A nonsemen copulatory fluid influences the outcome of sperm competition in Japanese quail

Journal of Evolutionary Biology

Volumn 26, Issue 9, 2013, Pages 1875-1889

  Finseth, F R ^a   Iacovelli, S R ^a   Harrison, R G ^a   Adkins Regan, E K ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Ejaculate evolution; Foam gland; Japanese quail; Post copulatory sexual selection; Seminal fluid proteins; Sperm competition

Indexed keywords

BEHAVIORAL RESPONSE; BIRD; COPULATION; DIVERGENCE; FERTILIZATION (REPRODUCTION); FLUID; MALE; SEXUAL SELECTION; SPERM COMPETITION;

COTURNIX JAPONICA;

ANIMAL; ARTICLE; CHEMISTRY; COPULATION; COTURNIX; COTURNIX JAPONICA; EJACULATE EVOLUTION; EXOCRINE GLAND; EXTRACELLULAR FLUID; FEMALE; FERTILIZATION; FOAM GLAND; GENETIC SELECTION; GENOTYPE; HISTOLOGY; MALE; PHYSIOLOGY; POST-COPULATORY SEXUAL SELECTION; SEMINAL FLUID PROTEINS; SPERM COMPETITION; SPERMATOZOON;

EJACULATE EVOLUTION; FOAM GLAND; JAPANESE QUAIL; POST-COPULATORY SEXUAL SELECTION; SEMINAL FLUID PROTEINS; SPERM COMPETITION;

ANIMALS; COPULATION; COTURNIX; EXOCRINE GLANDS; EXTRACELLULAR FLUID; FEMALE; FERTILIZATION; GENOTYPE; MALE; SELECTION, GENETIC; SPERMATOZOA;

EID: 84882597144     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/jeb.12189     Document Type: Article

References (90)

1. Adkins-Regan, E. 1995. Predictors of fertilization in the Japanese quail, Coturnix japonica. Anim. Behav. 50: 1405-1415.
2. Adkins-Regan, E. 1999. Foam produced by male Coturnix quail: What is its function? Auk 116: 184-193.
3. Alonzo, S.H. & Pizzari, T. 2010. Male fecundity stimulation: conflict and cooperation within and between the sexes: model analyses and coevolutionary dynamics. Am. Nat. 175: 174-185.
4. Andersson, M.B. 1994. Sexual selection. Princeton University Press, Princeton, NJ.
5. Bates, D., Maechler, M. & Bolker, B. 2012. lme4: linear mixed-effects models using S4 classes. R package version 0.999999-0. http://CRAN.R-project.org/package=lme4.
6. Birkhead, T.R. 1998. Sperm competition in birds. Rev. Reprod. 3: 123-129.
7. Birkhead, T.R. 2010. How stupid not to have thought of that: post-copulatory sexual selection. J. Zool. 281: 78-93.
8. Birkhead, T.R. & Fletcher, F. 1994a. Numbers of spermatozoa attached to and penetrating perivitelline layers of Japanese quail eggs. Auk 111: 997-1000.
9. Birkhead, T.R. & Fletcher, F. 1994b. Sperm storage and the release of sperm from the sperm storage tubules in Japanese quail Coturnix japonica. Ibis 136: 101-104.
10. Birkhead, T.R. & Fletcher, F. 1995. Male phenotype and ejaculate quality in the zebra finch Taeniopygia guttata. Proc. R. Soc. Lond. B Biol. Sci. 262: 329-334.
11. Birkhead, T.R. & Møller, A.P. 1998. Sperm competition and sexual selection. Academic Press, San Diego.
12. Birkhead, T.R. & Pizzari, T. 2002. Postcopulatory sexual selection. Nat. Rev. Genet. 3: 262-273.
13. Birkhead, T.R., Martinez, J.G., Burke, T. & Froman, D.P. 1999. Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc. R. Soc. Lond. B Biol. Sci. 266: 1759-1764.
14. Biswas, A., Ranganatha, O., Mohan, J. & Sastry, K. 2007. Relationship of cloacal gland with testes, testosterone and fertility in different lines of male Japanese quail. Anim. Reprod. Sci. 97: 94-102.
15. Biswas, A., Ranganatha, O.S. & Mohan, J. 2010. The effect of different foam concentrations on sperm motility in Japanese quail. Vet. Med. Int. 2010: 1-4.
16. Boutin-Ganache, I., Raposo, M., Raymond, M. & Deschepper, C.F. 2001. M13-tailed primers improve the readability and usability of microsatellite analyses performed with two different allele-sizing methods. Biotechniques 31: 24-26, 28.
17. Brillard, J.P. & Antoine, H. 1990. Storage of sperm in the uterovaginal junction and its incidence on the numbers of spermatozoa present in the perivitelline layer of hens' eggs. Br. Poult. Sci. 31: 635-644.
18. Cameron, E., Day, T. & Rowe, L. 2007. Sperm competition and the evolution of ejaculate composition. Am. Nat. 169: E158-E172.
19. Chapman, T. 2001. Seminal fluid-mediated fitness traits in Drosophila. Heredity 87: 511-521.
20. Chapman, T. & Davies, S. 2004. Functions and analysis of the seminal fluid proteins of male Drosophila melanogaster fruit flies. Peptides 25: 1477-1490.
21. Chapman, T., Neubaum, D.M., Wolfner, M.F. & Partridge, L. 2000. The role of male accessory gland protein Acp36DE in sperm competition in Drosophila melanogaster. Proc. R. Soc. Lond. B Biol. Sci. 267: 1097-1105.
22. Cheng, K.M., Hickman, A.R. & Nichols, C.R. 1989a. Role of the proctodeal gland foam of male Japanese quail in natural copulations. Auk 106: 279-285.
23. Cheng, K.M., McIntyre, R.F. & Hickman, A.R. 1989b. Proctodeal gland foam enhances competitive fertilization in domestic Japanese quail. Auk 106: 286-291.
24. Clark, A.G., Aguade, M., Prout, T., Harshman, L.G. & Langley, C.H. 1995. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics 139: 189-201.
25. Clark, A.G., Begun, D.J. & Prout, T. 1999. Female x male interactions in Drosophila sperm competition. Science 238: 217-220.
26. Clulow, J. & Jones, R. 1982. Production, transport, maturation, storage and survival of spermatozoa in the male Japanese quail, Coturnix coturnix. J. Reprod. Fertil. 64: 259-266. Soc Reprod Fertility.
27. Coil, W.H. & Wetherbee, D.K. 1959. Observations on the cloacal gland of the Eurasian quail Coturnix coturnix. Ohio. J Sci. 59: 268-270.
28. Cornwallis, C.K. & O'Connor, E.A. 2009. Sperm: seminal fluid interactions and the adjustment of sperm quality in relation to female attractiveness. Proc. R. Soc. Lond. B. Biol. Sci. 276: 3467-3475.
29. Dean, M.D., Findlay, G.D., Hoopman, M.R., Wu, C.C., MacCoss, M.J., Swanson, W.J., et al. 2011. Identification of ejaculated proteins in the house mouse (Mus domesticus) via isotopic labeling. BMC Genomics 12: 306.
30. Delville, Y., Sulon, J. & Balthazart, J. 1986. Diurnal variations of sexual receptivity in the female Japanese quail (Coturnix coturnix japonica). Horm. Behav. 20: 13-33.
31. Fedorka, K.M., Winterhalter, W.E. & Ware, B. 2010. Perceived sperm competition intensity influences seminal fluid protein production prior to courtship and mating. Evolution 65: 584-590.
32. Froman, D.P., Pizzari, T., Feltmann, A.J., Castillo-Juarez, H. & Birkhead, T.R. 2002. Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc. R. Soc. Lond. B. Biol. Sci. 269: 607-612.
33. Gilchrist, A. & Partridge, L. 1995. Male identity and sperm displacement in Drosophila melanogaster. J. Insect Physiol. 41: 1087-1092.
34. Harrell, F.E. Jr, 2012. Hmisc: Harrell Miscellaneous. R package version 3.10-1, URL: http://biostat.mc.vanderbilt.edu/Hmisc
35. Harshman, L.G. & Prout, T. 1994. Sperm displacement without sperm transfer in Drosophila melanogaster. Evolution 48: 758-766.
36. Hinton, H.E. 1964. Sperm transfer in insects and the evolution of haemocoelic insemination. In: Insect Reproduction (K.C. Highnam, ed.), pp. 95-107. Symp. Roy. Entomol. Soc. Lond. 2.
37. Hodgson, D.J. & Hosken, D.J. 2006. Sperm competition promotes the exploitation of rival ejaculates. J. Theor. Biol. 243: 230-234.
38. Ikeda, K. & Taji, K. 1954. On the foamy ejaculate of Japanese quail, Coturnix coturnix japonica. Scientific reports of the Matsuyama agricultural college 13: 1-4.
39. Kayang, B., Inoue-Murayama, M., Nomura, A., Kimura, K., Takahashi, H., Kimura, K., et al. 2000. Fifty microsatellite markers for Japanese quail. J. Hered. 91: 502-505.
40. Kayang, B., Inoue-Murayama, M., Hoshi, T., Matsuo, K., Takahashi, H., Minezawa, M., et al. 2002. Microsatellite loci in Japanese quail and cross-species amplification in chicken and guinea fowl. Genet. Sel. Evol. 34: 233.
41. Kilgallon, S.J. & Simmons, L.W. 2005. Image content influences men's semen quality. Biol. Lett. 1: 253-255.
42. King, A.S. 1981. Cloaca. In: Form and function in birds (A.S. King & J. McLelland, eds), pp. 63-105. Academic Press, New York.
43. Klemm, R., Knight, C.E. & Stein, S. 1973. Gross and microscopic morphology of glandula proctodealis (foam gland) of Coturnix c. japonica (aves). J. Morphol. 141: 171-184.
44. Korn, N., Thurston, R., Pooser, B. & Scott, T. 2000. Ultrastructure of spermatozoa from Japanese quail. Poult. Sci. 79: 407-414.
45. Lake, P. 1981. Male genital organs. In: Form and function in birds (A.S. King & J. McLelland, eds), pp. 1-61. Academic Press, London.
46. Lemaitre, J.F., Ramm, S.A., Hurst, J.L. & Stockley, P. 2011. Social cues of sperm competition influence accessory reproductive gland size in a promiscuous mammal. Proc. R. Soc. Lond. B Biol. Sci. 278: 1171-1176.
47. Locatello, L., Poli, F. & Rasotto, M.B. 2013. Tactic-specific differences in seminal fluid influence sperm performance. Proc. R. Soc. Lond. B Biol. Sci. 280: 20122891.
48. Marks, H. & Lepore, P. 1965a. A procedure for artificial insemination of Japanese quail. Poult. Sci. 44: 1001-1003.
49. Marks, H. & Lepore, P. 1965b. A simple intravaginal technique for artificial insemination of Japanese quail. Poult. Sci. 44: 1396.
50. Marshall, T.C., Slate, J., Kruuk, L.E. & Pemberton, J.M. 1998. Statistical confidence for likelihood-based paternity inference in natural populations. Mol. Ecol. 7: 639-655.
51. McFarquhar, A.M. & Lake, P.E. 1964. Artificial insemination in quail and the production of chicken-quail hybrids. J. Reprod. Fertil. 8: 261-263. Soc Reprod Fertility.
52. Mohan, J., Moudgal, R., Sastry, K., Tyagi, J. & Singh, R. 2002. Effects of hemicastration and castration on foam production and its relationship with fertility in male Japanese quail. Theriogenology 58: 29-39.
53. Møller, A.P. 1991. Sperm competition, sperm depletion, paternal care, and relative testis size in birds. Am. Nat. 137: 882-906.
54. Neubaum, D.M. & Wolfner, M.F. 1999. Mated Drosophila melanogaster females require a seminal fluid protein, Acp36DE, to store sperm efficiently. Genetics 153: 845-857.
55. Nichols, C.R. 1991. A comparison of the reproductive and behavioural differences of feral and domestic Japanese quail. University of British Columbia, masters thesis.
56. Ogasawara, F.X. & Huang, R. 1963. A modified method of artificial insemination in the production of chicken-quail hybrids. Poult. Sci. 42: 1386-1392. Poultry Science Association.
57. Parker, G.A. 1970. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 45: 525-567.
58. Parker, G.A. 1998. Sperm competition and the evolution of ejaculates: towards a theory base. In: Sperm competition and sexual selection (T.R. Birkhead & A.P. Møller, eds), pp. 3-49. Academic Press, San Diego.
59. Parker, G.A. & Pizzari, T. 2010. Sperm competition and ejaculate economics. Biol. Rev. 85: 897-934.
60. Peng, J., Chen, S., Büsser, S., Liu, H., Honegger, T. & Kubli, E. 2005. Gradual release of sperm bound sex-peptide controls female postmating behavior in Drosophila. Curr. Biol. 15: 207-213.
61. Perry, J.C. & Rowe, L. 2010. Condition-dependent ejaculate size and composition in a ladybird beetle. Proc. R. Soc. Lond. B Biol. Sci. 277: 3639-3647.
62. Pitnick, S., Wolfner, M.F. & Suarez, S.S. 2008. Ejacu-late-female and sperm-female interactions. In: Sperm Biology: An evolutionary perspective (T.R. Birkhead, D.J. Hosken & S. Pitnick, eds), pp. 247-304. Academic Press, London.
63. Pizzari, T. & Parker, G.A. 2008. Sperm competition and sperm phenotype. In: Sperm Biology: An evolutionary perspective (T.R. Birkhead, D.J. Hosken & S. Pitnick, eds), pp. 207-245. Academic Press, London.
64. Pizzari, T., Cornwallis, C.K. & Froman, D.P. 2007. Social competitiveness associated with rapid fluctuations in sperm quality in male fowl. Proc. R. Soc. Lond. B Biol. Sci. 274: 853-860.
65. Pizzari, T., Worley, K., Burke, T. & Froman, D.P. 2008. Sperm competition dynamics: ejaculate fertilising efficiency changes differentially with time. BMC Evol. Biol. 8: 33.
66. Poiani, A. 2006. Complexity of seminal fluid: a review. Behav. Ecol. Sociobiol. 60: 289-310.
67. Prout, T. & Clark, A.G. 2000. Seminal fluid causes temporarily reduced egg hatch in previously mated females. Proc. R. Soc. Lond. B Biol. Sci. 267: 201-203.
68. R Core Team 2012. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.
69. Ram, K.R. & Wolfner, M.F. 2005. Sustained post-mating response in Drosophila melanogaster requires multiple seminal fluid proteins. PLoS Genet. 3: 2428-2438.
70. Ram, K.R. & Wolfner, M. 2007. Seminal influences: Drosophila Acps and the molecular interplay between males and females during reproduction. Integr. Comp. Biol. 47: 427-445.
71. Ram, K.R. & Wolfner, M.F. 2009. A network of interactions among seminal proteins underlies the long-term postmating response in Drosophila. Proc. Natl. Acad. Sci. 106: 15384-15389.
72. Ramm, S.A., Parker, G.A. & Stockley, P. 2005. Sperm competition and the evolution of male reproductive anatomy in rodents. Proc. R. Soc. Lond. B Biol. Sci. 272: 949-955.
73. Seiwert, C. & Adkins-Regan, E. 1998. The foam production system of the male Japanese quail: Characterization of structure and function. Brain Behav. Evol. 52: 61-80.
74. Simmons, L.W. 2001. Sperm Competition and Its Evolutionary Consequences in the Insects. Princeton University Press, Princeton, NJ.
75. Simmons, L. & Fitzpatrick, J. 2012. Sperm wars and the evolution of male fertility. Reproduction 144: 519-534.
76. Singh, R.P., Sastry, K.V.H., Pandey, N.K., Shit, N., Singh, R. & Mohan, J. 2011a. Sperm competition in Japanese quail (Coturnix japonica): Last male precedence is declined in two successive matings with two different males. Indian. J. Poult. Sci. 46: 130-131.
77. Singh, R.P., Sastry, K.V.H., Shit, N., Pandey, N.K., Singh, K.B., Mohan, J., et al. 2011b. Cloacal gland foam enhances motility and disaggregation of spermatozoa in Japanese quail (Coturnix japonica). Theriogenology 75: 563-569.
78. Singh, R.P., Sastry, K.V.H., Pandey, N.K., Singh, K.B., Malecki, I.A., Farooq, U., et al. 2012. The role of the male cloacal gland in reproductive success in Japanese quail (Coturnix japonica). Reprod. Fertil. Dev. 24: 405.
79. Sirot, L.K., Laflamme, B.A., Sitnik, J.L., Rubinstein, C.D., Avila, F.W., Chow, C.Y., et al. 2009. Molecular social interactions: Drosophila melanogaster seminal fluid proteins as a case study. Adv. Genet. 68: 23-56.
80. Sirot, L.K., Wolfner, M.F. & Wigby, S. 2011. Protein-specific manipulation of ejaculate composition in response to female mating status in Drosophila melanogaster. Proc. Natl. Acad. Sci. 108: 9922-9926.
81. Sittmann, K. & Abplanalp, H. 1965. Duration and recovery of fertility in Japanese quail (Coturnix coturnix japonica). Br. Poult. Sci. 6: 245-250.
82. Smith, C.C. & Ryan, M.J. 2011. Tactic-dependent plasticity in ejaculate traits in the swordtail Xiphophorus nigrensis. Biol. Lett. 7: 733-735.
83. Snook, R. 2005. Sperm in competition: not playing by the numbers. Trends Ecol. Evol. 20: 46-53.
84. Teijeiro, J.R., Puigcerver, M. & Gallego, S. 2003. Pair bonding and multiple paternity in the polygamous common quail Coturnix coturnix. Ethology 109: 291-302.
85. Wentworth, B.C. & Mellen, W.J. 1963. Egg production and fertility following various methods of insemination in Japanese quail (Coturnix coturnix japonica). J. Reprod. Fertil. 6: 215-220. Soc Reprod Fertility.
86. Wickham, H. 2009. ggplot2: elegant graphics for data analysis. Springer Publishing Company, Incorporated.
87. Wigby, S., Sirot, L.K., Linklater, J.R., Buehner, N., Calboli, F.C.F., Bretman, A., et al. 2009. Seminal fluid protein allocation and male reproductive success. Curr. Biol. 19: 751-757.
88. Wilson, W.O. & Huang, R.H. 1962. A comparison of the time of ovipositing for Coturnix and chicken. Poult. Sci. 41: 1843-1845. Poultry Science Association.
89. Wilson, W.O., Abbott, U.K. & Abplanalp, H. 1961. Evaluation of Coturnix (Japanese quail) as pilot animal for poultry. Poult. Sci. 40: 651-657. Poultry Science Association.
90. Wolfner, M.F. 1997. Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochem. Mol. Biol. 27: 179-192.