Nevertheless sex persisted: facultative sex persists despite high costs in a sexually polymorphic aphid parasitoid

The prevalence of sexual reproduction has long puzzled evolutionary biologists. This is because of the ‘twofold cost of sex’, or, more accurately, ‘the twofold cost of males’; an individual that reproduces sexually is expected to invest half its resources in producing male offspring, but an equivalent asexual individual will produce all daughters and so should have twice as many grandoffspring. To understand how sex coexists with asexual reproduction despite the twofold cost I assayed behaviour and offspring production of sexual and asexual females of the sexually polymorphic aphid parasitoid Lysiphlebus fabarum . To fully measure the costs of sex (including the costs of mating and exposure to males) I exposed half of these females to sexual males. I found that when males were available, asexual females are often facultatively sexual; they readily mate with males and producee offspring with paternal genetic contributions. Sexual females did not appear to be limited in their fitness by the ‘twofold cost of males’; although they produced sons, they also produced the same number of daughters as asexual females because their overall offspring production was higher. Instead, the main cost of sex was increased reproductive failure, particularly when sex was facultative. Stable coexistence of both reproductive modes in L. fabarum may occur because this main cost of sex is paid by both asexual (under facultative sex) and sexual females. Coexistence and interbreeding with male-producing sexuals may be the very thing that has allowed asexual L. fabarum lineages to persist in the long-term; ensuring sufficient genetic variation for adaptation through occasional facultative sex, as well as reducing the costs, such as low fecundity, that accumulate under obligate asexual reproduction.