Do female parasitoid wasps recognize and adjust sex ratios to build cooperative relationships?

Abstract

Sex allocation theories provide excellent opportunities to investigate not only the extent to which individuals’ behaviour is adaptive, but also how they use relevant information for their decision‐making. Here, we investigated whether female parasitoid wasps recognize the sex ratios of other females and adjust their laying sex ratios accordingly. Specifically, we tested the prediction of reciprocal cooperation over sex allocation. Theory predicts more female‐biased (cooperative) sex ratios than in the interest of individual benefit, when a restricted number of ovipositing females interact for a long period and their offspring mate within the natal patch. This is because the female‐biased sex ratio reduces competition for mates among the male offspring of the females and increases the overall reproductive productivity of the patch. In this case, females would be expected to respond to more even (noncooperative) sex ratios by others and to retaliate by also producing a less female‐biased sex ratio to avoid exploitation by defectors. However, contrary to this prediction, our experiment using a sterile male technique showed that female Melittobia australica did not change their offspring sex ratios in response to the sex ratios produced by other females. This suggests that their extremely female‐biased sex ratios cannot be explained by reciprocity. A meta‐analysis of studies examining sex recognition ability in parasitoid wasps also did not support the predicted pattern of relevant sex ratio adjustment, suggesting that parasitoid females do not possess this ability. Here, we discuss the conditions necessary for the evolution of reciprocity linked to recognition ability.

Mutually beneficial host exploitation and ultra-biased sex ratios in quasisocial parasitoids

“…While this theory provides a candidate alternative explanation for S. harmandi sex ratios, for it to operate foundresses would have to recognize the sex ratio of eggs on the host and to respond by adjusting their own sex allocation decisions (a form of policing against cheating by some foundresses laying higher proportions of male eggs48); hymenopteran parasitoids generally do not have this ability53 and the egg stage of S. harmandi clutches is short relative to the prolonged period of brood tending through the larval stages1617. Although the sex of developing larvae may be more readily detectable by tending foundresses53, offspring mortality was unrelated to foundress number in S. harmandi so it does not seem that infanticide is common (see also Hu et al 161154), making post-ovipositional sex ratio adjustment of S. harmandi brood sex ratios a less likely explanation for sex ratio bias than LRE, although both selective mechanisms could potentially operate simultaneously.…”

“…However, these may be tempered by mutual policing and/or by foundress–foundress relatedness5255, especially since in some bethylids adults can recognize kin57 probably using variation in cuticular hydrocarbon profiles58. Close relatedness between foundresses may be enhanced by codispersal and foraging by females from a given natal patch34 and would be expected to select for more greatly female-biased sex ratios937535960. Cofoundress relatedness, which will be highest when females derive from broods produced by fewer mothers61, should also select, via inclusive fitness gains, for altruistic brood care7, and this may explain why female S. harmandi that have not laid eggs do not commit ovicide1617.…”

INEXPLICABLY FEMALE-BIASED SEX RATIOS INMELITTOBIAWASPS

“…S2). We obtained a sufficient number of males from the surrogate females using a sterile male technique with 60 Co gamma ray irradiation, in which a female mated with a normal male and subsequently with an irradiated male produced approximately ∼22% males with unchanged clutch size (Abe and Kamimura ). We confirmed that males produced by this technique could fertilize females, which subsequently produced offspring, with no differences from normal males (J. Abe, unpubl.…”

Development of microsatellite markers and estimation of inbreeding frequency in the parasitoid wasp Melittobia

“…Because their hosts include species commercially important for pollination management, such as Osmia and Megachile bees567, honey bees48, and bumblebees, in which the parasitoid invades mass-rearing factories and cause immense damage on the colonies67910, Melittobia is feared as one of the most destructive natural enemies and is capable of causing enormous economic losses. At the same time, Melittobia exhibits a number of interesting traits that attract evolutionary biologists34, which include courtship behavior1112, sex allocation13141516, lethal combat among males171819, female dispersal dimorphism2021, female cooperative dispersal22 and a mating system in which mothers mate with their sons23.…”

“…Although some molecular techniques and markers were applied for Melittobia 1230, only a single microsatellite marker is available in this genus until now17, which was used for behavioral studies in the laboratory1415172329. The identification of an extensive panel of microsatellite loci with more polymorphism will facilitate investigations of the population structure and genetic relationship between wasps in natural field populations.…”