Evolutionary aspects of the parasitoid life strategy, with a particular emphasis on fly–spider interactions

Parasitoids are significant ecological elements of terrestrial food webs and have evolved within seven insect orders. Interestingly, however, associations with spiders as hosts have evolved only in two insect orders, Diptera and Hymenoptera. Here, we summarize various aspects of host utilization by dipteran flies with an emphasis on associations with spiders. Our synthesis reveals that spider flies (family Acroceridae) have evolved a unique life strategy among all the parasitoid taxa associated with spiders, in which koinobiont small-headed flies utilize an indirect oviposition strategy. This indirect oviposition in spider flies is inherited from Nemestrinimorpha ancestors which appeared in the Late Triassic and is characterized by the evolution of planidial larvae. Further, we discuss the advantages and disadvantages of indirect oviposition in spider flies. On the one hand, indirect oviposition allows the fly to avoid contact/wrestling with spider hosts. On the other hand, larval survival is low because the planidium must actively seek out and infect a suitable host individually. The risk of failure to find a suitable spider host is offset by the fly’s extremely high fecundity.