uninfected male mice. These results indicate that males’ responses to female odor are not immunosuppressive per se, yet they increase the energetic costs of controlling infection. Our findings support the idea that there is a physiological trade-off between secondary sexual signaling vs resistance to infectious diseases and suggest that studies using only immunocompetence assays might fail to detect such energetic trade-offs. We dedicate this paper to the late Professor Chris Barnard who conducted pioneering research on this topic.     

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.     

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     

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     

An experimental study on the causal relationships between (ecto-)parasites, testosterone and sexual signalling

Bird song is considered to have evolved via sexual selection and should as such honestly signal aspects of the quality of its bearer. To ensure honesty, the immunocompetence handicap hypothesis proposed a dual role of testosterone, having positive effects on sexual signalling but suppressive effects on immune function. However, recent studies showed that it is rather an immune activation that suppresses the androgen production. This reversed chain of causation may significantly alter the pathways, which translate the effects of parasites and pathogens into changes in the expression of male sexual traits. We infested male canaries with Ixodes ricinus tick nymphs to investigate the causal relationships between (ecto-)parasites, testosterone and sexual signalling, here singing behaviour. We focused on flexible song traits, which may quickly reflect changes in the infestation status, and tested whether these effects relate to changes in the plasma testosterone levels or health state. The experimental tick infestation altered the males’ song performance by reducing song consistency, a trait that had previously been identified to reflect male quality. The tick infestation lowered the plasma testosterone levels and had a negative effect on the health status in terms of a reduced hematocrit. Our pathway analysis then revealed that it is the parasite-induced reduction of the plasma testosterone levels but not of the health state that caused the changes in song consistency. Thus, our study supports the view that it is the effect of parasites and immune activation on plasma testosterone levels that generates the trade-off between immunocompetence and sexual signalling.     

Testosterone and helping behavior in the azure-winged magpie (Cyanopica cyanus): natural covariation and an experimental test

In this study, we investigated patterns of natural covariation between testosterone and reproductive status in a cooperatively breeding bird species, the azure-winged magpie (Cyanopica cyanus). To assess the relationship between testosterone and breeding behavior, we also manipulated testosterone (T) levels early in the season (before breeding started) using testosterone-filled or empty implants. Our results do not support the hypothesis that circulating testosterone levels affect the occurrence of helping behavior in the azure-winged magpie. Helping males had similar T levels to breeding males. Furthermore, experimentally augmented plasma T did not affect the likelihood of becoming either a helper or a breeder. Overall, these results are consistent with previous findings in other bird species and only give some support to the behavioral suppression hypothesis, suggesting that helping in the azure-winged magpie is a flexible behavioral option moderated in the short-term by social and ecological factors. Experimentally elevated testosterone levels, however, reduced the reproductive success of male breeders because of markedly lower levels of paternal care, had similar effects on their mates, but had the contrary effect on helpers, which raised levels of parental effort. We suggest increases in the share of paternity and in social prestige as possible explanations for these results.Communicated by: A. Cockburn     

Parasite faunas,testosterone and secondary sexual traits in male red-winged blackbirds

Summary We examined associations among parasite infections, secondary sexual traits and testosterone in male red-winged blackbirds sampled at the start of the breeding season. Parasites quantified included ectoparasitic lice and mites and endoparasitic blood protozoans, nematodes, trematodes and cestodes. Secondary sexual traits that we quantified included body size, epaulet size and color, song repertoire size and song switching rate, and behavioral responses to male and female models. Overall we found few significant associations between parasites and secondary sexual traits, between secondary sexual traits and testosterone, or between parasites and testosterone. In addition, most parasite taxa appeared to infect birds independently, although the low prevalence (<50%) of many of the parasites meant that our sample sizes were too small to detect weak associations. Our most promising results were obtained for ectoparasitic mites, which tended to occur on birds uninfected with other parasites, on birds with longer epaulets, and on birds with higher levels of testosterone. Epaulet length and testosterone are both probable correlates of dominance in this species. Further research will be required to determine whether there is a causal link between the immunosuppressive effects of testosterone and the mite infections, and between testosterone, epaulet length and male mating success. Correspondence to: P. Weatherhead