Characterization of male-derived factors inhibiting female sexual receptivity in Lygus hesperus

Journal of Insect Physiology

Volumn 60, Issue 1, 2014, Pages 104-110

  Brent, Colin S ^a   Hull, J Joe ^a  

^a U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

Accessory glands; Juvenile hormone; Lygus hesperus; Sexual receptivity; Spermatophore

Indexed keywords

COPULATION; FEMALE BEHAVIOR; HORMONE; MALE BEHAVIOR; MATING BEHAVIOR; PEST SPECIES; PHYSIOLOGY; PROTEIN; SEXUAL REPRODUCTION; SPERMATOPHORE;

BIOLOGICAL FACTOR; INSECT PROTEIN; JUVENILE HORMONE;

ACCESSORY GLANDS; ANIMAL; ARTICLE; CHEMISTRY; FEMALE; HEMIPTERA; LYGUS HESPERUS; MALE; PHYSIOLOGY; SEXUAL BEHAVIOR; SPERMATOGONIUM; SPERMATOPHORE;

ACCESSORY GLANDS; JUVENILE HORMONE; LYGUS HESPERUS; SEXUAL RECEPTIVITY; SPERMATOPHORE;

ANIMALS; BIOLOGICAL FACTORS; FEMALE; HEMIPTERA; INSECT PROTEINS; JUVENILE HORMONES; MALE; SEXUAL BEHAVIOR, ANIMAL; SPERMATOGONIA;

EID: 84890851876     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2013.12.001     Document Type: Article

References (50)

1. Avila F.W., Sirot L.K., LaFlamme B.A., Rubinstein C.D., Wolfner M.F. Insect seminal fluid proteins: identification and function. Annu. Rev. Entomol. 2011, 56:21-40.
2. Borovsky D., Carlson D.A., Hancock R.G., Rembold H., Van Handel E. De novo biosynthesis of juvenile hormone III and I by the accessory glands of the male mosquito. Insect Biochem. Mol. Biol. 1994, 24:437-444.
3. Bouletreau-Merle J. Receptivite sexuelle et vitellogenese chez les femelles de Drosophila melanogaster: effets d'une application d'hormone juvenile et de deux analogues hormonaux. C.R. Acad. Sci. Ser. D 1973, 277:2045-2048.
4. Brent C.S. Reproduction of the western tarnished plant bug, Lygus hesperus, in relation to age, gonadal activity and mating status. J. Insect Physiol. 2010, 56:28-34.
5. Brent C.S. Reproductive refractoriness in the western tarnished plant bug (Hemiptera: Miridae). Ann. Entomol. Soc. Am. 2010, 102:300-306.
6. Brent C.S. Stage-specific effects of population density on the development and fertility of the western tarnished plant bug, Lygus hesperus. J. Insect Sci. 2010, 10:49.
7. Brent C.S., Spurgeon D.W. Diapause response of laboratory reared and native Lygus hesperus Knight (Hemiptera: Miridae). Environ. Entomol. 2011, 40:455-461.
8. Brent C.S., Vargo E.L. Changes in juvenile hormone biosynthetic rate and whole body content in maturing virgin queens of Solenopsis invicta. J. Insect Physiol. 2003, 49:967-974.
9. Brent C.S., Fasnacht M.P., Judd T.M. Post-mating enhancement of fecundity in female Lygus hesperus. Physiol. Entomol. 2011, 36:141-148.
10. Chen P.S., Stumm-Zollinger E., Aigaki T., Balmer J., Bienz M., Böhlen P. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell 1988, 54:291-298.
11. Cooper W.R. External visibility of spermatophores as an indicator of mating status of Lygus hesperus (Hemiptera: Miridae) females. J. Entomol. Sci. 2012, 47:285-290.
12. Debolt J.W. Meridic diet for rearing successive generations of Lygus hesperus. Ann. Entomol. Soc. Am. 1982, 75:119-122.
13. 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.
14. Gillot C. Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annu. Rev. Entomol. 2003, 48:163-184.
15. Hartfelder K. Insect juvenile hormone: from "status quo" to high society. Braz. J. Med. Biol. Res. 2000, 33:157-177.
16. Heifetz Y., Lung O., Frongillo E.A., Wolfner M.F. The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr. Biol. 2000, 10:99-102.
17. Jackson C.G., Debolt J.W., Ellington J. Lygus bugs. Biological Control in the Western United States 1995, 87-90. Division of Agriculture and Natural Resources, University of California. J.R. Nechols, L.A. Andres, J.W. Beardsley, R.D. Goeden, C.G. Jackson (Eds.).
18. Kalb J.M., DiBenedetto A.J., Wolfner M.F. Probing the function of Drosophila melanogaster accessory glands by directed cell ablation. Proc. Natl. Acad. Sci. USA 1993, 90:8093-8097.
19. Kingan T.G., Bodnar W.M., Raina A.K., Shabanowitz J., Hunt D.F. The loss of female sex pheromone after mating in the corn earworm moth Helicoverpa zea: identification of a male pheromonostatic peptide. Proc. Natl. Acad. Sci. USA 1995, 92:5082-5086.
20. Kubli E. The sex-peptide. BioEssays 1992, 14:779-784.
21. Lee J.J., Klowden M.J. A male accessory gland protein that modulates female mosquito (Diptera: Culicidae) host-seeking behavior. J. Am. Mosq. Control Assoc. 1999, 15:4-7.
22. Leopold R.A., Terranova A.C., Thorson B.J., Degrugillier M.E. The biosynthesis of the male housefly accessory secretion and its fate in the mated female. J. Insect Physiol. 1971, 17:987-1003.
23. Lung O., Wolfner M.F. Drosophila seminal fluid proteins enter the circulatory system of the mated female fly by crossing the posterior vaginal wall. Insect Biochem. Mol. Biol. 1999, 29:1043-1052.
24. Manning A. Corpus allatum and sexual receptivity in female Drosophila melanogaster. Nature 1966, 211:1321-1322.
25. Miyatake T., Chapman T., Partridge L. Mating-induced inhibition of remating in female Mediterranean fruit flies Ceratitis capitata. J. Insect Physiol. 1999, 45:1021-1028.
26. Mossinson S., Yuval B. Regulation of sexual receptivity of female Mediterranean fruit flies: old hypotheses revisited and a new synthesis proposed. J. Insect Physiol. 2003, 49:561-567.
27. Neubaum D.M., Wolfner M.F. Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics 1999, 153:845-857.
28. Park Y.I., Ramaswamy S.B. Role of brain, ventral nerve cord, and corpora cardiaca-corpora allata complex in the reproductive behavior of female tobacco budworm (Lepidoptera: Noctuidae). Ann. Entomol. Soc. Am. 1998, 91:329-334.
29. Park Y.I., Shu S., Ramaswamy S.B., Srinivasan A. Mating in Heliothis virescens: transfer of juvenile hormone during copulation by male to female and stimulation of biosynthesis of endogenous juvenile hormone. Arch. Insect Physiol. Biochem. 1998, 38:100-107.
30. Patana R. Disposable diet packet for feeding and oviposition of Lygus hesperus (Hemiptera: Miridae). J. Econ. Entomol. 1982, 75:668-669.
31. Peng J., Chen S., Busser S., Liu H., Honegger T., Kubli E. Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr. Biol. 2005, 15:207-213.
32. Pszczolkowski M.A., Tuckera A., Srinivasan A., Ramaswamy S.B. On the functional significance of juvenile hormone in the accessory sex glands of male Heliothis virescens. J. Insect Physiol. 2006, 52:786-794.
33. Qazi M.C.B., Wolfner M.F. An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage. J. Exp. Biol. 2003, 206:3521-3528.
34. Ringo J. Sexual receptivity in insects. Annu. Rev. Entomol. 1996, 41:473-494.
35. Ringo J., Werczberger R., Altaratz M., Segal D. Female sexual receptivity is defective in juvenile hormone-deficient mutants of the apterous gene in Drosophila melanogaster. Behav. Genet. 1991, 21:453-468.
36. Ringo J., Talyn B., Brannan M. Effects of precocene and low protein diet on reproductive behavior in Drosophila melanogaster (Diptera: Drosophilidae). Ann. Entomol. Soc. Am. 2005, 98:601-607.
37. Schmidt T., Choffat Y., Schneider M., Hunziker P., Fuyama Y., Kubli E. Drosophila suzukii contains a peptide homologous to the Drosophila melanogaster sex-peptide and functional in both species. Insect Biochem. Mol. Biol. 1993, 23:571-579.
38. Shirk P.D., Dahm K.H., Röller H. The accessory sex glands as the repository for juvenile hormone in male cecropia moths. Z. Naturforsch. C 1976, 31:199-200.
39. Shirk P.D., Bhaskaran G., Röller H. The transfer of juvenile hormone from male to female during mating in the Cecropia silkmoth. Experientia 1980, 36:682-683.
40. Sirot L.K., Poulson R.L., McKenna M.C., Girnary H., Wolfner M.F., Harrington L.C. Identity and transfer of male reproductive gland proteins of the dengue vector mosquito, Aedes aegypti: potential tools for control of female feeding and reproduction. Insect Biochem. Mol. Biol. 2008, 38:176-189.
41. Smid H.M. Transfer of a male accessory gland peptide to the female during mating in Leptinotarsa decemlineata. Invert. Reprod. Dev. 1998, 34:47-53.
42. Spurgeon D.W., Brent C.S. Morphological characters of diapause in Lygus hesperus Knight (Hemiptera: Miridae). J. Entomol. Sci. 2010, 45:303-316.
43. Strong F.E., Sheldahl J.A., Hughes P.R., Hussein E.M.K. Reproductive biology of Lygus hesperus Knight. Hilgardia 1970, 40:105-147.
44. Tian L., Ji B.-Z., Liu S.-W., Jin F., Gao J., Li S. Juvenile hormone III produced in male accessory glands of the longhorned beetle, Apriona germari, is transferred to female ovaries during copulation. Arch. Insect Biochem. Physiol. 2010, 75:57-67.
45. Wheeler A.G. Biology of the Plant Bugs (Hemiptera: Miridae) 2001, Cornell University Press, Ithaca,NY.
46. Wolfner M.F. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 2002, 88:85-93.
47. Wolfner M.F., Heifetz Y., Appelbaum S.W. Gonadal glands and their gene products. Comprehensive Molecular Insect Science 2005, vol. 1:179-212. Elsevier, Boston.
48. Yamane T., Kimura Y., Katsuhara M., Miyatake T. Female mating receptivity inhibited by injection of male-derived extracts in Callosobruchus chinensis. J. Insect Physiol. 2008, 54:501-507.
49. Yamaoka K., Hirao T. Stimulation of virginal oviposition by male factors and its effect on spontaneous nervous activity in Bombyx mori. J. Insect Physiol. 1977, 23:57-63.
50. Yapici N., Kim Y.-J., Ribeiro C., Dickson B.J. A receptor that mediates the post-mating switching in Drosophila reproductive behavior. Nature 2008, 451:33-38.