Effects of parasitization by Cotesia congregata on the brain-prothoracic gland axis of its host, Manduca sexta

Kelly, Thomas J.; Gelman, Dale B.; Reed, Darcy A.; Beckage, Nancy E.

doi:10.1016/s0022-1910(97)00112-1

Cited by 16 publications

(6 citation statements)

References 26 publications

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“…Often, for endoparasitoids, host molting is inhibited prior to parasitoid emergence and thus levels of physiologically active 20HE must be prevented from increasing to the threshold concentration, which will trigger a molt. M. sexta parasitized by C. congregata appear to have functional prothoracic glands that are not able to respond to prothoracicotropic hormone (Kelly et al, 1998). Results presented here and in our previous investigations support the view that C. congregata both produces and releases physiologically active ecdysteroid, and that the Fig.…”

Section: Discussionsupporting

confidence: 80%

“…Thus, normal negative signals that inhibit PTG production/ release of ecdysteroid are disrupted in parasitized M. sexta last instars. This was confirmed by experiments in which the in vitro production of ecdysteroid by PTGs from parasitized and unparasitized M. sexta was compared (Kelly et al, 1998). Host PTGs continued to secrete ecdysteroid after 3 h of incubation unlike glands from similarly aged unparasitized larvae in which ecdysteroid production reached a plateau.…”

Section: Introductionmentioning

confidence: 66%

“…Because this peak occurs just prior to and during the parasitoids' last larval molt and concomitant emergence from the host, it has been hypothesized that the parasitoid-induced increase in host hemolymph ecdysteroid titers is related to these parasitoid behaviors, and possibly to pupation, which occurs soon after emergence (Beckage, 1985;Gelman et al, 1998). The relative contributions of the parasitoid and the host to this ecdysteroid peak are unknown, although it has been shown that the parasitoid releases ecdysteroid in vivo and that host PTGs do synthesize and release ecdysteroid in vitro (Kelly et al, 1998). In other host-parasite systems, parasitoids have been reported to release ecdysteroids both in vivo and in vitro (Grossniklause-Burgin and Lanzrein, 1990;Brown and Reed-Larsen, 1991;Jones et al, 1992;Brown et al, 1993).…”

Section: Introductionmentioning

confidence: 99%

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Synthesis/release of ecdysteroids by Cotesia congregata, a parasitoid wasp of the tobacco hornworm, Manduca sexta

Gelman

Kelly

Reed

et al. 1999

Arch. Insect Biochem. Physiol.

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Parasitized Manduca sexta undergo developmental arrest in the instar (typically the fifth) from which the parasitoid wasp Cotesia congregata will emerge. Host hemolymph ecdysteroid titers as well as levels of other regulatory molecules are manipulated by the parasitoid to create an environmental milieu which is most suitable for the wasp to complete its life cycle. Based on the results of in vivo studies (reported earlier), the parasitoid appears to require a host hemolymph ecdysteroid titer of 300-400 pg/ml, which it effects in its host, in part, by synthesizing and releasing ecdysteroid. Here we used in vitro incubation to characterize C. congregata's synthesis and release of this group of steroid hormones. In addition, we identified physical characteristics as markers for tracking parasitoid ecdysteroid content as well as hormone synthesis and release. Ecdysteroid content of whole body homogenates increased with parasitoid age. Body length, anal vesicle size and time of ecdysis provided more precise indicators of times when ecdysteroid content would be high or low. Ecdysteroid levels peaked at the time of the parasitoid's molt from the 1st to the 2nd instar and again in the largest parasitoids that were preparing for their molt to the 3rd instar. Ecdysteroid synthesis and release also increased with parasitoid age. When body length was the independent variable, synthesis and release peaked in larvae that were 3.0 mm (often undergoing a molt), dipped in larvae that were 3.6 mm (post-molt), and rose again as larvae increased in length. E, 20HE and polar ecdysteroids were the predominant ecdysteroids released on days 1 through 4. Thus, an ecdysteroid known to be physiologically active is released by the parasitoid. This is the first time that a precise, detailed system of markers has been identified for tracking C. congregata development. Our results support the view that parasitoid synthe-

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Section: Discussionsupporting

confidence: 80%

Section: Introductionmentioning

confidence: 66%

Section: Introductionmentioning

confidence: 99%

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Synthesis/release of ecdysteroids by Cotesia congregata, a parasitoid wasp of the tobacco hornworm, Manduca sexta

Gelman

Kelly

Reed

et al. 1999

Arch. Insect Biochem. Physiol.

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“…Staining is especially intense in hosts from which the parasitoids have already emerged, and the intensity increases with days post-emergence. PTTH activity as measured by an in vitro PTG assay is also greater in brains from these fifth-instar hosts (95). In addition, an analysis of the PTTH present in host brains revealed the presence of a form whose molecular mass was larger than the 11 kDa form found in nonparasitized fifth instars (95).…”

Section: Effects On the Release Or Processing Of Host Neuropeptidesmentioning

confidence: 86%

WASPPARASITOIDDISRUPTION OFHOSTDEVELOPMENT: Implications for New Biologically Based Strategies for Insect Control

Beckage

Gelman²

2004

Annu. Rev. Entomol.

397

304

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Wasp parasitoids use a variety of methods to commandeer their insect hosts in order to create an environment that will support and promote their own development, usually to the detriment of the host insect. Parasitized insects typically undergo developmental arrest and die sometime after the parasitoid has become independent of its host. Parasitoids can deactivate their host's immune system and effect changes in host hormone titers and behavior. Often, host tissues or organs become refractory to stimulation by tropic hormones. Here we present an overview of the manipulative capabilities of wasp-injected calyx fluid containing polydnaviruses and venom, as well as the parasitoid larva and the teratocytes that originate from the serosal membrane that surrounds the developing embryo of the parasitoid. Possibilities for using regulatory molecules produced by the parasitoid or its products that would be potentially useful in developing new, environmentally safe insect control agents are discussed.

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“…Most studies have focused on the hypothesis that the wasp or its associated PDV produce molecules which directly reduce ecdysteroid titers by altering processing or release of PTTH Tanaka and Vinson, 1987;Zitnan et al, 1995;Kelly et al, 1998), disrupting ecdysteroid biosynthesis by prothoracic glands (Pennacchio et al, 1998;Pennacchio et al, 2001;Fallabella et al, 2003), or metabolizing ecdysteroids in circulation (Grossniklaus-Burgin et al, 1998;Coudron et al, 1990). An alternative hypothesis is that inhibition of pupation is an indirect response to virus-and/or parasitoid-induced alterations in host growth or nutritional physiology (Thompson, …”

Section: Introductionmentioning

confidence: 99%

Infection by a symbiotic polydnavirus induces wasting and inhibits metamorphosis of the mothPseudoplusia includens

Pruijssers

Falabella

Eum

et al. 2009

Journal of Experimental Biology

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SUMMARYInsect pathogens and parasites often affect the growth and development of their hosts, but understanding of these processes is fragmentary. Among the most species-rich and important mortality agents of insects are parasitoid wasps that carry symbiotic polydnaviruses (PDVs). Like many PDV-carrying wasps, Microplitis demolitor inhibits growth and pupation of its lepidopteran host, Pseudoplusia includens, by causing host hemolymph juvenile hormone (JH) titers to remain elevated and preventing ecdysteroid titers from rising. Here we report these alterations only occurred if P. includens was parasitized prior to achieving critical weight, and were fully mimicked by infection with only M. demolitor bracovirus (MdBV). Metabolic assays revealed that MdBV infection of pre-critical weight larvae caused a rapid and persistent state of hyperglycemia and reduced nutrient stores. In vitro ecdysteroid assays further indicated that prothoracic glands from larvae infected prior to achieving critical weight remained in a refractory state of ecdysteroid release, whereas infection of post-critical weight larvae had little or no effect on ecdysteroid release by prothoracic glands. Taken together, our results suggest MdBV causes alterations in metabolic physiology, which prevent the host from achieving critical weight. This in turn inhibits the endocrine events that normally trigger metamorphosis.

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Effects of parasitization by Cotesia congregata on the brain-prothoracic gland axis of its host, Manduca sexta

Cited by 16 publications

References 26 publications

Synthesis/release of ecdysteroids by Cotesia congregata, a parasitoid wasp of the tobacco hornworm, Manduca sexta

Synthesis/release of ecdysteroids by Cotesia congregata, a parasitoid wasp of the tobacco hornworm, Manduca sexta

WASPPARASITOIDDISRUPTION OFHOSTDEVELOPMENT: Implications for New Biologically Based Strategies for Insect Control

Infection by a symbiotic polydnavirus induces wasting and inhibits metamorphosis of the mothPseudoplusia includens

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