Direct manipulation of insect reproduction by agents of parasite origin

Reproductive output of female Tenebrio molitor beetles is reduced upon infection with metacestodes of the rat tapeworm, Hymenolepis diminuta. We are using this as a model to investigate the adaptive significance of parasite-induced curtailment of insect reproduction. Production of the yolk protein vitellogenin (Vg) in the insect fat body is significantly reduced both in vitro and in vivo by metacestodes. Synthesis can be measured by using [14C]L–leucine incorporation, followed by immunoprecipitation. In this paper we demonstrate that a significant decrease in [14C]Vg can be produced by an acetic acid extract of the parasite. Conclusive evidence is presented that the active component(s) originate from the metacestodes: an extract of parasites grown entirely axenically has similar deleterious effects. The developmental stage of the metacestode is important: immature (stage I to II) parasites had greater capacity to suppress Vg synthesis than mature ones (stage V to VI). Examination of the chemical nature of the effector molecule(s) revealed that acetic–acid–extractable, boiling–resistant, pronase–sensitive agents in the molecular mass range 10 to 50 kDa reduced Vg synthesis by 47.4%. These data suggest that metacestodes produce a modulator molecule that directly affects insect vitellogenesis and, therefore, that reduction of host fitness may confer a selective advantage upon the parasite.

[1]  H. Hurd,et al.  Parasite manipulation of insect reproduction: who benefits ? , 1998, Parasitology.

[2]  H. Hurd,et al.  The Interplay between Patency, Microsomal Na(+)/K(+) ATPase Activity and Juvenile Hormone, in Tenebrio molitor Parasitized by Hymenolepsis diminuta. , 1997, Journal of insect physiology.

[3]  H. Hurd,et al.  Haemolymph from female beetles infected with Hymenolepis diminuta metacestodes retards the development of ovarian follicles in recipient Tenebrio molitor (Coleoptera) , 1997, Parasitology.

[4]  H. Hurd,et al.  The Role of Endocrinological Versus Nutritional Influences in Mediating Reproductive Changes in Insect Hosts and Insect Vectors , 1997 .

[5]  H. Hurd,et al.  Hymenolepis diminuta: metacestode-induced reduction in the synthesis of the yolk protein, vitellogenin, in the fat body of Tenebrio molitor , 1996, Parasitology.

[6]  O. Richard,et al.  Detection of vitellogenin in the haemolymph of larval female locusts (Locusta migratoria) treated with the neurohormone, Lom OMP , 1996 .

[7]  G. R. Wyatt,et al.  Cellular and Molecular Actions of Juvenile Hormone. II. Roles of Juvenile Hormone in Adult Insects , 1996 .

[8]  H. Hurd,et al.  Observations on the axenic culture of metacestodes of Hymenolepis diminuta , 1994 .

[9]  E. Pshennikova,et al.  Stored forms of vitellogenin mRNA in fat body cells of Locusta migratoria , 1994 .

[10]  R. Poulin The evolution of parasite manipulation of host behaviour: a theoretical analysis , 1994, Parasitology.

[11]  C. Nespoulous,et al.  Physical characterization and sequence identification of the ovary maturating parsin. A new neurohormone purified from the nervous corpora cardiaca of the African locust (Locusta migratoria migratorioides. , 1991, European journal of biochemistry.

[12]  R. Dawkins Parasites, desiderata lists and the paradox of the organism , 1990, Parasitology.

[13]  P. Moshitzky,et al.  The role of adipokinetic hormone in the control of vitellogenesis in locusts , 1990 .

[14]  E. Pshennikova,et al.  The role of juvenile hormone and a brain factor in the regulation of vitellogenin biosynthesis in the locust (Locusta migratoria). , 1990 .

[15]  A. Read Parasites and the evolution of host sexual behaviour. , 1990 .

[16]  T. Triseleva,et al.  Differential regulation of protein biosynthesis at translational level in the fat body cells of adult Locusta migratoria , 1989, Molecular reproduction and development.

[17]  C. Arme Ontogenetic changes in helminth membrane function , 1988, Parasitology.

[18]  H. Hurd,et al.  An evaluation of Locusta migratoria as a model for the study of pathophysiology of Hymenolepis diminuta metacestodes in insects. , 1987, The Journal of parasitology.

[19]  H. Hurd,et al.  Hymenolepis diminuta: effect of infection upon the patency of the follicular epithelium in the intermediate host, Tenebrio molitor. , 1987, Journal of invertebrate pathology.

[20]  H. Hurd,et al.  Hymenolepis diminuta (Cestoda): the role of intermediate host sex in the establishment, growth and development of metacestodes in Tenebrio molitor (Coleoptera) , 1987 .

[21]  F. Couillaud,et al.  Anti-juvenile effect of neuroparsin A, a neuroprotein isolated from locust corpora cardiaca , 1987 .

[22]  E. Ampleford,et al.  Feeding causes the appearance of a factor in the haemolymph that stimulates protein synthesis , 1987 .

[23]  H. Hurd,et al.  Hymenolepis diminuta: influence of metacestodes on synthesis and secretion of fat body protein and its ovarian sequestration in the intermediate host, Tenebrio molitor , 1986, Parasitology.

[24]  M. Maema Experimental infection of Tribolium confusum (Coleoptera) by Hymenolepis diminuta (Cestoda): host fecundity during infection , 1986, Parasitology.

[25]  H. Hurd,et al.  Hymenolepis diminuta: effect of metacestodes on production and viability of eggs in the intermediate host, Tenebrio molitor. , 1986, Journal of invertebrate pathology.

[26]  H. Hurd,et al.  Tenebrio molitor (Coleoptera): effect of metacestodes of Hymenolepis diminuta (Cestoda) on haemolymph amino acids , 1984, Parasitology.

[27]  B. G. Loughton,et al.  A Protein Synthesis Stimulating Hormone in the Locust , 1984 .

[28]  A. Keymer The influence of Hymenolepis diminuta on the survival and fecundity of the intermediate host, Tribolium confusum , 1980, Parasitology.

[29]  B. G. Loughton,et al.  Adipokinetic hormone inhibits protein synthesis in Locusta , 1979, Nature.

[30]  M. Voge,et al.  Development of Hymenolepis nana and 80 Hymenolepis diminuta (Cestoda: Hymenolepididae) in the intermediate Host Tribolium confusum. , 1957 .