Owner positional disadvantage in contests over mating prevents monopolization of females

The act of mating may render individuals vulnerable by inhibiting mobility and defence. While the consequences of this vulnerability for predation risk are well known, the implications for male–male contests over mating have been largely ignored. We examined the influence of vulnerability during mating by assessing the effectiveness of asymmetries in resource-holding potential (RHP) and subjective resource value (female mating status) in determining access to females in a resident–intruder scenario. In the earwig Euborellia brunneri, mating males are vulnerable to attack because they cannot use their armaments, and may risk breakage of their extremely elongated intromittent organs. We expected agonistic outcomes and ‘ownership’ of females to be decided entirely according to imposed asymmetries, since defeat normally induces a strong loser effect and flight responses in losers. Using behavioural assays of dyads of males contesting one female we show that, although small differences in RHP strongly affected agonistic outcomes, dominant males could not monopolize females. Through recurrent harassment, subordinate males exploited the vulnerability of mating opponents to break up copulations and generate mating opportunities. Dominant males also employed this tactic and were more effective at it. While female mating status affected resident mating duration and investment in conflict, only asymmetry in RHP affected fighting and mating outcomes. Resource owners in E. brunneri hence experience a positional disadvantage specific to a mating context. This previously unrecognized phenomenon may provide a proximate explanation for the taxonomically widespread occurrence of attacks during copulation and the avoidance thereof. ► Dominance predicted the winner of fights and increased relative mating duration. ► Dominance did not allow monopolization of females and mating. ► Subordinate males used harassment to generate mating opportunities. ► Mechanical armaments may be ineffective during copulation. ► Nonmating males exploited a positional disadvantage of mating opponents.