Parasite manipulation of insect reproduction: who benefits?

Host fertility is often curtailed as a result of parasitic infection. The hypothesis that this may confer an adaptive advantage upon the symbionts if nutrients are directed from reproduction and made available for host/parasite maintenance is explored. The suggestion is made that an understanding of the mechanisms underlying the pathophysiology of fecundity reduction may shed light upon the evolutionary implications of this strategy for both parasite and host. To illustrate this the down-regulation of egg production is explored with reference to a particular model system, the association between metacestodes of the rat tapeworm, Hymenolepis diminuta and the mealworm beetle, Tenebrio molitor. Several aspects of host reproductive behavior and physiology are affected by infection in this association, including vitellogenesis. Metacestodes directly inhibit the fat body synthesis of vitellogenin in a stage-specific, density-dependent manner. This inhibition is likely to be orchestrated by a modulator molecule, produced by the parasite. In the ovarian follicles, juvenile hormone III binding to a specific follicular membrane-binding protein is inhibited in infected beetles, resulting in the down-regulation of a cascade of events which enables vitellogenin to pass into the developing oocyte. Data to support the proposed existence of a parasite-induced antigonadotrophin, of host origin, are discussed. Evidence that similar mechanisms operate in Plasmodium-infected anopheline mosquitoes and Onchocerca-infected blackflies is presented in support of the possibility that a parasite-induced reduction in host reproductive fitness is an adaptive strategy and an assessment of who is manipulating whom is made.