Seminal proteins but not sperm induce morphological changes in the Drosophila melanogaster female reproductive tract during sperm storage

Journal of Insect Physiology

Volumn 53, Issue 4, 2007, Pages 319-331

  Adams, Erika M ^a   Wolfner, Mariana F ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Fertility; Mating plug; Muscle contraction; Seminal proteins; Sperm; Uterus

Indexed keywords

DROSOPHILA PROTEIN; SEMINAL PLASMA PROTEIN;

FERTILITY; FLY; GAMETOGENESIS; MORPHOGENESIS; PROTEIN; REPRODUCTIVE BIOLOGY; SECONDARY SEXUAL CHARACTERISTICS; SPERM; SPERMATOPHORE;

ANIMAL; ARTICLE; CHEMISTRY; DROSOPHILA MELANOGASTER; FEMALE; HISTOLOGY; MALE; PHYSIOLOGY; REPRODUCTION; SPERM; SPERMATOZOON;

ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; MALE; REPRODUCTION; SEMEN; SEMINAL PLASMA PROTEINS; SPERMATOZOA;

DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 33947678116     PISSN: 00221910     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jinsphys.2006.12.003     Document Type: Article

References (67)

1. Alonso-Pimentel H., Tolbert L.P., and Heed W.B. Ultrastructural examination of the insemination reaction in Drosophila. Cell and Tissue Research 275 (1994) 467-479
2. Anderson R.C. A study of the factors affecting fertility of lozenge females of Drosophila melanogaster. Genetics 30 (1945) 280-296
3. Arthur Jr. B.I., Hauschteck-Jungen E., Nöthiger R., and Ward P.I. A female nervous system is necessary for normal sperm storage in Drosophila melanogaster: a masculinized nervous system is as good as none. Proceedings of the Royal Society of London, Series B 265 (1998) 1749-1753
4. Bairati A. Structure and ultrastructure of the male reproductive system in Drosophila melanogaster Meig. 2. The genital duct and accessory glands. Italian Journal of Zoology 2 (1968) 105-182
5. Bairati A., and Perotti M.E. Occurrence of a compact plug in the genital duct of Drosophila females after mating. Drosophila Information Service 45 (1970) 67-68
6. Bertram M.J., Neubaum D.M., and Wolfner M.F. Localization of the Drosophila male accessory gland protein Acp36DE in the mated female suggests a role in sperm storage. Insect Biochemistry and Molecular Biology 26 (1996) 971-980
7. Birkhead T.R. Cryptic female choice: criteria for establishing female sperm choice. Evolution 52 (1998) 1212-1218
8. Birkhead T.R., and Møller A.P. Female control of paternity. Trends in Ecology and Evolution 8 (1993) 100-104
9. Bloch Qazi M.C., and Wolfner M.F. An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage. Journal of Experimental Biology 206 (2003) 3521-3528
10. Bloch Qazi M.C., Aprille J.R., and Lewis S.M. Female role in sperm storage in the red flour beetle, Tribolium castaneum. Comparative Biochemistry and Physiology A 120 (1998) 641-647
11. Bloch Qazi M.C., Heifetz Y., and Wolfner M.F. The developments between gametogenesis and fertilization: ovulation and female sperm storage in Drosophila melanogaster. Developmental Biology 256 (2003) 195-211
12. Boswell R.E., and Mahowald A.P. Tudor, a gene required for assembly of the germ plasm in Drosophila melanogaster. Cell 43 (1985) 97-104
13. Bryant P.J. Pattern formation in imaginal discs. In: Ashburner M., and Wright T.R.F. (Eds). The Genetics and Biology of Drosophila vol. 2C (1978), Academic Press, New York 230-336
14. Clark A.G., and Begun D.J. Female genotypes affect sperm displacement in Drosophila. Genetics 149 (1998) 1487-1493
15. Clark A.G., Aguade M., Prout T., Harshman L.G., and Langley C.H. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics 139 (1995) 189-201
16. Clark A.G., Begun D.J., and Prout T. Female×male interactions in Drosophila sperm competition. Science 283 (1999) 217-220
17. Collins A.M., Williams V., and Evans J.D. Sperm storage and antioxidative enzyme expression in the honeybee, Apis mellifera. Insect Molecular Biology 13 (2004) 141-146
18. Davey K.G., and Webster G.F. Structure and secretion of spermatheca of Rhodnius prolixus Stal-a histochemical study. Canadian Journal of Zoology 45 (1967) 653-657
19. DeVries J.K. Insemination and sperm storage in Drosophila melanogaster. Evolution 18 (1964) 271-282
20. Eberhard W.G. Female Control: Sexual Selection by Cryptic Female Choice (1996), Princeton University Press, Princeton, NJ
21. Fedina T.Y., and Lewis S.M. Female influence over offspring paternity in the red flour beetle Tribolium castaneum. Proceedings of the Royal Society of London, Series B 271 (2004) 1393-1399
22. Filosi M., and Perotti M.E. Fine structure of the spermatheca of Drosophila melanogaster. Journal of Submicroscopic Cytology 7 (1975) 259-270
23. Fiumera A.C., Dumont B.L., and Clark A.G. Sperm competitive ability in Drosophila melanogaster associated with variation in male reproductive proteins. Genetics 169 (2005) 243-257
24. Fowler G.L. Some aspects of the reproductive biology of Drosophila: sperm transfer, sperm storage, and sperm utilization. Advances in Genetics 17 (1973) 293-360
25. Fuyama Y. Species specificity of paragonial substances as an isolating mechanism in Drosophila. Experientia 39 (1983) 190-192
26. Gilbert D.G. Ejaculate esterase 6 and initial sperm use by female Drosophila melanogaster. Journal of Insect Physiology 27 (1981) 641-650
27. Gillott C. Male accessory gland secretions: modulators of female reproductive physiology and behavior. Annual Review of Entomology 48 (2003) 163-184
28. Gromko M.H., Gilbert D.G., and Richmond R.C. Sperm transfer and use in the multiple mating system of Drosophila. In: Smith R.L. (Ed). Sperm Competition and the Evolution of Animal Mating Systems (1984), Academic Press, London 371-426
29. Heifetz Y., and Wolfner M.F. Mating, seminal fluid components, and sperm cause changes in vesicle release in the Drosophila female reproductive tract. Proceedings of the National Academy of Sciences USA 101 (2004) 6261-6266
30. Heifetz Y., Lung O., Frongillo Jr. E.A., and Wolfner M.F. The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Current Biology 10 (2000) 99-102
31. Hihara F. Effects of the male accessory gland secretion on oviposition and remating in females of Drosophila melanogaster. Zoological Magazine 90 (1981) 307-316
32. Hosken D.J., and Ward P.I. Copula in yellow dung flies (Scathophaga stercoraria): investigating sperm competition models by direct investigation. Journal of Insect Physiology 46 (2000) 1355-1363
33. Hosken D.J., Meyer E., and Ward P.I. Internal female reproductive anatomy and genitalic interactions during copula in the yellow dung fly, Scathophaga stercoraria (Diptera: Scathophagidae). Canadian Journal of Zoology 77 (1999) 1975-1983
34. Iida K., and Cavener D.R. Glucose dehydrogenase is required for normal sperm storage and utilization in female Drosophila melanogaster. Journal of Experimental Biology 207 (2004) 675-681
35. Jamieson B.G.M. The Ultrastructure and Phylogeny of Insect Spermatozoa (1987), Cambridge University Press, Cambridge, UK
36. Kalb J., DiBenedetto A.J., and Wolfner M.F. Probing the function of Drosophila melanogaster accessory glands by directed cell ablation. Proceedings of the National Academy of Sciences USA 90 (1993) 8093-8097
37. Kaufman B.P., and Demerec M. Utilization of sperm by the female Drosophila melanogaster. American Naturalist 76 (1942) 445-469
38. Lawniczak M.K., and Begun D.J. A QTL analysis of female variation contributing to refractoriness and sperm competition in Drosophila melanogaster. Genetical Research 86 (2005) 107-114
39. Lefevre G., and Jonsson U.B. Sperm transfer, storage, displacement, and utilization in Drosophila melanogaster. Genetics 47 (1962) 1719-1736
40. Linley J.R. Emptying of the spermatophore and spermathecal filling in Culicoides melleus (Coq.) (Diptera: Ceratopogonidae). Canadian Journal of Zoology 59 (1981) 347-356
41. Liu H., and Kubli E. Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proceedings of the National Academy of Sciences USA 100 (2003) 9929-9933
42. Ludwig M.Z., Uspensky I.I., Ivanov A.I., Kopantseva M.R., Dianov C.M., Tamarina N.A., and Korochkin L.I. Genetic control and expression of the major ejaculatory bulb protein (PEB-me) in Drosophila melanogaster. Biochemical Genetics 29 (1991) 215-239
43. Lung O., and Wolfner M.F. Drosophila seminal fluid proteins enter the circulatory system through the walls of the posterior vagina. Insect Biochemistry and Molecular Biology 29 (1999) 1043-1052
44. Lung O., and Wolfner M.F. Identification and characterization of the major D. melanogaster mating plug protein. Insect Biochemistry and Molecular Biology 31 (2001) 543-551
45. Manning A. A sperm factor affecting the receptivity of Drosophila melanogaster females. Nature 194 (1962) 252-253
46. Manning A. The control of sexual receptivity in female Drosophila. Animal Behavior 15 (1967) 239-250
47. Marchini D., Giordano P.C., Amons R., Bernini L.F., and Dallai R. Purification and primary structure of ceratotoxin A and B, two antibacterial peptides from the female reproductive accessory glands of the medfly Ceratitis capitata (Insecta: Diptera). Insect Biochemistry and Molecular Biology 23 (1993) 591-598
48. Meikle D.B., Sheehan K.B., Phillis D.M., and Richmond R.C. Localization and longevity of seminal-fluid esterase 6 in mated female Drosophila melanogaster. Journal of Insect Physiology 14 (1990) 1159-1168
49. Middleton C.A., Nongthomba U., Parry K., Sweeney S.T., Sparrow J.C., and Elliott C.G. Neuromuscular organization and aminergic modulation of contractions in the Drosophila ovary. BMC Biology 4 (2006) 17
50. Miller A. The internal anatomy and histology of the imago of Drosophila melanogaster. In: Demerec M. (Ed). Biology of Drosophila (1950), Wiley, New York 420-534
51. Miller G.T., and Pitnick S. Sperm-female coevolution in Drosophila. Science 298 (2002) 1230-1233
52. Monsma S.A., Harada H.A., and Wolfner M.F. Synthesis of two Drosophila male accessory gland proteins and their fate after transfer to the female during mating. Developmental Biology 142 (1990) 465-475
53. Neubaum D.M., and Wolfner M.F. Wise, winsome or wierd: mechanisms of sperm storage in female animals. Current Topics in Developmental Biology 41 (1999) 67-97
54. Neubaum D.M., and Wolfner M.F. Drosophila females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics 153 (1999) 845-857
55. Nonidez J.F. The internal phenomena of reproduction in Drosophila. Biological Bulletins of Woods Hole 39 (1920) 207-230
56. Parker G. Sperm competition and its evolutionary consequences in the insects. Biological Reviews 45 (1970) 525-567
57. Parker G.A., Simmons L.W., Stockley P., McChristie D.M., and Charnov E.L. Optimal copula duration in yellow dung flies: effects of female size and egg content. Animal Behavior 57 (1999) 795-805
58. Patterson J.T., and Stone W.S. Evolution in the Genus Drosophila (1952), Macmillan, New York
59. Peng J., Chen S., Busser S., Liu H., Honegger T., and Kubli E. Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Current Biology 15 (2005) 207-213
60. Pitnick S., Spicer G.S., and Markow T.A. How long is a giant sperm?. Nature 375 (1995) 109
61. Ravi Ram K., Ji S., and Wolfner M.F. Fates and targets of male accessory gland proteins in mated female Drosophila melanogaster. Insect Biochemistry and Molecular Biology 35 (2005) 1059-1071
62. Santel A., Winhauer T., Blumer N., and Renkawitz-Pohl R. The Drosophila don juan (dj) gene encodes a novel sperm specific protein component characterized by an unusual domain of repetitive amino acid motif. Mechanisms of Development 64 (1997) 19-30
63. Thornhill R. Cryptic female choice and its implications in the scorpionfly Harpobittacus nigriceps. American Naturalist 122 (1983) 765-788
64. Tram U., and Wolfner M.F. Male seminal fluid proteins are essential for sperm storage in Drosophila melanogaster. Genetics 153 (1999) 837-844
65. Ward P.I. Intraspecific variation in sperm size characters. Heredity 80 (1998) 655-699
66. Weirich G.F., Collins A.M., and Williams V.P. Antioxidant enzymes in the honeybee. Apis mellifera L. Apidologie 33 (2002) 3-14
67. Xue L., and Noll M. Drosophila female sexual behavior induced by sterile males showing copulation complementation. Proceedings of the National Academy of Sciences USA 97 (2000) 3272-3275