Common endosymbionts influence host sexual selection by shaping mating preferences via altered chemical communication

Maternally transmitted endosymbionts of arthropods are common and phylogenetically diverse. Several bacteria, including Wolbachia and Cardinium, have independently evolved the ability to induce cytoplasmic incompatibility (CI) limiting the reproduction in females lacking the endosymbionts carried by their mates. While promoting endosymbiont spread, CI is costly to endosymbiont-free females. Such host-endosymbiont conflicts are expected to affect host mating preferences, yet this has scarcely been studied in hosts carrying multiple, potentially competing, endosymbionts. We investigated mate choice and chemical communication in a significant pest of citrus, Kelly’s citrus thrips (Pezothrips kellyanus), naturally carrying CI-inducing Cardinium and Wolbachia. Unlike females with both endosymbionts (CW) that had no preference for males with particular endosymbiont associations, females with only Cardinium (C) preferred compatible C and endosymbiont-free males over incompatible CW males. In contrast, endosymbiont-free females showed no preference, despite experiencing similar CI risks when facing incompatible C and CW males. Male mating success, however, mostly depended on female receptivity and not on endosymbiont association. Furthermore, chemical analyses revealed that males with different endosymbiont associations had distinctly different cuticular hydrocarbon (CHC) profiles, with the CHC profile of CW males markedly including tridecane, a compound known to influence animal behavior. The results indicate that Cardinium enables females to avoid Wolbachia-induced CI based on the distinct chemical cues of incompatible males. Our findings highlight the role of common endosymbionts and their interactions in sexual selection through their effects on chemical and behavioral traits of hosts, emphasizing the importance of these factors in endosymbiont and host population dynamics, as well as endosymbiont-based pest control strategies.