The interplay between social rank, physiological constraints and investment in courtship in male spotted hyenas

In many animal societies, dominant males have a higher reproductive success than subordinate males. The proximate mechanisms by which social rank influences reproductive success are poorly understood. One prominent hypothesis posits that rank-related male attributes of attractiveness and fighting ability are the main mediators of reproductive skew. Yet, empirical evidence in support of this hypothesis is limited. An alternative hypothesis emphasises the inherent social dimension of dominance relationships and posits that the relationship between male social rank and reproductive success is mediated by the physiological costs of male?male competition. This has not been tested in systems in which the two hypotheses can be disentangled. We investigated the interplay between male social rank, physiological costs and male investment in social and sexual activities. We used measurements of faecal glucocorticoid metabolite concentrations (fGMC) as biomarkers of physiological costs and long-term behavioural data of 319 males in free-ranging spotted hyenas Crocuta crocuta, a species in which male access to females and reproductive success do not depend on physical attributes. When males courted females and interacted with male competitors, low-ranking males had higher fGMC than high-ranking males. In contrast, fGMC did not vary with social rank when males were alone or when they courted females and competitors were absent. Low-ranking males minimised their exposure to physiologically costly intrasexual competition; they spent more time alone and less time engaging in social and sexual activities than did high-ranking males. They also invested less than high-ranking males in courting the most contested and highest-quality females. Our findings demonstrate that the physiological costs of intrasexual competition in male spotted hyenas vary with social rank and shape behavioural trade-offs between the allocation of time and physiological resources to social integration, reproduction and self-maintenance. Our study suggests that physiological and social constraints play a pivotal role in the emergence of rank-related male reproductive success. The study provides insights into how the social organisation and breeding system shape physiological constraints and patterns of reproductive skew within and between species. A free Plain Language Summary can be found within the Supporting Information of this article