The benefits of being dominant: Health correlates of male social rank and age in a marmot

The benefits of dominance may not come without costs, particularly for males. For example, the “immunocompetence handicap hypothesis” states that males with enhanced mating success allocate resources to enhance reproductive output at a cost to their current health, whereas the “resource quality hypothesis” predicts that high-ranking males may benefit from increased reproduction and good health. While the predictions from each have been well tested in captive animals and in a variety of highly social primates, fewer studies have been carried out in free-living, facultatively social animals. Using adult male yellow-bellied marmots (Marmota flaviventer), we evaluated predictions of these hypotheses by examining the relationship between social rank and two health indicators–fecal corticosterone metabolite (FCM) levels, and neutrophil/lymphocyte (N/L) ratios–after accounting for variation explained by age, body mass, and seasonality. We found that higher-ranking males tended to have a lower N/L ratio (reflecting good health) than lower-ranking individuals, whereas FCM levels were not significantly related to rank. In addition, heavier male marmots had lower N/L ratios, while body mass was not associated with FCM levels. We also found that older adult males had lower FCM levels (reflecting less physiological stress) but higher N/L ratios than younger adults. Finally, we found that FCM levels decreased as the active season progressed and FCM levels were associated with the time of the day. Overall, our results suggest that socially-dominant male marmots enjoyed better, not worse health in terms of lower N/L ratios.

Sex-biased parasitism and expression of a sexual signal

Given that sexual signals are often expressed more highly in one sex than the other, they can impose a sex-specific cost of reproduction through parasitism. The two primary paradigms regarding the relationship of parasites to sexual signals are the good genes hypothesis and the immunocompetence handicap hypothesis; however, there are other ecological, morphological and energetic factors that might influence parasite infections in a sex-specific fashion. We tested the relationship between expression of a sexual signal (the dewlap) and ecological, morphological and energetic factors mediating ectoparasite (mite) load between male and female Panamanian slender anoles (Anolis apletophallus). We found that males were more highly parasitized than females because of the preponderance of ectoparasites on the larger dewlap of males. Indeed, ectoparasite infection increased with both body size and dewlap size in males but not in females, and parasite infection was related to energy storage in a sex-specific fashion for the fat bodies, liver and gonads. Our work and previous work on testosterone in anoles suggests that this pattern did not arise solely from immunosuppression by testosterone, but that mites prefer the dewlap as an attachment site. Thus, the expression of this sexual signal could incur a fitness cost that might structure life-history trade-offs.

Testing the differential cost assumption of the handicap hypothesis with a tropical jumping spider

The handicap hypothesis predicts that more elaborate males attract more predators, but are also better able to escape attacks. Thus, a unit increase in trait elaboration has a lower cost for a high-quality male (i.e., differential cost). Although widely accepted, the handicap hypothesis has seldom been appropriately tested, especially concerning the differential cost assumption. Here, we tested this assumption using the jumping spider Hasarius adansoni. The courtship display of male H. adansoni involves bright white patches that contrast with their dark-coloured body. In experimental trials, we measured male escape capacity following a simulated predatory attack. Measurements of escape capacity were correlated to the size of white patches. Contrary to expectations, spiders with larger white patches did not exhibit better escape capacity. We conclude that this trait does not function as a handicap. It is possible that other sexual selection processes are at work.

Developing a transcriptomic framework for testing testosterone-mediated handicap hypotheses

ABSTRACTSexually selected traits are hypothesized to be honest signals of individual quality due to the costs associated with their maintenance, development, and/or production. Testosterone, a sex steroid associated with the development and/or production of sexually selected traits, has been proposed to enforce the honesty of sexually selected traits via its immunosuppressive effects (i.e., the Immunocompetence Handicap Hypothesis) and/or by influencing an individual’s exposure/susceptibility to oxidative stress (i.e., the Oxidation Handicap Hypothesis). Previous work testing these hypotheses has primarily focused on physiological measurements of immunity or oxidative stress, but little is known about the molecular pathways by which testosterone could influence immunity and/or oxidative stress pathways. To further understand the transcriptomic consequences of experimentally elevated testosterone in the context of handicap hypotheses, we used previously published RNA-seq data from studies that measured the transcriptome of individuals treated with either a testosterone-filled or an empty (i.e., control) implant. Two studies encompassing three species of bird and three tissue types fit our selection criteria and we reanalyzed the data using weighted gene co-expression network analysis. Our results show that testosterone-treated individuals exhibited signatures of immunosuppression and we provide some evidence to suggest that the transcriptomic signature of immunosuppression is evolutionarily conserved between the three species. While our results provide no evidence to suggest testosterone mediates handicaps via pathways associated with oxidative stress, they do support the hypothesis that testosterone enforces the honesty of sexually-selected traits by influencing an individual’s immunocompetence. Overall, this study develops a framework for testing testosterone-mediated handicap hypotheses and provides guidelines for future integrative and comparative studies focused on the proximate mechanisms mediating sexually selected traits.

Social and endocrine correlates of immune function in meerkats: implications for the immunocompetence handicap hypothesis

Social status can mediate effects on the immune system, with profound consequences for individual health; nevertheless, most investigators of status-related disparities in free-ranging animals have used faecal parasite burdens to proxy immune function in the males of male-dominant species. We instead use direct measures of innate immune function (complement and natural antibodies) to examine status-related immunocompetence in both sexes of a female-dominant species. The meerkat is a unique model for such a study because it is a cooperatively breeding species in which status-related differences are extreme, evident in reproductive skew, morphology, behaviour, communication and physiology, including that dominant females naturally express the greatest total androgen (androstenedione plus testosterone) concentrations. We found that, relative to subordinates, dominant animals had reduced serum bacteria-killing abilities; also, relative to subordinate females, dominant females had reduced haemolytic complement activities. Irrespective of an individual's sex or social status, androstenedione concentrations (but not body condition, age or reproductive activity) negatively predicted concurrent immunocompetence. Thus, dominant meerkats of both sexes are immunocompromised. Moreover, in female meerkats, androstenedione perhaps acting directly or via local conversion, may exert a double-edged effect of promoting dominance and reproductive success at the cost of increased parasitism and reduced immune function. Given the prominent signalling of dominance in female meerkats, these findings may relate to the immunocompetence handicap hypothesis (ICHH); however, our data would suggest that the endocrine mechanism underlying the ICHH need not be mediated solely by testosterone and might explain trade-offs in females, as well as in males.