How does testosterone impact immune function, parasite load, and survival?

Testosterone regulates many aspects of behavior, morphology, and physiology that contribute to a male’s reproductive success. However, elevated levels of circulating testosterone can also reduce a male’s fitness if they have detrimental effects on survival (Fig. 1). For example, increased territorial aggression can expose a male to greater risk of injury during combat. Likewise, an increase in calling or courtship behavior could render a male more susceptible to predators. Testosterone can also have less obvious physiological effects, such as the suppression of immune function, thereby reducing a male’s ability to fight pathogens or parasites.

Testosterone and parasitism. One detrimental effect of testosterone that occurs repeatedly in different lizard species is an apparent increase in parasitism by trombiculid mites (Figs. 1, 2). In striped plateau lizards, males have substantially higher testosterone levels than females and, during the peak of the breeding season, males harbor nearly twice as many parasitic mites as females (Fig. 2a). When males are castrated, their levels of parasite infestation drop, but when castrated males are treated with testosterone, their levels of parasitism increase (Fig. 2b). Mite parasitism may impose a substantial energetic cost, as levels of parasitism are negatively correlated with growth rate across these treatment groups (Fig. 2c).

Figure 1. In male eastern fence lizards, testosterone stimulates (A) endurance, as measured on a motorized treadmill, (B) movement, reflecting increased patrolling of home ranges, and (C) home range area, which correlates with reproductive success. However, testosterone also (D) increases levels of mite parasitism, (E) reduces growth rate, and (F) may reduce survival, which is slightly higher in castrated males. CAST = castration + placeo implant, CON = sham surgery + placebo implant, TEST = castration + testosterone implant. Modified from John-Alder et al. (2009).

Related Papers

Cox, R.M., D.S. Stenquist*, J.P. Henningsen, and R. Calsbeek. 2009. Manipulating testosterone to assess links between behavior, morphology and performance in the brown anole, Anolis sagrei. Physiological and Biochemical Zoology 82: 686-698.

John-Alder, H.B., R.M. Cox, G. Haenel, and L. Smith. 2009. Hormones, performance and fitness: natural history and endocrine experiments on a lizard (Sceloporus undulatus). Integrative and Comparative Biology 49:393-407.

Cox, R.M. and H.B. John-Alder. Increased mite parasitism as a cost of testosterone in male striped plateau lizards, Sceloporus virgatus. Functional  Ecology 21: 327-334.

Cox, R.M., S.L. Skelly, and H.B. John-Alder. Testosterone inhibits growth of juvenile male eastern fence lizards (Sceloporus undulatus): implications for energy allocation and sexual size dimorphism. Physiological and Biochemical Zoology 78: 531-545.

Figure 2. (A) Male striped plateau lizards suffer higher levels of mite parasitism than females during the spring breeding season, when their testosterone levels are elevated. (B) Castration reduces parasitism, but testosterone increases parasitism in castrated males. (C) Across treatment groups, males with higher levels of mite parasitism have lower growth rates. Modified from Cox and John-Alder (2007).

Testosterone and immune function. Why do males suffer increased parasitism as a consequence of elevated testosterone levels? One possibility is that testosterone suppresses immune function. Dartmouth undergraduate Derek Stenquist tested this hypothesis in the brown anole by measuring immune function in males that received castration and testosterone-replacement treatments. Although his study did not reveal an effect of testosterone on one measure of immune function (swelling response to a novel mitogen), he did find a negative relationship between growth and immune function that was particularly strong in males with experimentally elevated testosterone levels.