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Parasite regulation of host insect metamorphosis: a new form of regulation in pseudoparasitized larvae ofTrichoplusia ni


When eggs ofTrichoplusia ni (Lepidoptera) are stung by a parasitic wasp,Chelonus sp., the developing host larvae precociously initiate metamorphosis ten days later. Precocious initiation of metamorphosis occurs even in ‘pseudoparasitized’ stung hosts which contain no living parasites at the time of symptoms of host regulation by the parasite. In feeding, penultimate instar, pseudoparasitized hosts, the corpora allata activity, hemolymph juvenile hormone esterase activity, in vivo rates of juvenile hormone metabolism and changes in hemolymph protein composition all follow the pattern of the normal last instar. This and other evidence suggests the entire developmental pattern of the last larval instar is precociously expressed in penultimate instar, pseudoparasitized hosts. The cause of precocious expression of the developmental program leading to metamorphosis is a significant decrease in the critical size parameter that, in normal larvae, signals attainment of the last instar. The induction, in preultimate instar larvae, of the entire feeding stage developmental program leading to metamorphic commitment, using either biochemical, surgical or parasitic experimental probes, has not been previously reported. The results have important implications for the study of host-parasite endocrine interaction, of normal insect metamorphosis and even of human puberty.

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  1. Ables JR, Vinson SB (1981) Regulation of host larval development by the egg-larval endoparasitoidChelonus insularis (Hym: Braconidae). Entomophaga 25:453–456

  2. Barton WS, Brill WJ (1983) Prospects in plant genetic engineering. Science 219:671–676

  3. Beckage NE, Riddiford LM (1982) Effects of parasitism byApanteles congregatus on the endocrine physiology of the tobacco hornworm,Manduca sexta. Gen Comp Endocrinol 47:308–322

  4. Bhaskaran G, Jones G, Jones D (1980) Neuroendocrine regulation of corpus allatum activity inManduca sexta: Sequential neurohumoral and nervous inhibition in the last instar larva. Proc Natl Acad Sci 77:4407–4411

  5. Decker GC, Maddox JV (1971) Bionomics ofSymyra henrici (Grote). J Econ Entomol 64:117–123

  6. Fain MJ, Riddiford LM (1975) Juvenile hormone titers in the hemolymph during the late larval development of the tobacco hornworm,Manduca sexta. Biol Bull 149:506–521

  7. Granger NA, Niemiec SM, Gilbert LI, Bollenbacher WE (1982) Juvenile hormone synthesis by larval and pupal corpora allata ofManduca sexta. Mol Cell Endocrinol 28:587–604

  8. Hammock BD, Sparks TC (1977) A rapid assay for insect juvenile hormone esterase activity. Analyt Biochem 82:573–579

  9. Jones D (1985a) The endocrine basis for developmentally stationary prepupae in larvae ofTrichoplusia ni pseudoparasitized byChelonus insularis. J Comp Physiol B 155:235–240

  10. Jones D (1985b) Endocrine interaction between host (Lepidoptera) and parasite (Cheloninae: Lepidoptera): Is the host or the parasite in control? Ann Entomol Soc Am 78:141–148

  11. Jones D (1985c) Use of parasite regulation of host endocrinology to enhance the potential of biological control. Entomophaga (in press)

  12. Jones D, Jones G, Bhaskaran G (1981a) Dietary sugars, hemolymph trehalose levels and supernumerary molting ofManduca sexta larvae. Physiol Zool 54:260–266

  13. Jones D, Jones G, Click A, Sreekrishna S (1984a) Anti-juvenile hormone effects in larvae ofTrichoplusia ni pseudoparasitized byChelonus sp. XVII International Congress of Entomology, Hamburg. Abstract Book

  14. Jones D, Jones G, Hammock BD (1981b) Growth parameters associated with endocrine events in larvalTrichoplusia ni (Hübner) and timing of these events with developmental markers. J Insect Physiol 27:779–788

  15. Jones D, Jones G, Hammock BD (1981c) Developmental and behavioural responses of larvalTrichoplusia ni to parasitization by an imported braconid parasiteChelonus sp. Physiol Entomol 6:387–394

  16. Jones D, Jones G, Jackson ML (1984b) Insects and tobacco: A model system for testing the feasibility of plant genetic engineering for insect resistance. In: Gustafson PL (ed) Gene manipulation in plant improvement. Plenum Press, New York, p 656

  17. Jones D, Jones G, Van Steenwyk RA, Hammock BD (1982a) Effect of the parasiteCopidosoma truncatellum (Dalman) on the development of its host,Trichoplusia ni (Hübner). Ann Entomol Soc Am 75:7–11

  18. Jones D, Jones G, Wing KD, Rudnicka M, Hammock BD (1982b) Juvenile hormone esterases of Lepidoptera. I. Activity in the hemolymph during the last larval instar of 11 species. J Comp Physiol 148:1–10

  19. Jones D, Sreekrishna S (1984) Precocious metamorphosis inChelonus parasitizedTrichoplusia ni: The endocrine basis for this anti-juvenile hormone effect. In: Borkovec AB, Kelly TJ (eds) Insect Neurochemistry and Neurophysiology. Plenum Press, New York, pp 389–391

  20. Jones G, Wing KD, Jones D, Hammock BD (1981) The source and action of head factors regulating juvenile hormone esterase in larvae of the cabbage looper,Trichoplusia ni. J Insect Physiol 27:85–91

  21. Lucky AW, Rich BH, Rosenfield RL, Fang VS, Roche-Bender N (1980) Bioactive LH: A test to discriminate true precocious puberty from premature thelarche and andrenarche. J Pediatr 97:214–216

  22. Mueller JF (1974) The biology ofSpirometra. J Parasit 60:3–14

  23. Nijhout HF (1975) A threshold size for metamorphosis in the tobacco hornworm,Manduca sexta L. Biol Bull 149:214–225

  24. Nijhout HF, Williams CM (1974) Control of molting and metamorphosis in the tobacco hornworm,Manduca sexta (L.): Cessation of juvenile hormone secretion as a trigger for pupation. J Exp Biol 61:493–501

  25. Rimoin DL, Schimke RN (1971) Genetic disorders of the endocrine glands. CV Mosby Co, Saint Louis

  26. Safranek L, Riddiford LM (1975) The biology of the black larval mutant of the tobacco hornworm,Manduca sexta. J Insect Physiol 21:1931–1938

  27. Shaw MR (1981) Delayed inhibition of host development by the nonparalyzing venoms of parasitic wasps. J Invert Pathol 37:215–221

  28. Smilowitz Z (1971) Hemolymph proteins in developing cabbage looper larvae and pupae. Ann Entomol Soc Am 64:340–343

  29. Smilowitz Z (1974) Relationships between the parasitoidHyposoter exigua (Viereck) and cabbage looper,Trichoplusia ni (Hübner): Evidence from endocrine involvement in successful parasitism. Ann Entomol Soc Am 67:317–320

  30. Sparks TC, Hammock BD (1979) Induction and regulation of juvenile hormone esterases during the last larval instar of the cabbage looper,Trichoplusia ni. J Insect Physiol 25:551–560

  31. Sparks TC, Hammock BD (1980) Comparative inhibition of the juvenile hormone esterases fromTrichoplusia ni, Musca domestica andTenebrio molitor. Pestic Biochem Physiol 14:290–302

  32. Staal GB, Henrick CA, Bergot BJ, Cerf DC, Edwards JP, Kramer SJ (1981) Relationships and interactions between JH and anti-JH analogues in Lepidoptera. In: Sehnal F, Zabza A, Menn JJ, Cymborowski B (eds) Regulation of Insect Development and Behavior. Warsaw Tech Univ Press, pp 322–340

  33. Thompson SN (1983) Biochemical and physiological effects of metazoan endoparasites on their host species. Comp Biochem Physiol 74B:183–212

  34. Varley GC, Butler CG (1933) The acceleration of development of insects by parasitism. Parasitol 25:263–268

  35. Vinson SB, Iwantsch GF (1980) Host regulation by insect parasitoids. Q Rev Biol 55:143–165

  36. Wigglesworth VB (1970) The physiology of insect metamorphosis. Cambridge University Press, New York

  37. Williams CM (1967) Third generation pesticides. Sci Am 217:13–17

  38. Winter A, Ek K, Andersson UB (1977) Analytical electrofocusing in thin layers of polyacrylamide gels. LKB Application Note 250

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Jones, D. Parasite regulation of host insect metamorphosis: a new form of regulation in pseudoparasitized larvae ofTrichoplusia ni . J Comp Physiol B 155, 583–590 (1985). https://doi.org/10.1007/BF00694448

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  • Juvenile Hormone
  • Tobacco Hornworm
  • Cabbage Looper
  • Corpus Allata
  • Juvenile Hormone Analog