Optional sex harms the wasp Lysiphlebus fabarum

The parasitoid wasp Lysiphlebus fabarum, known for attacking aphids on crops in Europe, has an intriguing biological peculiarity. Some of its populations reproduce exclusively by parthenogenesis — a form of asexual reproduction that does not require males. Others reproduce sexually. But among them, there is a group that can alternate between the two modes.

This behavior, known as facultative sex, has been considered by evolutionists as a way to combine the genetic benefits of sex with the reproductive efficiency of parthenogenesis.

However, a recent study suggests that this flexibility can be a burden. Females that usually reproduce without males but occasionally mate suffer significant losses in reproductive success. Instead of “having the best of both worlds,” they appear to reap the worst.

Rebecca Boulton of the University of Stirling investigated seven asexual lines and one sexual population of the species. Females were either exposed to males or kept virgin. In both cases, they were given aphids as hosts for parasitism.

Those that mated were evaluated to determine whether they actually used sperm to fertilize their eggs. The reproductive performance of these females and their daughters was then monitored for two generations.

The results were clear. Sexual reproduction by normally asexual females resulted in a higher rate of reproductive failure. They produced fewer "mummies"—dead aphids with developing wasp larvae—and fewer adults emerged from these. The daughters of these females were also less successful at parasitizing new aphids.

Contrary to expectations, the classic advantage of asexual reproduction — avoiding the so-called "male cost", that is, producing only daughters — was not confirmed. Sexual females produced as many daughters as asexual females. The reason? Higher fertility of sexual females. Even investing in children of both sexes, they managed to keep the number of daughters at a similar level.

Furthermore, there were additional unforeseen costs to facultative sex. Some of the hybrid offspring—the result of genetic mixing between asexual and sexual lineages—may suffer from genetic problems such as triploidy or outcrossing depression between genetically distant individuals. The hypothesis of "genetic drift," where coadapted genetic combinations fall apart at random, has gained traction to explain the failure of the offspring of females that crossed.

Despite being reproductively inefficient, sexual behavior remained present in all seven asexual lineages tested, even after hundreds of generations without contact with males.

This persistence raises the question: why have costly sexual traits, such as copulation acceptance and sperm use, not been eliminated by natural selection?

One hypothesis involves the "bet against risk" strategy. At the end of summer, populations of L. fabarum increase rapidly before a seasonal collapse. At this stage, encountering males becomes more likely and the environment more unstable. Sex, in this context, can generate genetic diversity useful for surviving the winter. The immediate cost of lower fertility may be offset by a greater chance of future adaptation.

Another important factor is the social and behavioral structure of the species. Wasps tend to parasitize in the same place where they emerged, which favors crossbreeding between siblings. Inbreeding, in this case, can reduce the negative effects of crossbreeding between very different lineages, as would be the case of an asexual female mating with a distantly sexual male.

The study also points out that the occurrence of sex between asexual females and sexual males — or even between rare males generated by parthenogenesis — can maintain the genetic diversity observed in asexual populations of L. fabarum.

More information at doi.org/10.1098/rsos.242162