Lifetime reproductive success for males is usually constrained by access to fecund females (i.e., fertilizations). Male-male contest competition for mating opportunities is common in mammals, and in those species that typically form multi-male groups, one outcome of this competition is the formation of dominance hierarchies. Male dominance hierarchies occur in many primate species, and males typically invest considerable effort into attaining and maintaining high dominance rank. Monopolization of fecund females by high ranking males and/or exclusion of rivals via aggression, alliance formation or other means at times when females are most likely to conceive would be advantageous if it leads to increased reproductive success. Genetic analyses now support the argument that high dominance rank can yield reproductive payoffs in several nonhuman primate species [1–6].
Chimpanzees (Pan troglodytes) live in multi-male, multi-female communities. Males are philopatric; social bonds between them are strong, and they cooperate with each other in various ways within communities and also cooperate in aggression between communities. However, males also compete for mating opportunities and form dominance hierarchies, and most males invest considerable effort into striving for high rank . Because chimpanzees have a fission-fusion social system and individuals can go for long periods without encountering each other, males face an additional need to assert themselves frequently towards subordinates when they are together to maintain dominance over them. Genetic data from several chimpanzee study sites indicate that alpha males and others who attain high rank generally achieve disproportionately high reproductive success, although reproductive skew is only moderate in communities with more than a few adult males [8, 9].
Male dominance status is not a simple function of aggressiveness, but acquisition and maintenance of high dominance rank often involves frequent aggression, and testosterone has been considered the quintessential physiological moderator of such behavior. Testosterone can alter both neurological and musculoskeletal functions that may potentiate pre-existing patterns of aggression. As an anabolic steroid, testosterone increases basal metabolic rates and stimulates muscle anabolism, adipose catabolism and redistribution [10–12]. Testosterone increases metabolic rates in muscle cells in vitro , which would be useful during competitive interactions. Testosterone reduces the refractory period between action potentials throughout the stria terminalis (connecting the hypothalamus with the amygdala), which can potentiate an aggressive response . Testosterone also influences the organization of typical masculinized morphological and behavioral characteristics beginning in utero [15, 16].
Direct associations between testosterone, rates of aggression, and dominance rank have been identified in several species, including nonhuman primates [17, 18]. Conversely, several studies have failed to demonstrate significant correlations between aggression, dominance rank and testosterone levels [19, 20]. In fact, there is surprisingly little evidence that short-term changes in testosterone levels correlate with increased levels of aggression, and fluctuations in testosterone levels in healthy, eugonadal individuals over time do not necessarily predict changes in levels of aggression within individuals, human or nonhuman [reviewed in  and ]. Rather, testosterone may have a permissive effect, potentiating pre-existing patterns of aggression . Testosterone is also more frequently associated with aggression and dominance rank during situations of social instability, such as during challenges by conspecific males for territory or access to mates, the establishment of territorial boundaries, the formation of dominance relationships, or in the presence of receptive females .
Testosterone may facilitate attainment of high rank, and thus increase reproductive success, by modifying behaviors (e.g., aggression, mate seeking, courtship, mate guarding) and physical attributes (i.e., secondary sexual characteristics and muscle anabolism). However, there are a number of costs imposed by elevated testosterone levels. These include increased metabolic rates [25, 26], increased risk of prostate cancer , production of oxygen radicals , and immunosuppression [reviewed in ], all of which could compromise survivorship.
Testosterone, along with many other hormones, functions as a biochemical link between various somatic and reproductive traits. Trade-offs between competing functions and traits (i.e., maintenance, reproduction and growth) are fundamental to life history evolution, particularly in organisms that are constrained by limited energy supplies . Because of its multiple effects, testosterone is an important endocrinological mediator of various trade-offs, particularly that between reproduction and survivorship [31, 32]. More specifically, it may balance the competing demands of increased reproductive success afforded by testosterone-mediated physique, aggressive behavior, and dominance status with increased susceptibility to illness.
As Folstad and Karter  originally suggested, testosterone can stimulate the development and maintenance of secondary sexual characteristics while also reducing immunocompetence. Wedekind and Folstad  added that the suppression of the immune system by testosterone could allow for energy to be reallocated to the production of secondary sexual characteristics, particularly muscle mass in mammals . The presence of elaborate secondary sexual characteristics, or other characteristics that honestly reflect health, may therefore advertise good survivability to potential mates . Many morphological and behavioral characteristics appear to be honest sexual signals of immunocompetence in avian and other species. Just a few examples include tail length in peacocks (Pavo cristatus)  and barn swallows (Hirundo rustica) , badge size in house sparrows (Passer domesticus) , antler size in white-tailed deer (Odocoileus virginianus) , song length and complexity in several avian species , coloration in satin bowerbirds (Ptilorhynchus violaceus) , and antler symmetry in caribou (Rangifer tarandus) . Phenotypic traits, like coloration, in male nonhuman primates may also indicate health status [reviewed in ], although this has yet to be adequately investigated.
Dominance rank in nonhuman primate males may be an honest indicator of immunocompetence. If testosterone is immunosuppressive, and high dominance rank is associated with high testosterone levels, then high rank may also be associated with higher parasite burden. 'Higher quality' males may be able to withstand the immunosuppressive effects of high testosterone levels, allowing them to invest in secondary sexual characteristics or behaviors dependent on androgens. Those males with greater innate disease resistance may be better able to maintain higher testosterone levels, high ejaculate quality and other traits associated with successful reproduction . Lower quality males may not be able to tolerate the immunosuppressive effects or increased energetic costs of high testosterone levels [45–47]. The antagonist pleiotropic effects of androgens may thus both limit trait exaggeration and have important influences on social behavior.
Glucocorticoids are also likely important in mediating the relationships between agonistic interactions, dominance rank, reproductive function, and immunocompetence. Glucocorticoids like cortisol and corticosterone are steroids released from the adrenal cortex in response to disruption of physiological and psychological homeostasis. While this increases circulating glucose levels to facilitate physical and mental activities and basic stress responses, prolonged elevation of glucocorticoid levels can have pathological effects on cognition, growth, reproduction, immunity and other functions . For example, cortisol can inhibit inflammation and allergic reactions, lymphocyte proliferation, antibody and cytokine secretion, and macrophage activity [49–51]. Glucocorticoids can inhibit gonadotropin releasing hormone release from the hypothalamus, downregulate testicular luteinizing hormone receptors, and decrease testicular steroidogenesis [52–54].
Because cortisol is released in response to various stressors, a typical assumption has been that acute and sustained social stressors associated with low dominance status would result in chronic elevations in cortisol levels in low ranking animals. In some species, cortisol levels are higher in low than high ranking individuals, whereas in other species the opposite is true . The relationships between cortisol and dominance rank may depend on access to social support systems . Furthermore, during times of social instability, high ranking animals will likely exhibit the highest cortisol levels, probably due to the need for increased arousal and vigilance .
To improve understanding of the relationships among dominance rank, testosterone and cortisol levels, and infection status in nonhuman primates, we collected fecal samples and behavioral data from an unusually large community of wild chimpanzees. Our previous work on this community indicated a significant positive association between testosterone levels and dominance rank for adult males (n = 22 animals with 67 total fecal samples; mixed model analysis controlling for age, p = 0.032) . Other analyses indicated that fecal testosterone (p = 0.033) and cortisol (p = 0.020) were positively associated with parasite richness (the number of unique intestinal parasite species recovered from hosts' fecal samples) in both adult and adolescent males (n = 35 animals with 100 total fecal samples; mixed model analysis controlling for age) . In the present study, we add to this research agenda by better describing the complex relationships between dominance rank, fecal intestinal parasite infections, and cortisol and testosterone levels in the adult male chimpanzees from the Ngogo population.