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

TL;DR

Common bacteria in insects influence mating choices by altering chemical signals, helping females avoid infertile pairings.

Contribution

Shows how endosymbionts like Cardinium and Wolbachia shape sexual selection through chemical communication in citrus thrips.

Findings

Females with only Cardinium prefer compatible males to avoid Wolbachia-induced infertility.

Males with different endosymbionts have distinct chemical profiles, aiding female recognition.

Endosymbiont interactions affect host mating behavior and population dynamics.

Abstract

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.

Sexual selection drives the evolution of traits that enhance reproductive success. While such traits are shaped by genetic and environmental factors, microbial symbionts can also play a role. Our study demonstrates that common maternally transmitted endosymbionts of arthropods mediate sexual selection by affecting mating preferences and chemical communication of their host. Cardinium enabled females to preferentially mate with compatible males thereby avoiding the risk of infertility arising from matings with incompatible males carrying Wolbachia. The males’ endosymbiont association status was linked to distinct cuticular hydrocarbon profiles, which may assist females to recognize their compatibility. Such multipartite interactions are important as they can affect the population dynamics of both endosymbionts and hosts, as well as the effectiveness of endosymbiont-based pest control.

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