The costs of dominance: testosterone, cortisol and intestinal parasites in wild male chimpanzees

Abstract

BackgroundMale members of primate species that form multi-male groups typically invest considerable effort into attaining and maintaining high dominance rank. Aggressive behaviors are frequently employed to acquire and maintain dominance status, and testosterone has been considered the quintessential physiological moderator of such behaviors. Testosterone can alter both neurological and musculoskeletal functions that may potentiate pre-existing patterns of aggression. However, elevated testosterone levels impose several costs, including increased metabolic rates and immunosuppression. Cortisol also limits immune and reproductive functions.MethodsTo improve understanding of the relationships between dominance rank, hormones and infection status in nonhuman primates, we collected and analyzed 67 fecal samples from 22 wild adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda. Samples were analyzed for cortisol and testosterone levels as well as intestinal parasite prevalence and richness. 1,700 hours of observation data were used to determine dominance rank of each animal. We hypothesized that dominance rank would be directly associated with fecal testosterone and cortisol levels and intestinal parasite burden.ResultsFecal testosterone (but not cortisol) levels were directly associated with dominance rank, and both testosterone and cortisol were directly associated with intestinal parasite richness (number of unique species recovered). Dominance rank was directly associated with helminth (but not protozoan) parasite richness, so that high ranking animals had higher testosterone levels and greater helminth burden.ConclusionsOne preliminary interpretation is that the antagonist pleiotropic effects of androgens and glucocorticoids place a cost on attaining and maintaining high dominance rank in this species. Because of the costs associated with elevated steroid levels, dominance status may be an honest signal of survivorship against helminth parasites.

Short‐term resource allocation during extensive athletic competition

“…As such, testosterone is an effective mediator of quality signalling due to the significant metabolic costs of a muscular physique (Andersson, 1994; Graffen, 1990; Zahavi, 1975), immunomudulation (Muehlenbein & Bribiescas, 2005; Muehlenbein & Watts, 2010; Muehlenbein, Cogswell, James, Koterski, & Ludwig, 2006), and the negative health effects of high levels of the hormone.…”

Intestinal parasite communities of six sympatric lemur species at Kirindy Forest, Madagascar

“…All fecal samples were processed using a modification of the formalin-ethyl acetate sedimentation technique, as described in Clough (2010). This technique is commonly used to recover helminth eggs from formalin-fixed fecal samples of wild primates (Muehlenbein and Watts, 2010;Pebsworth et al, 2012) and results in the sedimentation of eggs, larvae and protozoa on the bottom of the test tube during centrifugation (Ash and Orihel, 1987). Parasite stages were microscopically identified to genus level, if possible, based on morphological criteria following the key in Irwin and Raharison (2009).…”

“…They are herbivorous, feeding mainly on leaves, but incorporate flowers and fruit into their diet based on seasonal availability (Norscia et al, 2006). Being vertical clingers and leapers, they rarely descend to the ground and do not drink from waterholes, but rather they rely entirely on the water content of their diet and on dew present on trees (Kappeler and Fichtel, 2012).…”

Circadian Rhythms of Urinary Cortisol Levels Vary Between Individuals in Wild Male Chimpanzees: A Reaction Norm Approach

“…Chimpanzees are an interesting species to study repeatability of urinary cortisol excretion and urinary cortisol reaction norms as infants are nursed by their mothers for around 4 years and carried and cared for even longer (Boesch and BoeschAchermann, 2000), rendering maternal priming of the HPA axis possible. Factors affecting glucocorticoid levels, such as circadian rhythms (Muller and Lipson, 2003), dominance rank (e.g., Muller and Wrangham, 2004;Anestis, 2005;Anestis et al, 2006;Muehlenbein and Watts, 2010), social dynamics (e.g., Fraser et al, 2008;Emery Thompson et al, 2010;Wittig et al, 2016), and maternal care (Murray et al, 2016) are well-studied in this species. This allows for an informed decision on potential control factors in statistical models and a sound biological interpretation of different patterns.…”