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.