Same-sex sexual behaviours in a wasp despite sex recognition cues: the broad mating filter hypothesis

Abstract

Same-sex sexual behaviour (SSB) in animals, once considered an evolutionary dead end, is surprisingly widespread, particularly among male insects. These behaviours may arise from either adaptive or non-adaptive processes. Over shorter timescales, SSB can occur when courtship costs are low or when missing a mating opportunity is costly, leading to a reduced behavioural threshold for courtship--a "broad mating filter," as predicted by threshold acceptance theory. We investigated SSB in males of the parasitoid wasp Venturia canescens (Hymenoptera: Ichneumonidae), a species where encounters are infrequent and male courtship is energetically not costly. We hypothesised that males exhibit a broad mating filter, accepting conspecifics for courtship regardless of sex. First, behavioural assays assessed whether SSB correlated with higher reproductive success. Second, we compared cuticular hydrocarbon (CHC) profiles between sexes, as these compounds may serve as cues for sex recognition. Our chemical analyses revealed clear quantitative CHC differences between males and females, indicating potential for sex recognition. Nonetheless, 18% of males displayed SSB, and these behaviours had no detectable effect on either courting or mating success. Moreover, males receiving SSB did not experience any reproductive advantage. Our findings support the hypothesis of a broad mating filter in V. canescens males. In this species, where conspecific encounters are rare, SSB appears to arise from reduced discrimination rather than adaptive benefits, consistent with a low-cost courtship strategy and high opportunity costs of missed mating events.