Pheromone Diversification and Age-Dependent Behavioural Plasticity Decrease Interspecific Mating Costs in <i>Nasonia</i>

<div><p>Interspecific mating can cause severe fitness costs due to the fact that hybrids are often non-viable or less fit. Thus, theory predicts the selection of traits that lessen reproductive interactions between closely related sympatric species. Males of the parasitic wasp <i>Nasonia vitripennis</i> differ from all other <i>Nasonia</i> species by an additional sex pheromone component, but the ecological selective forces underlying this pheromone diversification are unknown. Here we present data from lab experiments suggesting that costly interspecific sexual interactions with the sympatric species <i>N. giraulti</i> might have been responsible for the pheromone evolution and some courtship-related behavioural adaptations in <i>N. vitripennis.</i> Most <i>N. giraulti</i> females are inseminated already within the host, but <i>N. giraulti</i> males still invest in costly sex pheromones after emergence. Furthermore, they do not discriminate between <i>N. vitripennis</i> females and conspecifics during courtship. Therefore, <i>N. vitripennis</i> females, most of which emerge as virgins, face the risk of mating with <i>N. giraulti</i> resulting in costly all-male broods due to <i>Wolbachia</i>-induced cytoplasmic incompatibility. As a counter adaptation, young <i>N. vitripennis</i> females discriminate against <i>N. giraulti</i> males using the more complex conspecific sex pheromone and reject most of them during courtship. With increasing age, however, <i>N. vitripennis</i> females become less choosy, but often compensate mating errors by re-mating with a conspecific. By doing so, they can principally avoid suboptimal offspring sex ratios, but a microcosm experiment suggests that under more natural conditions <i>N. vitripennis</i> females cannot completely avoid fitness costs due to heterospecific mating. Our study provides support for the hypothesis that communication interference of closely related sympatric species using similar sexual signals can generate selective pressures that lead to their divergence.</p>