Mass killing by female soldier larvae is adaptive for the killed male larvae in a polyembryonic wasp.

Self-sacrifice is very rare among organisms. Here, we report a new and astonishing case of adaptive self-sacrifice in a polyembryonic parasitic wasp, Copidosoma floridanum. This wasp is unique in terms of its larval cloning and soldier larvae. Male clone larvae have been found to be killed by female soldier larvae, which suggests intersexual conflict between male and female larvae. However, we show here that mass killing is adaptive to all the killed males as well as the female soldiers that have conducted the killing because the killing increases their indirect fitness by promoting the reproduction of their clone sibs. We construct a simple model that shows that the optimal number of surviving males for both male and female larvae is very small but not zero. We then compare this prediction with the field data. These data agree quite well with the model predictions, showing an optimal killing rate of approximately 94-98% of the males in a mixed brood. The underlying mechanism of this mass kill is almost identical to the local competition for mates that occurs in other wasp species. The maternal control of the sex ratio during oviposition, which is well known in other hymenopterans, is impossible in this polyembryonic wasp. Thus, this mass kill is necessary to maximize the fitness of the female killers and male victims, which can be seen as an analogy of programmed cell death in multicellular organisms.

Sexual complementarity between host humoral toxicity and soldier caste in a polyembryonic wasp.

Defense against enemies is a type of natural selection considered fundamentally equivalent between the sexes. In reality, however, whether males and females differ in defense strategy is unknown. Multiparasitism necessarily leads to the problem of defense for a parasite (parasitoid). The polyembryonic parasitic wasp Copidosoma floridanum is famous for its larval soldiers' ability to kill other parasites. This wasp also exhibits sexual differences not only with regard to the competitive ability of the soldier caste but also with regard to host immune enhancement. Female soldiers are more aggressive than male soldiers, and their numbers increase upon invasion of the host by other parasites. In this report, in vivo and in vitro competition assays were used to test whether females have a toxic humoral factor; if so, then its strength was compared with that of males. We found that females have a toxic factor that is much weaker than that of males. Our results imply sexual complementarity between host humoral toxicity and larval soldiers. We discuss how this sexual complementarity guarantees adaptive advantages for both males and females despite the one-sided killing of male reproductives by larval female soldiers in a mixed-sex brood.

Male soldiers are functional in the Japanese strain of a polyembryonic wasp.

Polyembryonic parasitoids clonally produce sterile soldier larvae in both sexes. Female soldier larvae of Copidosoma floridanum defend their siblings and host resources against heterospecific competitors as well as conspecific male embryos that results in female biased sex ratios. However, the male soldiers of the USA strain exhibit no aggressive behaviors against them, suspected to be a secondary loss of male defense function in the course of evolution. From vitro and vivo experiments, we have found functional male soldiers in the Japanese strain of C. floridanum. In vitro experiments, male soldiers exhibit aggressions against four larval competitors, though aggressiveness is much weaker than that of female soldiers. In vivo experiments, heterospecific competitors are equivocally excluded in both male and female broods. Our findings support the idea that male soldiers have evolved primarily to defend against heterospecific competitors. Further experiments against conspecific embryos may be able to confirm this hypothesis.

Physiological suppression of the larval parasitoid Glyptapanteles pallipes by the polyembryonic parasitoid Copidosoma floridanum.

Precocious larvae, clonally produced together with reproductive siblings in the polyembryonic parasitoid Copidosoma floridanum, are known to physically attack competitors in multiparasitized hosts. In this study, we show that physiological suppression by C. floridanum, as well as precocious larval activity, causes death of the larval parasitoid Glyptapanteles pallipes. Approximately 70% of the hosts multiparasitized by C. floridanum and G. pallipes produced C. floridanum offspring, irrespective of the interval of multiparasitism. G. pallipes eggs or larvae died even in multiparasitized hosts that did not contain precocious larvae of C. floridanum. An injection of C. floridanum-parasitized or multiparasitized-host hemolymph into G. pallipes singly-parasitized hosts paralyzed almost all G. pallipes larvae within 70 h. In vitro analysis showed that the hemolymph factor toxic to G. pallipes eggs and larvae was present in C. floridanum-parasitized hosts through their larval stages. Heating or proteinase treatment reduced its toxicity, suggesting that the factor is a protein.