Harem-holding males do not rise to the challenge: androgens respond to social but not to seasonal challenges in wild geladas.

David J Pappano,Jacinta C Beehner

doi:10.1098/rsos.140081

Abstract

The challenge hypothesis has been enormously successful in predicting interspecific androgen profiles for vertebrate males. Nevertheless, in the absence of another theoretical framework, many researchers ‘retrofit’ the challenge hypothesis, so that its predictions also apply to intraspecific androgen comparisons. We use a wild primate, geladas (Theropithecus gelada), to illustrate several considerations for androgen research surrounding male contests that do not necessarily fit within the challenge hypothesis framework. Gelada society comprises harem-holding males (that can mate with females) and bachelor males (that cannot mate with females until they take over a harem). Using 6 years of data from known males, we measured androgens (i.e. faecal testosterone (fT) metabolites) both seasonally and across specific male contests. Seasonal androgen variation exhibited a very different pattern than variation resulting from male contests. Although harem-holding males had higher testosterone levels than bachelors across the year, bachelors had higher testosterone during the annual ‘takeover season’. Thus, harem-holding males did not ‘rise to the challenge’ exactly when needed most. Yet, androgen profiles across male contests indicated that both sets of males exhibit the expected fT rise in response to challenges. Results from male geladas also support the idea that the context before (e.g. male condition) and after (e.g. contest outcome) a contest are critical variables for predicting hormones and behaviour.

Highlights

For nearly a quarter of a century, the challenge hypothesis [1] has been the predominant paradigm for explaining short-term androgen responses to social challenges for male vertebrates [2,3]
Higher testosterone was associated with warmer days, more rainfall, younger age (β = −0.066, s.e. = 0.007, t = −8.80, p < 0.001) and leader male status (β = 0.116, s.e. = 0.033, t = 3.56, p < 0.01)
Geladas are not classified as seasonal breeders [44,45], there is a clear seasonal bias to male contests that escalate to takeovers

Summary

Introduction

For nearly a quarter of a century, the challenge hypothesis [1] has been the predominant paradigm for explaining short-term androgen responses to social challenges for male vertebrates [2,3]. This framework, originally developed for interspecific comparisons among temperate birds [1], predicts that social. Androgen levels can be up- and downregulated by the hypothalamic–pituitary gonadal axis as necessitated by competing mating and parenting demands (‘androgen responsiveness’) It follows, that androgen responsiveness should track both the breeding season (of the individual) and the social system (of the species). This broad pattern has been upheld using interspecific comparisons of seasonal androgen profiles in birds and fishes [2,3], but see [8], support deriving from mammalian species has been less conclusive [3]

Methods

Results

Discussion

Conclusion