Symbiont-mediated shifts in cuticular hydrocarbon profiles reduce female attractiveness after mating

Abstract

Males can influence future mating interactions of females after copulation by changing female signals that subsequent males will encounter. In insects, such effects commonly involve cuticular hydrocarbons (CHCs), but whether heritable microbial symbionts contribute to post-mating chemical signalling remains largely unknown. Kelly's citrus thrips, Pezothrips kellyanus, provides an ideal system to address this question because reproductive compatibility is shaped by common arthropod endosymbionts. Across P. kellyanus populations, Cardinium occurs in almost all individuals whereas Wolbachia varies in prevalence and appears to spread by cytoplasmic incompatibility (CI). Yet, females with only Cardinium (C) avoid incompatible males carrying both Cardinium and Wolbachia (CW), and this discrimination is linked to the distinct CHC profile of CW males. Here, we tested whether this endosymbiont-associated male perfume persists on females beyond copulation by altering the female CHC profile and subsequent male mating behaviour. Using behavioural assays and GC-MS-based CHC profiling, we found that, independent of female endosymbiont association, females first mated with CW males received fewer antennal contacts and mating attempts from subsequent C males. Furthermore, mating remodelled female CHC profiles, while mating with CW males produced a distinctive post-mating chemical signature. Most notably, tridecane, previously detected only in CW males, occurred exclusively in females mated with CW males. Our findings show that endosymbionts can alter mated female CHCs and influence future sexual communication between male and female hosts. These findings reveal a previously unrecognised post-mating route through which endosymbionts reshape sexual communication, with potential consequences for reproductive compatibility and symbiont transmission dynamics.