Scents for safe sex: a volatile sex pheromone promotes outbreeding in a parasitoid wasp with severe genetic load

When mating among genetically related individuals results in inbreeding depression, various behaviors and life-history traits evolve to favor outbreeding. Long-range sexual communication following natal dispersal is one such adaptation. In parasitoid wasps with single-locus complementary sex determination (sl-CSD), inbreeding increases the production of unviable or sterile diploid males. Mastrus ridens is such a species, with a genetic load underpinned by sl-CSD, combined with a high potential for sibmating because siblings emerge in close proximity from the same host and become sexually active shortly after emergence. With this context in mind, we investigated the mate-finding strategy of M. ridens using complementary behavioral, chemical, and electrophysiological approaches. Wind-tunnel bioassays and field experiments showed that males orient toward virgin females and, to a lesser extent, mated females. This attraction from a distance appeared to be the sole form of conspecific attraction. Chemical analyses using static and dynamic headspace sampling and solvent extracts, followed by GC-MS, revealed several potential pheromonal candidates, including methyl 6-methylsalicylate. This compound elicited reproducible antennal responses in males in GC-EAD recordings. Altogether, our results suggest that mate finding in M. ridens is guided by a volatile sex pheromone emitted by females, with methyl 6-methylsalicylate as one putative component. Such mate-finding mechanisms promote outbreeding and may explain the low proportion of unfit diploid males observed in natural populations. Surprisingly, chemical analyses suggested that males also emit this compound, whereas neither males nor females showed behavioral responses to males. This apparent discrepancy suggests that attraction may depend on a more complex pheromonal signal and opens further avenues for investigation.