Testes size, testosterone production and reproductive behaviour in a natural mammalian mating system

1. Testosterone (T) is a key mediator in the expression of numerous morphological and behavioural traits in mammals, but the factors underlying individual variation in circulating T levels are poorly understood. 2. The intimate structural integration of sperm and T production within the testes, alongside the dependency of sperm production on high levels of T, suggests that T requirements for spermatogenesis could be an important driver of individual differences in T. 3. To test this hypothesis, we examine how male capacity for sperm production (as indicated by their testes size) is associated with T levels in a feral population of Soay sheep, resident on St. Kilda, Scotland, during their rutting season. 4. We found a strong positive relationship between an individual's testes size (as measured before their seasonal enlargement) and the levels of circulating T during their rut, suggesting that T requirements for spermatogenesis has a prominent influence on the production of this androgen. 5. In contrast, body condition and competitive ability did not independently predict T levels, findings that are inconsistent with conventional 'condition-dependent' and 'challenge' hypotheses of T production. 6. This influence of male's capacity for sperm production on T appeared to be substantial enough to be biologically relevant, as testes size also predicted male aggression and mate-seeking behaviour. 7. Our results suggest that a male's inherent capacity for sperm and T production is tightly phenotypically integrated, with potential consequences for a wide range of other T-mediated reproductive traits.