Mating history shapes Wolbachia-induced cytoplasmic incompatibility and female fitness in an insect pest.

BACKGROUND: Maternally transmitted endosymbionts like Wolbachia and Cardinium are common in arthropods including many pest species. By inducing cytoplasmic incompatibility (CI), they can support sustainable pest management via population-suppression or replacement strategies. However, models underlying these approaches often neglect female remating and the pre- and post-copulatory mechanisms that influence sperm use and compatibility. In many species, females mate multiple times and may encounter both compatible and incompatible males, potentially altering CI expression and endosymbiont spread. We therefore tested how remating and mating order affect CI and reproductive fitness in Kelly's citrus thrips, Pezothrips kellyanus, a haplodiploid citrus pest naturally carrying either Cardinium alone (C) or both Cardinium and Wolbachia (CW). RESULTS: We found that CI depended strongly on mating history. When a C female first mated with an incompatible CW male, CI was strong, and a second mating with a compatible C male only restored approximately 21% of female offspring production. Conversely, when a C female first mated with a compatible C male and then with an incompatible CW male, CI was substantially weaker, consistent with first-male sperm precedence. Female fitness also varied with mating history; C females mated twice with CW males had the lowest fecundity, highest embryonic and post-embryonic mortality, and shortest survival. CONCLUSION: First-male sperm precedence limits restoration of female offspring production by a compatible mating following an incompatible mating. This may increase the fitness costs of accepting incompatible males in hosts with pre-copulatory mate discrimination. More broadly, remating and mate sequence can alter CI strength, affecting models of endosymbiont spread and endosymbiont-based pest management. © 2026 The Author(s). Pest Management Science published by John Wiley & Sons Ltd on behalf of Society of Chemical Industry.