Adaptive and maladaptive sex ratios in a pollinating fig wasp

Abstract

When a trait enhances fitness and arose as a result of natural selection, it is termed an adaptation. The optimization strategy employs selection thinking which makes the explicit assumption that the globally best trait will be fixed. Organisms, do not always respond optimally across all environments encountered as the strength of selection is finite. An excellent example of optimality is skewed sex ratios predicted by Hamilton's local mate competition (LMC) theory. It occurs when brothers compete in isolated groups for matings. Hamilton showed mathematically that in such groups, the unbeatable sex ratio is female-biased and this bias increase as the number of mothers that contribute to isolated patches decrease. One taxon that has been used to test LMC is the fig wasps. Fig wasps are haplodiploid, with unfertilized haploid eggs developing into males and fertilized diploid eggs into females. One or a few mothers crawl into a fig and lay all their eggs within, resulting in extreme local mate competition and sib mating. Sibmating increases relatedness of the daughter to the mother as genes from the father are identical by descent to the mother. Relatedness to sons is unaffected. This relatedness asymmetry selects for even more female-biased ratios. Thus, an extra daughter instead of a son will decrease local mate competition, and an extra daughter provides a higher fitness to the mother due to relatedness. There are two mechanisms that can explain how fig wasps sex ratios are adjusted to the number of mothers in a patch. First, a byproduct of a constraint on clutch size, where mothers lay all or most of their sons first, followed by daughters. Mothers do not change their behaviour, but limited oviposition space prevents them from laying all their eggs destined to be daughters. Second, a facultative strategy where mothers sense other ovipositing females and adjust the number of sons they lay. We studied sex ratio adjustments in Ceratosolen galili, the cuckoo wasp that oviposits in Ficus sycomorus, which is pollinated by C. arabicus. Different numbers of C. galili foundresses and a mix of these species were entered into figs to study the mechanism of sex ratio adjustment. We found that mothers adjust their sex ratios facultatively when another foundress is present, and there is no constraint on clutch size. However, if the fig becomes saturated with eggs from three foundresses, the mothers’ clutches are constrained, and sex ratios are also adjusted as a result of a byproduct. Since these foundress numbers are frequently observed in nature, selection effectively solved this problem. However, C. galili mothers often share figs with C. arabicus and C. galili should not adjust their sex ratios in their presence of C. arabicus. However, C. galili erroneously adjust their sex ratio facultatively in the presence of C. arabicus. Erroneous adjustment can be considered a maladaptation. Interestingly, the lack of pollination behaviour of C. galili is not sanctioned by reduced offspring survival.