Nutrient limitation results in juvenile hormone-mediated resorption of previtellogenic ovarian follicles in mosquitoes

Journal of Insect Physiology

Volumn 57, Issue 9, 2011, Pages 1274-1281

  Clifton, Mark E ^a   Noriega, Fernando G ^a  

^a FLORIDA INTERNATIONAL UNIVERSITY   (United States)

Author keywords

Apoptosis; Juvenile hormone; Mosquito; Oosorption; Reproduction; Sugar feeding

Indexed keywords

CASPASE; JUVENILE HORMONE; METHOPRENE;

APOPTOSIS; DEVELOPMENTAL BIOLOGY; HORMONE; JUVENILE; LIFE HISTORY TRAIT; MOSQUITO; NUTRIENT LIMITATION; REPRODUCTIVE BIOLOGY; REPRODUCTIVE ISOLATION; RESORPTION; RESTING STAGE; SEXUAL MATURITY; STARVATION; SUCROSE; TRADE-OFF;

AEDES; ANIMAL; APOPTOSIS; ARTICLE; DISEASE CARRIER; FEMALE; FERTILITY; FOOD DEPRIVATION; MALE; METABOLISM; OVARY FOLLICLE; OVIPARITY; PHYSIOLOGY;

AEDES; ANIMALS; APOPTOSIS; CASPASES; FEMALE; FERTILITY; FOOD DEPRIVATION; INSECT VECTORS; JUVENILE HORMONES; MALE; METHOPRENE; OVARIAN FOLLICLE; OVIPARITY;

AEDES AEGYPTI;

EID: 80052266200     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2011.06.002     Document Type: Article

References (65)

1. Ahmed A.M., Hurd H. Immune stimulation and malaria infection impose reproductive costs in Anopheles gambiae via follicular apoptosis. Microbes and Infection 2006, 8:308-315.
2. Barrett E.L.B., Preziosi R.F., Moore A.J., Moore P.J. Effects of mating delay and nutritional signals on resource recycling in a cyclically breeding cockroach. Journal of Insect Physiology 2008, 54:25-31.
3. Bell W.J., Bohm M.K. Oosorption in insects. Biological Reviews 1975, 50:373-396.
4. Boggs C.L. Nutritional and life-history determinants of resource allocation in holometabolous insects. The American Naturalist 1981, 117:692-709.
5. Boggs C.L. Resource allocation: exploring connections between foraging and life history. Functional Ecology 1992, 6:508-518.
6. Boggs C.L., Ross C.L. The effect of adult food limitation on life-history traits in Speyeria mormonia (Lepidoptera, Nymphalidae). Ecology 1993, 74:433-441.
7. Borovsky D., Whisenton L.R., Thomas B.R., Fuchs M.S. Biosynthesis and distribution of ecdysone and 20-OH-ecdysone in Aedes aegypti. Archives of Insect Biochemistry and Physiology 1986, 3:19-30.
8. Briegel H. Metabolic relationship between female body size, reserves, and fecundity of Aedes aegypti. Journal of Insect Physiology 1990, 36:165-172.
9. Briegel H., Knüsel I., Timmermann S.E. Aedes aegypti: size, reserves, survival, and flight potential. Journal of Vector Ecology 2001, 26:21-31.
10. Briegel H., Hefti M., Dimarco E. Lipid metabolism during sequential gonotrophic cycles in large and small female Aedes aegypti. Journal of Insect Physiology 2002, 48:547-554.
11. Caroci A., Li Y., Noriega F.G. Reduced juvenile hormone synthesis in mosquitoes with low teneral reserves prevents ovarian previtellogenic development in Aedes aegypti. Journal of Experimental Biology 2004, 207:2685-2690.
12. Carwardine S.L., Hurd H. Effects of Plasmodium yoelii nigeriensis infection on Anopheles stephensi egg development and resorption. Medical and Veterinary Entomology 1997, 11:265-269.
13. Casas J., Pincebourde S., Mandon N., Vannier F., Poujol R., Giron D. Lifetime nutrient dynamics reveal simultaneous capital and income breeding in a parasitoid. Ecology 2005, 86:545-554.
14. Clements A.N. The Biology of Mosquitoes 1992, Chapman aand Hall, London.
15. Clements A.N., Boocock M.R. Ovarian development in mosquitoes: stages of growth and arrest and follicular resorption. Physiological Entomology 1984, 9:1-8.
16. Cooper D.M., Thi E.P., Chamberlain C.M., Pio F., Lowenberger C. Aedes Dronc: a novel ecdysone-inducible caspase in the yellow fever mosquito, Aedes aegypti. Insect Molecular Biology 2007, 16:563-572.
17. Feinsod F.M., Spielman A. Nutrient-mediated juvenile hormone secretion in mosquitoes. Journal of Insect Physiology 1980, 26:113-117.
18. Flatt T., Tu M.P., Tatar M. Hormonal pleiotropy and the juvenile hormone regulation of Drosophila development and life history. BioEssays 2005, 27:999-1010.
19. Foster W.A. Mosquito sugar feeding and reproductive energetics. Annual Review of Entomology 1995, 40:443-474.
20. Gwadz R.W., Spielman A. Corpus allatum control of ovarian development in Aedes aegypti. Journal of Insect Physiology 1973, 19:1441-1448.
21. Hagedorn H.H., Turner S., Hagedorn E.A., Pontecorvo D., Greenbaun P., Pfeiffer D., Wheelock G., Flanagan T.R. Post emergence growth of the ovarian follicles of Aedes aegypti. Journal of Insect Physiology 1977, 23:203-206.
22. Hernández-Martínez S., Mayoral J.G., Li Y., Noriega F.G. Role of juvenile hormone and allatotropin on nutrient allocation, ovarian development and survivorship in mosquitoes. Journal of Insect Physiology 2007, 53:230-234.
23. Hopwood J.A., Ahmed A.M., Polwart A., Williams G.T., Hurd H. Malaria-induced apoptosis in mosquito ovaries: a mechanism to control vector egg production. Journal of Experimental Biology 2001, 204:2773-2780.
24. Judson C.L., de Lumen H.Z. Some effects of juvenile hormone and analogues on ovarian follicles of the mosquito Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 1976, 13:197-201.
25. Lea A.O. Some relationships between environment, corpora allata, and egg maturation in Aedine mosquitoes. Journal of Insect Physiology 1963, 9:793-809.
26. Lea A.O., Briegel H., Lea H.M. Arrest, resorption, or maturation of oocytes in Aedes aegypti: dependence on the quantity of blood and the interval between blood meals. Physiological Entomology 1978, 3:309-316.
27. Li Y., Hernandez-Martinez S., Unnithan G.C., Feyereisen R., Noriega F.G. Activity of the corpora allata of adult female Aedes aegypti: effects of mating and feeding. Insect Biochemistry and Molecular Biology 2003, 33:1307-1315.
28. Moczek A.P. Horn polyphenism in the beetle Onthophagus taurus: larval diet quality and plasticity in parental investment determine adult body size and male horn morphology. Behavioral Ecology 1998, 9:636-641.
29. Moczek A.P., Nijhout H.F. Trade-offs during the development of primary and secondary sexual traits in a horned beetle. The American Naturalist 2004, 163:184-191.
30. Naksathit A.T., Edman J.D., Scott T.W. Amounts of glycogen, lipid, and sugar in adult female Aedes aegypti (Diptera: Culicidae) fed sucrose. Journal of Medical Entomology 1999, 36:8-12.
31. Nayar J.K., Sauerman J.D.M. The effects of diet on life-span, fecundity and flight potential of Aedes taeniorhynchus adults. Journal of Medical Entomology 1971, 8:506-513.
32. Nayar J.K., van Handel E. The fuel for sustained mosquito flight. Journal of Insect Physiology 1971, 17:471-481.
33. Nijhout H.F., Wheeler D.E. Juvenile hormone and the physiological basis for insect polymorphisms. The Quarterly Review of Biology 1982, 57:109-133.
34. Noriega F.G. Nutritional regulation of JH synthesis: a mechanism to control reproductive maturation in mosquitoes?. Insect Biochemistry and Molecular Biology 2004, 34:687-693.
35. Noriega F.G., Shah D.K., Wells M.A. Juvenile hormone controls early trypsin gene transcription in the midgut of Aedes aegypti. Insect Molecular Biology 1997, 6:63-66.
36. Ohgushi T. A reproductive tradeoff in an herbivorous lady beetle: egg resorption and female survival. Oecologia 1996, 106:345-351.
37. Oliveira G.A., Baptista D.L., Guimaraes-Motta H., Almeida I.C., Masuda H., Atella G.C. Flight-oogenesis syndrome in a blood sucking bug: biochemical aspects of lipid metabolism. Archives of Insect Biochemistry and Physiology 2006, 62:164-175.
38. Osawa, N., 2005. The effect of prey availability on ovarian development and oosorption in the ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). European Journal of Entomology, 102, 503-511.
39. Parker E.R., Pianka W.S. Age specific reproductive tactics. The American Naturalist 1975, 109:453-464.
40. Raikhel A.S., Lea A.O. Hormone-mediated formation of the endocytic complex in mosquito oocytes. General and Comparative Endocrinology 1984, 57:422-433.
41. Raikhel A.S., Lea A.O. Control of follicular epithelium development and vitelline envelope formation in the mosquito: role of juvenile hormone and 20-hydroxyecdysone. Tissue and Cell 1991, 23:577-591.
42. Rantala M.J., Vainikka A., Kortet R. The role of juvenile hormone in immune function and pheromone production trade-offs: a test of the immuno-competence handicap principle. Proceedings of the Royal Society B 2003, 270:2257-2261.
43. Richard, R., Casas., J., 2009. Stochasticity and controllability of nutrient sources in foraging: host-feeding and egg resorption in parasitoids. Ecological Monographs 79 (3), 465-483.
44. Rivero A., Giron D., Casas J. Lifetime allocation of juvenile and adult nutritional resources to egg production in a Holometabolous insect. Proceedings of National Academy of Sciences 2001, 268:1231-1237.
45. Rosenheim J.A., Heimpel G.E., Mangel M. Egg maturation, egg resorption and the costliness of transient egg limitation in insects. Proceedings of the Royal Society B 2000, 267:1565-1573.
46. Schal C., Chiang A.-S., Burns E.L., Gado M., Cooper R.A. Role of the brain in juvenile hormone synthesis and oocyte development: effects of dietary protein in the cockroach Blattella germanica (L.). Journal of Insect Physiology 1993, 39:303-313.
47. Shapiro A.B., Wheelock G.D., Hagedorn H.H., Baker F.C., Tsai L.W., Schooley D.A. JH and juvenile esterase in adult females of the mosquito A. aegypti. Journal of Insect Physiology 1986, 32:867-877.
48. Soller M., Bownes M., Kubli E. Control of oocyte maturation in sexually mature Drosophila females. Developmental Biology 1999, 208:337-351.
49. Spindler, K.D., Honl, C., Tremmel, C.H. Braun, S., Ruff, H., M. Spindler-Barth, 2009. Ecdysteroid hormone action. Cellular and Molecular Life Sciences 66, 3837-3850.
50. Stevens D.J., Hansell M.H., Monaghan P. Developmental trade-offs and life histories: strategic allocation of resources in caddis flies. Proceedings of the Royal Society B 2000, 267:1511-1515.
51. Telang A., Li Y., Noriega F.G., Brown M.R. Effects of larval nutrition on the endocrinology of mosquito egg development. Journal of Experimental Biology 2006, 209:645-655.
52. Terashima J., Bownes M. Translating available food into the number of eggs laid by Drosophila melanogaster. Genetics 2004, 167:1711-1719.
53. Terashima J., Takaki K., Sakurai S., Bownes M. Nutritional status affects 20-hydroxyecdysone concentration and progression of oogenesis in Drosophila melanogaster. Journal of Endocrinology 2005, 187:69-79.
54. Tobe S.S., Chapman C.S. The effects of starvation and subsequent feeding on juvenile hormone synthesis and oocyte growth in Schistocerca americana gregaria. Journal of Insect Physiology 1979, 25:701-708.
55. Troy S., Anderson W.A., Spielman A. Lipid content of maturing ovaries of Aedes aegypti mosquitoes. Comparative Biochemistry and Physiology B 1975, 50:457-461.
56. Trumbo S.T., Robinson G.E. Nutrition, hormones and life history in burying beetles. Journal of Insect Physiology 2004, 50:383-391.
57. Uchida K., Nishizuka M., Ohmori D., Ueno T., Eshita Y., Fukunaga A. Follicular epithelial cell apoptosis of atretic follicles within developing ovaries of the mosquito Culex pipiens pallens. Journal of Insect Physiology 2004, 50:903-912.
58. Wheeler D.E. The role of nourishment in oogenesis. Annual Review of Entomology 1996, 41:345-379.
59. Winckler J. Vital staining of lysosomes and other cell organelles of the rat with neutral red. Progress in Histochemistry and Cytochemistry 1974, 6:1-91.
60. Wu Y., Parthasarathy R., Bai H., Palli S.R. Mechanisms of midgut remodeling: juvenile hormone analog methoprene blocks midgut metamorphosis by modulating ecdysone action. Mechanisms of Development 2006, 123:530-547.
61. Yin C.M., Qin W.H., Stoffolano J.G. Regulation of mating behaviour by nutrition and the corpus allatum in both male and female Phormia regina (Meigen). Journal of Insect Physiology 1999, 45:815-822.
62. 14C]-labeled meal protein amino acids in Aedes aegypti mosquitoes. Journal of Insect Physiology 2004, 50:337-349.
63. Ziegler R. Lipid synthesis by ovaries and fat body of Aedes aegypti (Diptera: Culicidae). European Journal of Entomology 1997, 94:385-391.
64. Ziegler R., Ibrahim M.M. Formation of lipid reserves in fat body and eggs of the yellow fever mosquito, Aedes aegypti. Journal of Insect Physiology 2001, 47:623-627.
65. Ziegler R., Van Antwerpen R. Lipid uptake by insect oocytes. Insect Biochemistry and Molecular Biology 2006, 36:264-272.