Female Remating, Sperm Competition and Sexual Selection in Drosophila

Singh, Dr. Shree Ram and Singh, Dr. B N and Hoenigsberg, Dr. H F (2002) Female Remating, Sperm Competition and Sexual Selection in Drosophila. [Journal (Paginated)] (In Press)

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Female remating is the fundamental to evolutionary biology as it determines the pattern of sexual selection and sexual conflict. Remating in females is an important component of Drosophila mating systems because it is associated with pattern of sperm usage and sexual selection. Remating is common in females of many species of Drosophila in both natural and laboratory populations. It is reported in many insect species and vertebrates also. Female remating is prerequisite for the occurrence of sperm competition between the males and the consequences of this competition such as sperm precedence or sperm displacement have also been reported in many species of Drosophila. Female remating is dependent on the amount of sperm stored, the components of male seminal fluid, the level of nutrition and egg-laying, in laboratory by different experimental designs and density of flies. Remating by female is an insurance against male sterility and sub-fertility and result in increasing the genetic heterogeneity of a female offspring. Remating results in greater productivity in females of many species of Drosophila. In this paper we review the female remating with respect to sperm competition and sexual selection in Drosophila and have given the possible female’s benefits of remating. We also review the role of accessory gland fluid in remating, cost associated with remating and genetic basis of female remating and some possible mechanisms of sperm competition in the light of last male sperm priority and paternity assurance in Drosophila and other insects. We have also suggested the future area of research.

Item Type:Journal (Paginated)
Keywords:female remating, Drosophila, sperm competition, sexual selection, multiple mating, sperm precedence, remating speed, male accessory gland, human sperm competition
Subjects:Biology > Evolution
ID Code:2360
Deposited By:Singh, Shree Ram
Deposited On:04 Aug 2002
Last Modified:11 Mar 2011 08:54

References in Article

Select the SEEK icon to attempt to find the referenced article. If it does not appear to be in cogprints you will be forwarded to the paracite service. Poorly formated references will probably not work.


1. Darwin, C. (1859). On the Origin of Species by Means of Natural Selection. John Murray,


2. Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. John Murray, London.

3. Parker, G. A. (1970). Sperm competition and its evolutionary consequences in the insects.

Biological Reviews, 45: 525-568.

4. Eberhard, W. G. (1996). Female control: Sexual Selection by Cryptic Female Choice.

Princeton Univ. Press, Princeton, NJ.

5. Møller, A. P. (1994). Sexual Selection and the Barn Swallow. Oxford University Press, Oxford.

6. Hoenigsberg, H. F. (1960). Sexual behavior: a discussion. Evolution 14: 527-528.

7. Singh, S.R. and Singh, B.N. (2000). Male remating in Drosophila ananassae: Evidence for

interstrain variation in remating time and shorter duration of copulation during second mating.

Zool. Sci. 17: 389-393.

8. Arnquist, G. and Nilson, T. (2000). The evolution of polyandry: Multiple mating and female

fitness in insects. Anim. Behav. 60: 145-164.

9. Pitnick, S., Markow, T. and Spicer, G. S. (1999). Evolution of multiple kinds of female spermstorage

organs in Drosophila. Evolution 53: 1804-1822.

10. Tram, U. and Wolfner, M. F. (1999). Male seminal fluid proteins are essential for sperm

storage in Drosophila melanogaster. Genetics 153: 837-844.

11. Neubaum, D. M. and Wolfner, M. F. (1999). Mated Drosophila melanogaster females require

a seminal fluid protein, Acp 36PE to store sperm efficiently. Genetics 153: 845-857.

12. Wolfner, M. F. (1997). Tokens of love: Functions and regulation of Drosophila male accessory

gland products. Insect Biochem. Mol. Biol. 27: 179-192.

13. Manning, A. (1962). A sperm factor affecting the receptivity of Drosophila melanogaster

females. Nature 194: 252-253.

14. Lefevre, G. and Jonsson, U. B. (1962). Sperm transfer, storage, displacement and utilization in

Drosophila melanogaster. Genetics 47: 1719-1736.

15. Tram, U. and Wolfner, M. F. (1998). Seminal fluid regulation of female sexual attractiveness

in Drosophila melanogaster. Proc. Nat. Acad. Sci. USA 95: 4051-4054.

16. Tompkins, L., Gross, A. C., Hall, J. C., Gailey, D. A. and Siegel, R. W. (1982). The role of

female movement in the sexual behavior of Drosophila melanogaster. Behav. Genet. 12: 295-


17. Fuyama, Y. (1995). Genetic evidence that ovulation reduces sexual receptivity in Drosophila

melanogaster females. Behav. Genet. 25: 581-587.

18. Ringo, J. (1996). Sexual receptivity in insects. Ann. Rev. Entomol. 41: 473-494.

19. Heifetz, Y., Tram, U., and Wofner, M F. (2001). Male contributions to egg production: the role

of accessory gland products and sperm in Drosophila melanogaster. Proc. R. Soc. Lond. B 268:


20. Gromko, M. H., Gilbert, D. G. and Richmond, R. C. (1984). Sperm transfer and use in the

multiple mating system of Drosophila. In: Sperm Competition and the Evolution of Animal

Mating Systems (Smith, R. L., ed.). Academic Press, New York, pp. 372-427.

21. Chapman, T., Liddle, L. F., Kalb, J. M., Wolfner, M. F. and Partridge, L. (1995). Cost of

mating in Drosophila melanogaster females is mediated by male accessory gland products.

Nature 373: 241-244.

22. Sgro, C. M. and Partridge, L. (1999). A delayed wave of death from reproduction in

Drosophila. Science 286: 2521-2524.

23. Scott, D. (1987). The timing of the sperm effect on female Drosophila melanogaster receptivity.

Anim. Behav. 35: 142-149.

24. Tompkins, L. and Hall, J. C. (1983). Identification of brain sites controlling female receptivity

in mosaics of Drosophila melanogaster. Genetics 103: 179-195.

25. Levine, L., Asmussen, M., Olvera, O., Powell, J. R., Delarosa, M. E., Salceda, V. M., Gaso,

M. I., Gujman, J. and Anderson, W. W. (1980). Population genetics of Mexican Drosophila.

V. A high rate of multiple insemination in a natural population of Drosophila pseudoobscura.

Am. Nat. 116: 493-503.

26. Richmond, R. C. and Powell, J. R. (1970). Evidence of heterosis associated with an enzyme

locus in a natural population. Proc. Natl. Acad. Sci. USA 67: 1264-1267.

27. Milkman, R. and Zeitler, R. R. (1974). Concurrent multiple paternity in natural populations of

Drosophila melanogaster. Genetics 78: 1191-1193.

28. Ikeda, H. (1974). Multiple copulation: An abnormal mating behaviour, which deleteriously

affects fitness in Drosophila mercatorum. Mem. Ehime. Univ. Sci. Ser. B 3: 18-28.

29. Anderson, W. W. (1974). Frequent multiple insemination in a natural population of Drosophila

pseudoobscura. Am. Nat. 108: 709-711.

30. Richmond, R. C. and Ehrman, L. (1974). The incidence of repeated mating in the superspecies

Drosophila paulistorum. Experientia 30: 489-490.

31. Richmond, R. C. (1976). Frequency of multiple insemination in natural populations of

Drosophila. Am. Nat. 110 :485-486.

32. Stalker, H. D. (1976). Enzymes and reproduction in natural populations of Drosophila

euronotus. Genetics 84: 375-384.

33. Prout, T. and Bundgaard, J. (1977). The population genetics of sperm displacement. Genetics

85: 95-124.

34. Cobbs, G. (1977) Multiple insemination and male sexual selection in natural population of

Drosophila pseudoobscura. Am. Nat. 111: 641-656.

35. Craddock, E. M. and Johnson, W. E. (1978). Multiple insemination in natural populations of

Drosophila silvestris. Dros. Inf. Serv. 53: 138-139.

36. Turner, M. E. (1986). Multiple mating, sperm competition and the fertility component of fitness

in Drosophila pseudoobscura. Florida Entomol. 69: 121-128.

37. Gromko, M. H. and Pyle, D. W. (1978). Sperm competition, male fitness, and repeated mating

by female Drosophila melanogaster. Evolution 32: 588-593.

38. Gromko, M. H., Sheehan, K. and Richmond, R. C. (1980). Random mixing in two species of

Drosophila. Am. Nat. 115: 467-479.

39. Loukas, M., Vergini, Y. and Krimbas, C. B. (1981). The genetics of Drosophila subobscura

populations. XVII. Multiple insemination and sperm displacement in Drosophila suboscura.

Genetica 57: 29-37.

40. Griffiths, R. C., McKechnie, S. W. and McKenzie, J. A. (1982). Multiple mating and sperm

displacement in a natural population of Drosophila melanogaster. Theor. Appl. Genet. 62: 89-96

41. Markow, T. A. (1982). Mating systems of cactophilic Drosophila. In: Ecological genetics and

Evolution: The cactus-yeast-Drosophila model system (J. R. F. Barker and W. T. Starmer, eds.).

Academic Press, Australia, pp. 273-287.

42. Markow, T. A. and Ankey, P. F. (1984). Drosophila males contribute to oogenesis in a multiple

mating species. Science 224: 302-303.

43. Markow, T. A. (1985). A comparative investigations of mating system of Drosophila hydei.

Anim. Behav. 33: 775-781.

44. Marks, R. W., Seager, R. D., Ayala, F. J. and Barr, L. G. (1988). Local ecology and multiple

matings in a natural population of Drosophila melanogaster. Am. Nat. 131: 918-923.

Bressec, C., Joly, D., Devaux, J. and Lachaise, D. (1991). Can we predict the mating pattern of

Drosophila females from the sperm length distribution in males?. Experientia 47: 111-114.

46. Aspi, J. (1992). Incidence and adaptive significance of multiple mating in females of two boreal

Drosophila virilis group species. Ann. Zool. Fenn. 29: 147-159.

47. Aspi, J. and Lankinen, P. (1992). Frequency of multiple insemination in a natural population of

Drosophila montana. Hereditas 117: 169-177.

48. Schwartz, J. M. and Boake, C. R. B. (1992). Sexual dimorphism in remating in Hawaiian

Drosophila species. Anim. Behav. 44: 231-238.

49. Etges, W. J. and Heed, W. B. (1992). Remating effects on the genetic structure of female life

histories in populations of Drosophila mojavensis. Heredity 68: 515-528.

50. Joly, D., Bressac, C. and Lachaise, D. (1995). Disentangling giant sperm. Nature 377: 202.

51. Pitnick, S. and Markow, T. A. (1994). Male gametic strategies: Sperm size, testes size and the

allocation of ejaculate among successive mates by the sperm-limited fly Drosophila pachea and

its relatives. Am. Nat. 143: 785-819.

52. Price, C. S. C. (1997). Conspecific sperm precedence in Drosophila. Nature 388: 663-666.

53. McRobert, S. P., Adams, C. R., Wutjke, M., Frank, J. and Jackson, L. L. (1997). A

comparison of female post-copulatory behaviour in Drosophila melanogaster and Drosophila

biarmipes. J. Insect Behav. 10: 761-770.

54. Harshman, L. G. and Clark, A. G. (1998). Interference of sperm competition from broods of

field-caught Drosophila. Evolution 52: 1334-1341.

55. Snook, R. (1998). The risk of sperm competition and the evolution of sperm heteromorphism.

Anim. Behav. 56: 1497-1507.

56. Hirai, Y. and Kimura, M. T. (1999). Effects of copulation duration on fertility and sexual

receptivity of females of Drosophila elegans. Zool. Sci. 16: 417-421.

57. Singh, B.N. and Singh, S.R. (1999). Female remating in Drosophila ananassae: Shorter

duration of copulation during second mating as compared to first mating. J. Biosci. 24: 427-431.

58. Bundgaard, J. and Barker, J. S. F. (2000). Remating, sperm transfer, and sperm displacement

in cactophilic species Drosophila buzzatii Patterson & Wheeler (Diptera: Drosophilidae). Biol. J.

Linn. Soc. 71: 145-164.

59. Mery, F. and Joly, D. (2002). Multiple mating, sperm transfer and oviposition pattern in the

giant species, Drosophila bifurca. J. Evol. Biol. 15: 49-56.

60. Birkead, T. R. and Møller, A. P. (1998). Sperm competition and sexual selection. Academic

Press, London.

61. Imhoff, M., Harr, B., Brem, G. and Schlotterer, C. (1998). Multiple mating in wild

Drosophila melanogaster revisited by microsatellite analysis. Mol. Ecol. 7: 915-917.

62. Simmons, L. W. and Siva-Jothy, M. T. (1998). Sperm competition in insects: mechanisms and

the potential for selection. In: Sperm Competition and Sexual Selection (Birkhead, T. R. and

Moller, A. P., eds). Academic Press, San Diego, pp. 341-434.

63. Garant, D., Dodson, J. J. and Bernatchez, L. (2001). A genetic evaluation of mating system

and determinants of individual reproductive success in Atlantic Salmon (Salmo salar L.). J.

Hered. 92: 132-145.

64. Pearse, D. E. and Avise, J. C. (2001). Turtle mating systems: behavior, sperm storage and

genetic paternity. J. Hered. 92: 206-211.

65. Baker, R., and Bellis, M. A. (1993). Human sperm competition: ejaculate manipulation by

females and a function for the female orgasm. Anim. Behav. 46: 887-909.

66. Smith, R. L. (1984). Sperm Competition and the Evolution of Animal Mating Systems.

Academic Press, New York.

67. Danielsson, I. (1998). Mechanisms of sperm competition in insects. Ann. Zool. Fennici. 35: 241-


68. Civetta, A. (1999). Direct visualization of sperm competition and sperm storage in Drosophila.

Curr. Biol. 9: 841-844.

69. Halliday, T. and Arnold, S. J. (1987). Multiple mating by females: a perspective from

quantitative genetics. Anim. Behav. 35: 939-941.

70. Pitnick, S., Markow, T. A. and Riedly, M. F. (1991). Transfer of ejaculate and incorporation of

male-derived substances by females in the nannoptera species group (Diptera: Drosophilidae).

Evolution 45:774-780.

71. Maynard-Smith, J. (1956). Fertility, mating behaviour and sexual selection in Drosophila

subobscura. J. Genet. 54: 261-279.

72. Pyle, D. W. and Gromko, M. H. (1978). Repeated mating by female Drosophila melanogaster:

The adaptive importance. Experientia 34: 449-450.

73. Dobzhansky, Th. and Pavlovsky, O. (1967). Repeated mating and sperm mixing in Drosophila

pseudoobscura. Am. Nat. 101: 527-533.

74. Barbadilla, A., Quezada-Diaz, J. E., Ruiz, A., Santos, M. and Fontedevila, A. (1991). The

evolutionary history of Drosophila buzzatii. XVII. Double mating and sperm predominance.

Genet. Sel. Evol. 23: 133-140.

75. Hardeland, R. (1972). Species differences in the diurnal rhythmicity of courtship behaviour

within the melanogaster group of the genus Drosophila. Anim. Behav. 20: 170-174.

76. Turner, M. E. and Anderson, W. W. (1984). Sperm predominance among Drosophila

pseudoobscura karyotypes. Evolution 38: 983-995.

77. Newport, M. E. A. and Gromko, M. H. (1984). The effect of experimental design on female

receptivity to remating and its impact on reproductive success in Drosophila melanogaster.

Evolution 38: 1261-1272.

78. Letsinger, J. T. and Gromko, M. H. (1985). The role of sperm numbers in sperm competition

and female remating in Drosophila melanogaster. Genetics 66: 195-202.

79. Trevitt, S., Fowler, K. and Partridge, L. (1988). An effect of egg deposition on the subsequent

fertility and remating frequency of female Drosophila melanogaster. J. Insect Physiol. 34: 821-


80. Service, P. M. and Vossbrink, R. E. (1996). Genetic variation in “First” male effect on egg

laying and remating by female Drosophila melanogaster. Behav. Genet. 26: 39-48.

81. Joly, D., Cariou, M. L. and Lachaise, D. (1991). Can sperm competition explain sperm

polymorphism in Drosophila teissieri? Evol. Biol. 5: 25-44.

82. Joly, D. and Lachaise, D. (1993). Multiple mating frequency differs in two different geographic

strains of Drosophila teissieri. Dros. Inf. Serv. 72: 126-127.

83. Gilchrist, A. S. and Partridge, L. (2000). Why it is difficult to model sperm displacement in

Drosophila melanogaster: The relation between sperm transfer and copulation duration.

Evolution 54: 534-542.

84. Fukui, H. H. and Gromko, M. H. (1989). Female receptivity to remating and early fecundity in

Drosophila melanogaster. Evolution 43: 1311-1315.

85. Gromko, M. H. and Markow, T. A. (1993). Courtship and remating in field populations of

Drosophila. Anim. Behav. 45: 253-262.

86. Turner, M. E. and Anderson, W. W. (1983). Multiple mating and female fitness in Drosophila

pseudoobscura. Evolution 37: 714-723.

87. Harshman, L. G., Hoffman, A. A. and Prout, T. (1988). Environmental effects on remating in

Drosophila melanogaster. Evolution 42: 312-321.

88. Chapman, T. and Partridge, L. (1996). Female fitness in Drosophila melanogaster: an

interaction between the effect of nutrition and of encounter rate with males. Proc. Roy. Soc.

London, B 263: 755-759.

89. Boorman, E. and Parker, G. A. (1976). Sperm (ejaculate) competition in Drosophila

melanogaster, and the reproductive value of females to males in relation to female age and

mating status. Ecol. Entomol. 1: 145-155.

90. Gromko, M. H. and Gerhart, P. D. 1984. Increased density does not increase remating

frequency in laboratory populations of Drosophila melanogaster. Evolution 38: 451-455.

91. Ochando, M. D., Reyes, A. and Ayala, F. J. (1996). Multiple paternity in two natural

populations (Orchard and Vinayard) of Drosophila. Proc. Natl. Acad. Sci. USA 93: 11769-


92. Singh, B.N. and Singh, S.R. (2001). Female remating in Drosophila ananassae: Evidence for

sperm displacement and greater productivity after remating. Zool. Sci. 18: 181-185.

93. Pitnick, S., Markow, T. A. and Spicer, G. S. (1995). Delayed male maturity is a cost of

producing large sperm in Drosophila. Proc. Natl. Acad. Sci. USA 92: 10614-10618.

94. van-Vianen, A. and Bijlsma, R. (1993). The adult component of selection in Drosophila

melanogaster. Some aspect of early remating activity in females. Heredity 71: 269-276.

95. Sgro, C. M., Chapman, T. and Partridge, L. (1998). Sex-specific selection on time to remate

in Drosophila melanogaster. Anim. Behav. 56: 1267-1278.149.

96. Harshman, L. G. and Prout, T. 1994. Sperm displacement without sperm transfer in

Drosophila melanogaster. Evolution 48: 758-766.

97. Chapman, T., Trevitt, S. and Partridge, L. 1994. Remating and male derived nutrients in

Drosophila melanogaster. J. Evol. Biol. 7: 51-69.

98. Markow, T. A. (2000). Forced matings in natural populations of Drosophila. Amer. Nat. 156:


99. Snook, R. and So, Y. K. (2000). Associations between female remating behaviour, oogenesis

and oviposition in Drosophila melanogaster and Drosophila pseudoobscura. J. Insect Physiol.

46: 1489-1149.

100. Gibson, R. M. and Jewell, P. A. (1982). Semen quality, female choice and multiple mating in

domestic sheep: A test of Trivers’ sexual competence hypothesis. Behaviour 90: 9-31.

101. Ridley, M. (1988). Mating frequency and fecundity in insects. Biol. Rev. 63: 509-549.

102. LaMunyon, C. W. and Ward, S. (1999). Evolution of sperm size in nematodes: sperm

competition favours larger sperm. Proc. Roy. Soc. Lond. B 266: 263-267.

103. Rice, R. (1996). Sexually antagonistic male adaptation triggered by experimental arrest of

female evolution. Nature 381: 232-234.

104. Nonidez, J. F. (1920). The internal phenomenon of reproduction in Drosophila. Biol. Bull., 39:


105. Clark, A. G., Aguade, M., Prout, T., Harshman, L. G. and Langley, C. H. (1995). Variation

in sperm displacement and its association with accessory gland protein loci in Drosophila

melanogaster. Genetics 139: 189-201.

106. Singh, S.R. and Singh, B.N. (2001). Female remating in Drosophila ananassae: Evidence for

the effect of density on female remating frequency. J. Insect Behav. 14: 659-668.

107. Hughes, K. A. (1997). Quantitative genetics of sperm precedence in Drosophila melanogaster.

Genetics 145: 139-151.

108. Clark, A. G. and Begun, D. J. (1998). Female genotypes affect sperm displacement in

Drosophila. Genetics 149: 1487-1493.

109. Civetta, A. and Clark, A. G. (2000). Chromosomal effects on male and female components of

sperm precedence in Drosophila. Genet. Res. 75: 143-151.

110. Clark, A. G., Begun, D. J. and Prout, T. 1999. Female x male interaction in Drosophila sperm

competition. Science 283: 217-220.

111. Price, C. S. C., Kim, C. H., Posluszny, J. and Coyne, J. A. (2000). Mechanisms of conspecific

sperm precedence. Evolution 54: 2028-2037.

112. Parker, G. A. (1998). Sperm competition and the evolution of ejaculates: Toward a theory base.

In: Sperm Competition and Sexual Selection (Birkhead, T. R. and Moller, A. P. eds.). Academic

Press, New York, pp. 3-54.

113. Greeff, J. M. and Parker, G. A. (2000). Spermicide by females: What should males do? Proc.

Roy. Soc. Lond. 267: 1759-1763.

114. Walker, W. F. (1980). Sperm utilization strategies in non-social insects. Am. Nat. 115 780-799.

115. Cook, P. A., Harvey, I. F. and Parker, G. A. (1997). Predicting variation in sperm precedence.

Phil. Trans. R. Soc. Lond. B 352: 771-780.

116. Parker, G. A., Simmons, L. W. and Kirk, H. (1990). Analysing sperm competition data:

Simple models for predicting mechanisms. Behav. Ecol. Sociobiol. 27: 55-65.

117. Polak, M., Wolf, L. L., Starmer, W. T. and Barker, J. S. F. (2001). Function of the mating

plug in Drosophila hibisci Bock. Behav. Ecol. Sociobiol. 49: 196-205.

118. Hunter, F. M. and Birkhead, T. R. (2002). Sperm viability and sperm competition in insects.

Curr. Biol. 12:121-123.

119. Baker, R. R. and Belis, M. A. (1988). “Kamikaze” sperm in mammals? Anim. Behav. 36: 936-


120. Wyckoff, G.J., Wang, W. and Wu C-I. (2000). Rapid evolution of male reproductive genes in

the descent of man. Nature 403: 304-309.

121. Lung, O., Tram, U., Finnerty, C. M., Eipper-Mains, M. A., Kalb, J. M., and Wolfner, M. F.

(2002). The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is

toxic upon ectopic expression. Genetics 160: 211-224.

122. Lung, O. and Wolfner, M. F. (2001) Identification and characterization of the major

Drosophila melanogaster mating plug protein. Insect Biochem. Mol. Biol. 31: 543-551.

123. Price, C. S. C., Dyer, K. A. and Coyne, J. A. (1999). Sperm competition between Drosophila

males involves both displacement and incapacitation. Nature 400: 449-452.

124. Civetta, A. and Singh, R. S. (1995). High divergence of reproductive tract proteins and their

associates with postzygotic reproductive isolation in Drosophila melanogaster and D. virilis

group species. J. Mol. Evol. 41: 1085-1095.

125. Prout, T. and Clark, A. G. (1996). Polymorphism in genes that influence sperm displacement.

Genetics 144: 401-408.

126. Reinhardt, K. (2000). Variation in sperm precedence in Chorthippus grasshoppers (Caelifera:

Gomphocerinae). Physiol. Entomol. 25: 324-329.

127. Huck, W. W., Quinn, R. P. and Lisk, R. D. (1985). Determinants of mating success in the

golden hamster (Mesocricetus auratus). Behav. Ecol. Sociobiol. 17: 239-252.

128. Parker, G. A. (1993). Sperm competition games: Sperm size and number under adult control.

Proc. R. Soc. Lond. B 253: 245-254.

129. Civetta, A. and Clark, A. G. (2000). Correlated effects of sperm competition and postmating

female mortality. Proc. Natl. Acad. Sci. USA 97: 13162-13165.

130. Ridley, M. (1989). The incidence of sperm displacement in insects: Four conjectures, one

corroboration. Biol. J. Linn. Soc. 38: 349-367.

131. Gwynne, D. T. (1984). Male mating effort, confidence of paternity and insect sperm

competition. In: Sperm Competition and the Evolution of Animal Mating Systems (Smith R. L.

ed.). Academic Press, New York, pp. 117-150.

132. Simmons, L. W. and Parker, G. A. (1992). Individual variation in sperm competition success

of yellow Dung flies, Scatophaga stercoraria. Evolution 46: 366-375.

133. Gilchrist, A. S. and Partridge, L. (1997). Heritability of pre-adult viability differences can

explain apparent heritability of sperm displacement ability in Drosophila melanogaster. Proc. R.

Soc. Lond. B 264: 1271-1275.

134. Parker, G. A. and Simmons, L. W. (1991). A model of constant random sperm displacement

during mating: Evidence from Scaptophaga. Proc. Roy. Soc. Lond. B 246: 107-115.

135. Harvey, I. F. and Parker, G. A. (2000). ‘Sloppy’ sperm mixing and intra-specific variation in

sperm precedence (P2) patterns. Proc. R. Soc. Lond. B 267: 2537-2542.

136. Pyle, D. W. and Gromko, M. H. (1981). Genetic basis for repeated mating in Drosophila

melanogaster. Am. Nat. 117: 133-146.

137. Gromko, M. H. and Newport, M. E. A. (1988). Genetic basis for remating in Drosophila

melanogaster. II. Response to selection based on the behaviour of one sex. Behav. Genet. 18:


138. Gromko, M. H. and Newport, M. E. A. (1988). Genetic basis for remating in Drosophila

melanogaster. II. Correlated responses to selection for female remating speed. Behav. Genet. 18:


139. Hudak, M. J. and Gromko, M. H. (1989). Response to selection for early and late development

of sexual maturity in Drosophila melanogaster. Anim. Behav. 38: 344-351.

140. Fukui, H. H. and Gromko, M. H. 1991. Genetic basis for remating in Drosophila

melanogaster. IV. A chromosome substitution analysis. Behav. Genet. 21: 169-182.

141. Fukui, H. H. and Gromko, M. H. 1991. Genetic basis for remating in Drosophila

melanogaster. V. Biometrical and planned comparison analysis. Behav. Genet. 21: 183-197.

142. Fukui, H. H. and Gromko, M. H. 1991. Genetic basis for remating in Drosophila

melanogaster. VI. Recombination analysis. Behav. Genet. 21: 199-209.

143. Stamencovic-Radak, M., Partridge, L. and Andjelcovic, M. (1993). Genetic correlation between

the sexes in Drosophila melanogaster: A reply to Butlin. Anim. Behav. 45: 405.

144. Singh, S.R. and Singh, B.N. (2001). Female remating in Drosophila ananassae: Bidirectional

selection for remating speed. Behav. Genet. 31: 361-370.

145. Singh, B.N. (1996). Population and behaviour genetics of Drosophila ananassae. Genetica 97:


146. Singh, B. N. (2000). Drosophila ananassae–a species characterised by several unusual genetic

features. Curr. Sci. 78: 391-398.

147. Clark, A. G., Dermitzakis, E. T. and Civetta, A. (2000). Nontransitivity of sperm precedence

in Drosophila. Evolution 54: 1030-1035.

148. Markow, T. A., Gallagher, P. D. and Krebs, R. A. (1990). Ejaculate-derived nutritional

contribution and female reproductive success in Drosophila mojavensis (Patterson and Low).

Funct. Ecol. 4: 67-73.

149. Snook, R. R. and Markow, T. A. (1996). Possible role of non-fertilizing sperm as a nutrient

source for female Drosophila pseudoobscura (Diptera: Drosophilidae). Pan. Entomol. 72: 121-


150. Reynolds, J. D. (1996). Animal breeding systems. Trends Ecol. Evol. 11: 68-72.

151. Hesselquist, D., Bensch, S. and Schantz, T. (1996). Correlation between male song repertoire,

extra-pair paternity and offspring survival in the great reed warbler. Nature 381: 229-232.

152. Ridley, M. (1993). Clutch size and mating frequency in parasitic Hymenoptera. Am. Nat. 142:


153. Keller, L. and Reeve, H. K. (1995). Why do females mate with multiple males? The sexuallyselected

sperm hypothesis. Adv. Stud. Behav. 24: 291-315.

154. Stockley, P. (1999). Sperm selection and genetic incompatibility: does relatedness of mates

affect male success in sperm competition? Proc. R. Soc. Lond. B 266: 1663-1669.

155. Zeh, J. E. and Zeh, D. W. (2001). Reproductive mode and the genetic benefits of polyandry.

Anim. Behav. 61: 1051-1063.

156. Zahavi, A. (1977). The cost of honesty (further remarks on the handicap principle). J. Theor.

Biol. 67: 603-605.

157. Hoenigsberg, H. F. (1999). Female competition in mate choice decreases fitness in flies

(Drosophila pseudoobscura) from Colombia. Genet. Mol. Biol. 22: 213-215.

158. Yasui, Y. (1997). A “good-sperm” model can explain the evolution of multiple mating by

females. Am. Nat. 149: 573-584.

159. Curtsinger, J. W. (1991). Sperm competition and evolution of multiple mating. Am. Nat. 138:


160. Bernasconi, G. and Keller, L. (2001). Female polyandry affects their sons’ reproductive

success in the red flour beetle Tribolium castaneum. J Evol Biol 14: 186-193.

161. Tregenza, T. and Wedell, N. (2000). Genetic compatibility, mate choice and patterns of

parentage. Mol. Ecol. 9: 1013-1027

162. Rice, W. R. and Holland, B. (1997). The enemies within: inter-genomic conflict, inter-locus

contest evolution (ICE), and the intra-specific red queen. Behav. Ecol. Sociobiol. 41:1-10.

163. Li, S-H. and Brown, J. L. (2002) Reduction of maternal care: a new benefit of multiple mating?

Behav. Ecol. 13: 87-93.

164. Medsen, T., Shine, R., Loman, J. and Hakansson, T. (1992). Why do female adders copulate

so frequntly? Nature 355: 440-441.

165. Haig, D. and Bergstrom, C. T. (1995). Multiple mating, sperm competition and meiotic drive.

J. Evol. Biol., 8: 265-282.

166. Lessels, C. M. and Parker, G. A. (1999). Parent-offspring conflict: the full-sib-half-sib fallacy.

Proc. R. Soc. Lond. B 266:1637-1643.

167. Bateman, A. J. (1948). Intra-sexual selection in Drosophila. Heredity 2: 349-368.

168. Holland, B. and Rice, W. R. (1999). Experimental removal of sexual selection reverses intersexual

antagonistc co-evolution and removes reproductive load. Proc. Natl. Acad. Sci. USA 96:


169. Partridge, L. and Hurst, L. D. 1998. Sex and conflict. Science 281: 2003-2008.

170. Pitnick, S., Brown, W. D. and Miller, G. T. (2001). Evolution of female remating behaviour

following experimental removal of sexual selection. Proc. Roy. Soc. Lond. 268:557-563.


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