Asymmetric Assortative Mating Behaviour Reflects Incomplete Pre‐zygotic Isolation in the Nasonia Species Complex

Abstract

Preference of con‐ over heterospecific mates leading to assortative mating can substantially contribute to pre‐zygotic reproductive isolation and prevent fitness losses if post‐zygotic hybridization barriers already exist. The jewel wasp genus Nasonia displays quite strong and well‐studied post‐zygotic reproductive isolation due to a ubiquitous Wolbachia infection causing cytoplasmic incompatibility between different species. Pre‐zygotic isolation, however, has received far less research attention in this model organism, especially concerning the mechanisms and criteria of mate choice. In the present study, we analysed mate rejection and mate acceptance rates in cross‐comparisons between all four Nasonia species. We put emphasis on observing which sex is more likely to interrupt interspecific matings and how discriminatory behaviour varies across the different species in all possible combinations. We found an asymmetric distribution of assortative mating among the four Nasonia species that appears to be highly influenced by the respective combinations of sex and species. Females appeared to be the main discriminators against heterospecific mating partners, but interestingly, we could also detect mate discrimination and rejection behaviour in males, a widely neglected factor in research on mating behaviour in general and on Nasonia in particular. Moreover, the asymmetry in the assortative mating behaviour was partially reflective of sym‐ or allopatric distributions of natural Nasonia populations.

The chemical basis of mate recognition in two parasitoid wasp species of the genus Nasonia

“…In contrast to our study, Buellesbach et al. () found no discrimination of N. giraulti males against N. vitripennis females. However, they investigated only male mate rejection rates, possibly overlooking more subtle indicators of mate discrimination such as time effects in courtship and copulation.…”

“…These results pointed to a seemingly non‐adaptive preference for heterospecific over conspecific mating partners in N. giraulti males, which is somewhat difficult to explain from an evolutionary perspective. The findings also raise questions relating to observations from other studies, where N. giraulti males readily courted and mated con‐ and heterospecific females equally (live females: Buellesbach et al., ; dead females: Ruther et al., ). A shift from chemical communication to other modes of communication, e.g., via behavioral, tactile, or acoustic cues, has been suggested for N. giraulti (Buellesbach et al., ).…”

“…In the parasitoid wasp Nasonia vitripennis Walker (Hymenoptera: Pteromalidae), female‐derived CHCs elicit courtship behavior in males, whereas male‐derived CHCs do not (Steiner et al., ). Males of N. vitripennis , however, do not discriminate between con‐ and heterospecific females and engage equally in mounting and courtship activities with females of different Nasonia species (Giesbers et al., ; Buellesbach et al., ). Females of N. vitripennis on the other hand mate more often with con‐ than with heterospecific males (Bordenstein & Werren, ; Giesbers et al., ; Buellesbach et al., ; Ruther et al., ).…”

“…Males of N. vitripennis , however, do not discriminate between con‐ and heterospecific females and engage equally in mounting and courtship activities with females of different Nasonia species (Giesbers et al., ; Buellesbach et al., ). Females of N. vitripennis on the other hand mate more often with con‐ than with heterospecific males (Bordenstein & Werren, ; Giesbers et al., ; Buellesbach et al., ; Ruther et al., ). A possible mechanism for females to recognize conspecific males is the males’ courtship behavior, which consists of a stereotypic sequence of distinct behavioral elements.…”

Diet, Gut Microbes and Host Mate Choice

“…[2,[54][55][56][57] These effects benefit the Wolbachia as they promote its spread via maternal transmission through the elimination, in various ways, of male hosts from the population. Wolbachiainduced uni-directional CI is a particular focus for understanding host biology because, in theory, CI can lead to host RI, [58][59][60] because CI increases the fitness of infected females relative to uninfected females, and hence may select Wolbachia-derived mechanisms for avoiding mating with uninfected females.…”