Seminal fluid protein depletion and replenishment in the fruit fly, Drosophila melanogaster: An ELISA-based method for tracking individual ejaculates

Behavioral Ecology and Sociobiology

Volumn 63, Issue 10, 2009, Pages 1505-1513

  Sirot, Laura K ^a   Buehner, Norene A ^a   Fiumera, Anthony C ^b   Wolfner, Mariana F ^a  

^a Department of Obstetrics Gynecology   (United States)

^b BINGHAMTON UNIVERSITY   (United States)

Author keywords

Drosophila melanogaster; Ejaculate quantification; Ovulin; Reproductive investment; Sex peptide

Indexed keywords

ADAPTATION; ANTIBODY; BIOASSAY; EGG PRODUCTION; FEEDING BEHAVIOR; FLY; IMMUNOASSAY; MATING BEHAVIOR; PEPTIDE; PROTEIN; REPRODUCTIVE SUCCESS; SPERM;

ANIMALIA; DROSOPHILA MELANOGASTER;

EID: 70349993080     PISSN: 03405443     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00265-009-0806-6     Document Type: Article

References (66)

1. Andersson J, Borg-Karlson AK, Wiklund C (2004) Sexual conflict and anti-aphrodisiac titre in a polyandrous butterfly: male ejaculate tailoring and absence of female control. Proc Roy Soc Lond B 271:1765-1770.
2. Bertram MJ, Akerkar GA, Ard GA, Gonzalez C, Wolfner MF (1992) Cell type-specific gene expression in the Drosophila melanogaster accessory gland. Mech Devel 38:33-40.
3. Bertram MJ, Neubaum DM, Wolfner MF (1996) Localization of the Drosophila male accessory gland proteins Acp36DE in the mated female suggests a role for sperm storage. Insect Biochem Mol Biol 26:971-980.
4. Bissoondath CJ, Wiklund C (1996) Effect of male mating history and body size on ejaculate size and quality in two polyandrous butterflies, Pieris napi and Pieris rapae (Lepidoptera: Pieridae). Func Ecol 10:457-464.
5. Bloch Qazi MC, Wolfner MF (2003) An early role for Drosophila melanogaster male seminal protein Acp36DE in female sperm storage. J Exp Biol 206:3521-3528.
6. Braswell WE, Andrés JA, Maroja LS, Harrison RG, Howard DJ, Swanson WJ (2006) Identification and comparative analysis of accessory gland proteins in Orthoptera. Genome 49:1069-1080.
7. Bretman AJ, Fricke C, Chapman T (2009) Plastic responses of male Drosophila melanogaster to the level of sperm competition increase male reproductive fitness. Proc Roy Soc Lond B 276:1705-1711.
8. Carter DB, Timmins JG, Adams LD, Lewis RW, Karr JP, Resnick MI, Buhl AE (1985) The antigenic relatedness of proteins from human and simian prostate fluid. Prostate 6:395-402.
9. Carvalho GB, Kapahi P, Anderson DJ, Benzer S (2006) Allocrine modulation of feeding behavior by the sex peptide of Drosophila. Curr Biol 16:692-696.
10. Cattini R, Robinson D, Gill O, Jolley N, Bacaresehamilton T (1994) Measurement of prostate specific antigen in serum using 4 different immunoassays. Eur J Clin Chem Clin Biochem 32:181-185.
11. Chapman T, Bangham J, Vinti G, Seifried B, Lung O, Wolfner MF, Smith HK, Partridge L (2003) The sex peptide of Drosophila melanogaster: female post-mating responses analyzed by using RNA interference. Proc Natl Acad Sci USA 100:9923-9928.
12. Clark NL, Swanson WJ (2005) Pervasive adaptive evolution in primate seminal proteins. Plos Genet 1:335-342.
13. Coleman S, Drahn B, Petersen G, Stolorov J, Kraus K (1995) A Drosophila male accessory-gland protein that is a member of the serpin superfamily of proteinase-inhibitors is transferred to females during mating. Insect Biochem Mol Biol 25:203-207.
14. Collins AM, Caperna TJ, Williams V, Garrett WM, Evans JD (2006) Proteomic analyses of male contributions to honey bee sperm storage and mating. Insect Mol Biol 15:541-549.
15. Davies SJ, Chapman T (2006) Identification of genes expressed in the accessory glands of male Mediterranean Fruit Flies (Ceratitis capitata). Insect Biochem Mol Biol 36:846-856.
16. DiBenedetto AJ, Harada HA, Wolfner MF (1990) Structure, cell-specific expression and mating-induced regulation of a Drosophila melanogaster male accessory-gland gene. Devel Biol 139:134-148.
17. Dottorini T, Nicolaides L, Ranson H, Rogers DW, Crisanti A, Catteruccia F (2007) A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior. Proc Natl Acad Sci USA 104:16215-16220.
18. Friberg U (2006) Male perception of female mating status: its effect on copulation duration, sperm defence and female fitness. Anim Behav 72:1259-1268.
19. Gillott C (2003) Male accessory gland secretions: Modulators of female reproductive physiology and behavior. Annu Rev Entomol 48:163-184.
20. Gonzalez A, Rossini C, Eisner M, Eisner T (1999) Sexually transmitted chemical defense in a moth (Utetheisa ornatrix). Proc Natl Acad Sci USA 96:5570-5574.
21. Griffin TJ, Gygi SP, Ideker T, Rist B, Eng J, Hood L, Aebersold R (2002) Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol Cell Proteom 1:323-333.
22. Harshman LG, Clark AG (1998) Inference of sperm competition from broods of field-caught Drosophila. Evol 52:1334-1341.
23. Heifetz Y, Lung O, Frongillo EA, Wolfner MF (2000) The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr Biol 10:99-102.
24. Herndon LA, Wolfner MF (1995) A Drosophila seminal fluid protein, Acp26Aa, stimulates egg-laying in females for 1 day after mating. Proc Natl Acad Sci USA 92:10114-10118.
25. Herndon LA, Chapman T, Kalb JM, Lewin S, Partridge L, Wolfner MF (1997) Mating and hormonal triggers regulate accessory gland gene expression in male Drosophila. J Insect Physiol 43:1117-1123.
26. Hihara F (1981) Effects of the male accessory gland secretion on oviposition and re-mating in females of Drosophila melanogaster. Zool Mag (Tokyo) 90:307-316.
27. Ignotz GG, Cho MY, Suarez SS (2007) Annexins are candidate oviductal receptors for bovine sperm surface proteins and thus may serve to hold bovine sperm in the oviductal reservoir. Biol Reprod 77:906-913.
28. Linklater JR, Wertheim B, Wigby S, Chapman T (2007) Ejaculate depletion patterns evolve in response to experimental manipulation of sex ratio in Drosophila melanogaster. Evol 61:2027-2034.
29. Liu HF, Kubli E (2003) Sex-peptide is the molecular basis of the sperm effect in Drosophila melanogaster. Proc Natl Acad Sci USA 100:9929-9933.
30. Lung O, Wolfner MF (1999) Drosophila seminal fluid proteins enter the circulatory system of the mated female fly by crossing the posterior vaginal wall. Insect Biochem Mol Biol 29:1043-1052.
31. Lung O, Wolfner MF (2001) Identification and characterization of the major Drosophila melanogaster mating plug protein. Insect Biochem Mol Biol 31:543-551.
32. McGraw LA, Fiumera AC, Ramakrishnan M, Madhavarapu S, Clark AG, Wolfner MF (2007) Larval rearing environment affects several post-copulatory traits in Drosophila melanogaster. Biol Lett 3:607-610.
33. Monsma SA, Harada HA, Wolfner MF (1990) Synthesis of 2 Drosophila male accessory gland proteins and their fate after transfer to the female during mating. Devel Biol 142:465-475.
34. Moura AA, Chapman DA, Koc H, Killian GJ (2007) A comprehensive proteomic analysis of the accessory sex gland fluid from mature Holstein bulls. Anim Reprod Sci 98:169-188.
35. Neubaum DM, Wolfner MF (1999) Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics 153:845-857.
36. Peng J, Chen S, Busser S, Liu HF, Honegger T, Kubli E (2005) Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr Biol 15:207-213.
37. Perez-Staples D, Aluja M, Macias-Ordonez R, Sivinski J (2008) Reproductive trade-offs from mating with a successful male: the case of the tephritid fly Anastrepha obliqua. Behav Ecol Sociobiol 62:1333-1340.
38. Pilch B, Mann M (2006) Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome Biol 7:R40.
39. Pilpel N, Nezer I, Applebaum SW, Heifetz Y (2008) Mating increases trypsin in female Drosophila hemolymph. Insect Biochem Mol Biol 38:320-330.
40. Pitnick S, Markow TA (1994) Male gametic strategies-sperm size, testes size, and the allocation of ejaculate among success mates by the sperm-limited fly Drosophila pachea and its relatives. Am Nat 143:785-819.
41. Poiani A (2006) Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60:289-310.
42. Radhakrishnan P, Taylor PW (2008) Ability of male Queensland fruit flies to inhibit receptivity in multiple mates, and the associated recovery of accessory glands. J Insect Physiol 54:421-428.
43. Ravi Ram K, Wolfner MF (2007) Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr Comp Biol 47:427-445.
44. Ravi Ram K, Ji S, Wolfner MF (2005) Fates and targets of male accessory gland proteins in mated female Drosophila melanogaster. Insect Biochem Mol Biol 35:1059-1071.
45. Ravi Ram K, Sirot LK, Wolfner MF (2006) Predicted seminal astacin-like protease is required for processing of reproductive proteins in Drosophila melanogaster. Proc Natl Acad Sci USA 103:18674-18679.
46. + antiporter (NHA) from a metazoan, Anopheles gambiae. J Exp Biol 210:3848-3861.
47. Robertson SA (2005) Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res 322:43-52.
48. Robertson SA (2007) Seminal fluid signaling in the female reproductive tract: Lessons from rodents and pigs. J Anim Sci 85:E36-E44.
49. Rogers DW, Chapman T, Fowler K, Pomiankowski A (2005) Mating-induced reduction in accessory reproductive organ size in the stalk-eyed fly Cyrtodiopsis dalmanni. BMC Evol Biol 18:642-650.
50. Savalli UM, Fox CW (1999) The effect of male size, age, and mating behavior on sexual selection in the seed beetle Callosobruchus maculatus. Ethol Ecol Evol 11:49-60.
51. Schmidt T, Chen PS, Pellegrini M (1985) The induction of ribosome biosynthesis in a nonmitotic secretory tissue. J Biol Chem 280:7645-7650.
52. Simmerl E, Schäfer M, Schäfer U (1995) Structure and regulation of a gene cluster for male accessory gland transcripts in Drosophila melanogaster. Insect Biochem Mol Biol 25:127-137.
53. Sirot LK, Poulson RL, McKenna MC, Girnary H, Wolfner MF, Harrington LC (2008) 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 38:176-189.
54. Smith PH, Gillott C, Browne LB, Vangerwen ACM (1990) The mating induced refractoriness of Lucilia cuprina females- manipulating the male contribution. Physiol Entomol 15:469-481.
55. Styger D (1992) Molekulare analyse des sexpeptidgens aus Drosophila melanogaster. Dissertation, University of Zurich.
56. Svärd L, Wiklund C (1986) Different ejaculate delivery strategies in 1st versus subsequent matings in the swallowtail butterfly Papilio machaon L. Behav Ecol Sociobiol 18:325-330.
57. Svärd L, Wiklund C (1989) Mass and production rate of ejaculates in relation to monandry and polyandry in butterflies. Behav Ecol Sociobiol 24:395-402.
58. Torres-Vila LM, Jennions MD (2005) Male mating history and female fecundity in the Lepidoptera: do male virgins make better partners? Behav Ecol Sociobiol 57:318-326.
59. Tripet F, Toure YT, Dolo G, Lanzaro GC (2003) Frequency of multiple inseminations in field-collected Anopheles gambiae females revealed by DNA analysis of transferred sperm. Am J Trop Med Hyg 68:1-5.
60. Vahed K (2007) Comparative evidence for a cost to males of manipulating females in bushcrickets. Behav Ecol 18:499-506.
61. Veveris-Lowe TL, Kruger SJ, Walsh T, Gardiner RA, Clements JA (2007) Seminal fluid characterization for male fertility and prostate cancer: Kallikrein-related serine proteases and whole proteome approaches. Semin Thromb Hemost 33:87-99.
62. Walters JR, Harrison RG (2008) EST analysis of male accessory glands from Heliconius butterflies with divergent mating systems. BMC Genomics 9:592.
63. Wedell N, Gage MJG, Parker GA (2002) Sperm competition, male prudence and sperm-limited females. Trends Ecol Evol 17:313-320.
64. Whittier TS, Kaneshiro KY (1991) Male mating success and female fitness in the Mediterranean fruit-fly (Diptera, Tephritidae). Ann Entomol Soc Am 84:608-611.
65. Wigby S, Sirot LK, Linklater JR, Buehner N, Calboli FCF, Bretman A, Wolfner MF, Chapman T (2009) Seminal fluid proteins allocation and reproductive success. Curr Biol 19:1-7.
66. Wojtczak M, Calka J, Glogowski J, Ciereszko A (2007) Isolation and characterization of alpha 1-proteinase inhibitor from common carp (Cyprinus carpio) seminal plasma. Comp Biochem Physiol B 148:264-276.