Unravelling complex associations between testosterone and parasite infection in the wild

Abstract

Summary1. Testosterone has emerged as an important mechanism linking variation in male reproductive behaviour to parasite infection in vertebrates, and there are numerous pathways by which testosterone can influence infection risk, particularly in free-living animals. 2. The immunocompetence handicap hypothesis posits that the positive effects of testosterone on sexual signalling and behaviour are traded off with negative effects on immune function. While this obligate trade-off may sometimes explain the association between testosterone and parasite infection, testosterone-parasite relationships may also be mediated by correlated changes in stress, condition and exposure to parasites. 3. In this study, we explored associations between testosterone and reproductive behaviour, immune function and parasitism in free-living Grant's gazelle (Nanger granti). In particular, we examined how stress (glucocorticoids), behaviour and condition might mediate associations between testosterone, immunity and parasitism. 4. We found that variation in endogenous testosterone in male gazelle was correlated with mating behaviour in terms of sexual signal intensity (horn size) and resource-holding potential (territoriality). We also showed that these same levels of testosterone were associated with immunity and parasite infection, but associations between testosterone, immunity and parasitism were complex. Testosterone was negatively associated with adaptive immunity, but positively associated with innate immunity. Relationships between testosterone and parasitism varied for different parasites. 5. Our results suggest that the effects of testosterone on male immunity are not universally suppressive and that immunoenhancement may also occur. In addition, testosterone-parasite relationships vary depending on the parasite, most likely due to the opposing effects of testosterone on different aspects of immunity and indirect effects on parasite exposure mediated by changes in behaviour.

Role of testosterone and photoperiod on seasonal changes in horn growth and sperm variables in the Iberian ibex: a model for polygynous wild bovids

“…Therefore, it would be expected that dominant males with greater horn development and sperm quality show higher testosterone levels during the spring period of horn growth. Although Decristophoris et al (2007) found no relationship between rutting season testosterone levels and dominance in Alpine ibex (Capra ibex), most studies in wild ruminants, such as Grant's gazelle (Nanger granti) and bighorn sheep, have found positive relationships between these variables (Pelletier et al 2003, Ezenwa et al 2012.…”

Androgens predict parasitism in female meerkats: a new perspective on a classic trade-off

“…concentrations in female meerkats (Suricata suricatta)-a species in which all females naturally experience raised androstenedione and T [12]-relate to parasite loads in a manner similar to that experienced by many males [4][5][6][7][8].…”

Reciprocal relationships between behaviour and parasites suggest that negative feedback may drive flexibility in male reproductive behaviour

“…Since territoriality and breeding occur year round at the study site [18], males were monitored continuously from the month after capture (starting in either March or September 2009) through to June 2011, or until the subject was lost from the study due to death or emigration from the study site. At each sighting, male status was recorded as territorial (T), bachelor (B), or unknown (U).…”

“…Animals were captured using drive nets on the ground (January -Feburary) or a handheld net gun fired from a helicopter (August), fitted with unique colour ear tags, and then released after sample collection and morphological measurements [18]. Individuals were anaesthetized to facilitate age estimation via tooth wear.…”