Box 13.1. Viruses, wasp parasitoids, and host immunity
In certain endoparasitoid wasps in the families Ichneumonidae and Braconidae, the ovipositing female wasp injects the larval host not only with her egg(s), but also with accessory gland secretions and substantial numbers of viruses (as depicted in the upper drawing for the braconid Toxoneuron (formerly Cardiochiles) nigriceps, after Greany et al. 1984) or virus-like particles (VLPs). The viruses belong to a distinct group, the polydnaviruses (PDVs), which are characterized by the possession of multipartite double-stranded circular DNA. PDVs are transmitted between wasp generations through the germline. The PDVs of braconids (called bracoviruses) differ from the PDVs of ichneumonids (ichnoviruses) in morphology, morphogenesis, and in relation to their interaction with other wasp-derived factors in the parasitized host. The PDVs of different wasp species generally are considered to be distinct viral species. Furthermore, the evolutionary association of ichnoviruses with ichneumonids is known to be unrelated to the evolution of the braconid—bracovirus association and, within the braconids, PDVs occur only in the monophyletic microgastroid group of subfamilies and appear to have coevolved with their wasp hosts.
VLPs are known only in some ichneumonid wasps. It is not clear whether all VLPs are viruses, as the morphology of some VLPs is different from that of typical PDVs and some VLPs lack DNA. However, all PDVs and VLPs appear to be involved in overcoming the host’s immune reaction and often are responsible for other symptoms in infected hosts. For example, the PDVs of some wasps apparently can induce most of the changes in growth, development, behavior, and hemocytic activity that are observed in infected host larvae. The PDVs of other parasitoids (usually braconids) seem to require the presence of accessory factors, particularly venoms, to completely prevent encapsulation of the wasp egg or to fully induce symptoms in the host.
The calyx epithelium of the female reproductive tract is the primary site of replication of PDVs (as depicted for the braconid Toxoneuron nigriceps in the lower left drawing, and for the ichneumonid Campoletis sonoren- sis on the lower right, after Stoltz & Vinson 1979) and is the only site of VLP assembly (as in the ichneumonid Venturia canescens). The lumen of the wasp oviduct becomes filled with PDVs or VLPs, which thus surround the wasp eggs. If VLPs or PDVs are removed artificially from wasp eggs, encapsulation occurs if the unprotected eggs are then injected into the host. If appropriate PDVs or VLPs are injected into the host with the washed eggs, encapsulation is prevented. The physiological mechanism for this protection is not clearly understood, although in the wasp Venturia, which coats its eggs in VLPs, it appears that molecular mimicry of a host protein by a VLP protein interferes with the immune recognition process of the lepidopteran host. The VLP protein is similar to a host hemocyte protein involved in recognition of foreign particles. In the case of PDVs, the process is more active and involves the expression of PDV-encoded gene products that directly interfere with the mode of action of hemocytes.
