No evidence that polyandry benefits females in Drosophila melanogaster

Evolution

Volumn 58, Issue 6, 2004, Pages 1242-1250

  Brown, William D ^a   Bjork, Adam ^b   Schneider, Karin ^b   Pitnick, Scott ^b  

^a STATE UNIVERSITY OF NEW YORK AT FREDONIA   (United States)

^b SYRACUSE UNIVERSITY   (United States)

Author keywords

Multiple mating; Offspring viability; Polyandry; Reproductive success; Sexual selection; Sperm competition

Indexed keywords

ADAPTATION; EVOLUTION; FITNESS; POLYANDRY; REPRODUCTIVE SUCCESS; SEXUAL SELECTION;

ANIMALIA; DIPTERA; DROSOPHILA MELANOGASTER; DROSOPHILIDAE; MELANOGASTER;

EID: 3042631768     PISSN: 00143820     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.0014-3820.2004.tb01703.x     Document Type: Article

References (73)

1. Arnqvist, G. 1989. Multiple mating in a water strider: mutual benefits or intersexual conflict? Anim. Behav. 38:749-756.
2. Arnqvist, G., and L. Nilsson. 2000. The evolution of polyandry: multiple mating and female fitness in insects. Anim. Behav. 60:145-164.
3. Bateman, A. J. 1948. Intra-sexual selection in Drosophila. Heredity 2:349-368.
4. Birkhead, T. R. 2000. Promiscuity. Faber, London.
5. Chapman, T., L. F. Liddle, J. M. Kalb, M. F. Wolfner, and L. Partridge. 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373:241-244.
6. Chippindale, A. K., J. R. Gibson, and W. R. Rice. 2001. Negative genetic correlation for fitness between sexes reveals ontogenetic conflict in Drosophila. Proc. Natl. Acad. Sci. USA 98:1671-1675.
7. Clark, A. G., D. J. Begun, and T. Prout. 1999. Female X male interactions in Drosophila sperm competition. Science 283:217-220.
8. Colegrave, N., and G. D. Ruxton. 2003. Confidence intervals are a more useful complement to nonsignificant tests than are power calculations. Behav. Ecol. 14:446-447.
9. Curtsinger, J. W. 1991. Sperm competition and the evolution of multiple mating. Am. Nat. 138:93-102.
10. Eady, P. E., N. Wilson, and M. Jackson. 2000. Copulating with multiple mates enhances female fecundity but not egg-to-adult survival in the bruchid beetle Callosobruchus maculates. Evolution 54:2161-2165.
11. Evans, J. P., and A. E. Magurran. 2000. Multiple benefits of multiple mating in guppies. Proc. Natl. Acad. Sci. USA 97:10074-10076.
12. Evans, J. P., L. Zane, S. Francescato, and A. Pilastro. 2003. Directional postcopulatory sexual selection revealed by artificial insemination. Nature 421:360-363.
13. Foerster, K., K. Delhey, A. Johnsen, J. T. Lifjeld, and B. Kempenaers. 2003. Females increase offspring heterozygosity and fitness through extra-pair matings. Nature 425:714-717.
14. Fowler, K., and L. Partridge. 1989. A cost of mating in female fruitflies. Nature 338:760-761.
15. Fox, C. W., and C. M. Rauter. 2003. Bet-hedging and the evolution of multiple mating. Evol. Ecol. Res. 5:273-286.
16. Garner, T. W., and B. R. Schmidt. 2003. Relatedness, body size and paternity in the alpine newt, Triturus alpestris. Proc. R. Soc. Lond. B 270:619-624.
17. Gilchrist, A. S., and L. Partridge. 1997. Heritability of pre-adult viability differences can explain apparent heritability of sperm displacement ability in Drosophila melanogaster. Proc. Roy. Soc. Lond. B 264:1271-1275.
18. Gillespie, J. H. 1974. Natural selection for within-generation variance in offspring number. Genetics 76:601-606.
19. Gromko, M. H., D. G. Gilbert, and R. C. Richmond. 1984. Sperm transfer and use in the multiple mating system of Drosophila. Pp. 371-426 in R. L. Smith, ed. Sperm competition and the evolution of animal mating systems. Academic Press, New York.
20. Hohoff, C., K. Franzen, and N. Sachser. 2003. Female choice in a promiscuous wild guinea pig, the yellow-toothed cavy (Galea musteloides). Behav. Ecol. Sociobiol. 53:341-349.
21. Holland, B., and W. R. Rice. 1998. Chase-away sexual selection: antagonistic seduction versus resistance. Evolution 52:1-7.
22. Hosken, D. J., and P. Stockley. 2003. Benefits of polyandry: a life history perspective. Evol. Biol. 33:173-194.
23. Hosken, D. J., T. W. J. Garner, T. Tregenza, N. Wedell, and P. I. Ward. 2003. Superior sperm competitors sire higher quality young. Proc. R. Soc. Lond. B. 270:1933-1938.
24. Jennions, M. D., and M. Petrie. 2000. Why do females mate multiply? A review of the genetic benefits. Biol. Rev. 75:21-64.
25. Keil, A., and N. Sachser. 1998. Reproductive benefits from female promiscuous mating in a small mammal. Ethology 104:897-903.
26. Keller, L., and H. K. Reeve. 1995. Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv. Study Behav. 24:291-315.
27. Madsen, T., R. Shine, J. Loman, and T. Håkansson. 1992. Why do female adders copulate so frequently? Nature 355:440-441.
28. Markow, T. A. 2000. Forced mating in natural populations of Drosophila. Am. Nat. 156:100-103.
29. Matthews, I. M., J. P. Evans, and A. E. Magurran. 1997. Male display rate reveals ejaculate characteristics in the Trinidadian guppy Poecilia reticulata. Proc. R. Soc. Lond. B 264:695-700.
30. Miller, G. T., and S. Pitnick. 2002. Sperm-female coevolution in Drosophila. Science 298:1230-1233.
31. Møller, A. P. 1994. Directional selection on directional asymmetry: testes size and secondary sexual characteristics in birds. Proc. R. Soc. Lond. B 258:147-151.
32. Morrow, E. H., G. Arnqvist, and S. Pitnick. 2003. Adaptation versus pleiotropy: why do males harm their mates? Behav. Ecol. 14:802-806.
33. Newcomer, S. D., J. A. Zeh, and D. W. Zeh. 1999. Genetic benefits enhance the reproductive success of polyandrous females. Proc. Natl. Acad. Sci. USA 96:10236-10241.
34. Olsson, M., T. Madsen, R. Shine, A. Gullberg, and H. Tegelström. 1994. Rewards of promiscuity. Nature 372:230.
35. Olsson, M., R. Shine, T. Madsen, A. Gullberg, A., and H. Tegelström. 1996. Sperm selection by females. Nature 383:585.
36. Page, R. E., G. E. Robinson, and M. K. Fondrk. 1989. Genetic specialists, kin recognition, and nepotism in honey-bee colonies. Nature 338:576-579.
37. Parker, G. 1992. Snakes and female sexuality. Nature 355:395-396.
38. Partridge, L., A. Ewing, and A. Chandler. 1987a. Male size and mating success in Drosophila melanogaster: the roles of male and female behaviour. Anim. Behav. 35:555-562.
39. Partridge, L., A. Hofman, and J. S. Jones. 1987b. Male size and mating success in Drosophila melanogaster and D. pseudoobscura under field conditions. Anim. Behav. 35:468-476.
40. Pitnick, S. 1991. Male size influences mate fecundity and remating interval in Drosophila melanogaster. Anim. Behav. 41:735-745.
41. Pitnick, S., W. D. Brown, and G. T. Miller. 2001. Evolution of female remating behaviour following experimental removal of sexual selection. Proc. R. Soc. Lond. B 268:557-563.
42. Pitnick, S., and F. García-González. 2002. Harm to females increases with male body size in Drosophila melanogaster. Proc. R. Soc. Lond. B 269:1821-1828.
43. Pitnick, S., G. S. Spicer, and T. A. Markow. 1997. Phylogenetic examination of male ejaculatory donations in Drosophila. Evolution 51:833-845.
44. Radwan, J. 2003. Male age, germline mutations, and the benefits of polyandry. Ecol. Lett. 6:581-586.
45. Rice, W. R. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381:232-234.
46. Ridley, M. 1990. The control and frequency of mating in insects. Funct. Ecol. 4:75-84.
47. Robertson, F. W., and E. C. R. Reeve. 1952. Studies in quantitative inheritance. I. The effects of selection for wing and thorax length in Drosophila melanogaster. J. Genet. 50:416-448.
48. Schmid-Hempel, P. 1994. Infection and colony variability in social insects. Phil. Trans. R. Soc. Lond. B 346:313-321.
49. Schneider, J. M., and M. A. Elgar. 1998. Spiders hedge genetic bets. Trends Ecol. Evol. 13:218-219.
50. Simmons, L. W. 2001a. The evolution of polyandry: an examination of the genetic incompatibility and good-sperm hypotheses. J. Evol. Biol. 14:585-594.
51. _. 2001b. Sperm competition and its evolutionary consequences in insects. Princeton Univ. Press, Princeton, NJ.
52. _. 2003. The evolution of polyandry: patterns of genotypic variation in female mating frequency, male fertilization success and a test of the sexy-sperm hypothesis. J. Evol. Biol. 16:626-634.
53. Slatkin, M. 1974. Hedging one's evolutionary bets. Nature 250:704-705.
54. Sokal, R. R., and F. J. Rohlf. 1981. Biometry, 2d ed. Freeman, San Francisco, CA.
55. 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.
56. _. 2003. Female multiple mating behaviour, early reproductive failure and litter size variation in mammals. Proc. R. Soc. Lond. B 270:271-278.
57. Thornhill, R., and J. Alcock. 1983. The evolution of insect mating systems. Harvard Univ. Press, Cambridge, U.K.
58. Tregenza, T., and N. Wedell. 1998. Benefits of multiple mates in the cricket Gryllus bimaculatus. Evolution 52:1726-1730.
59. _. 2000. Genetic compatibility, mating choice and patterns of parentage: invited review. Mol. Ecol. 9:1013-1027.
60. _. 2002. Polyandrous females avoid costs of inbreeding. Nature 415:71-73.
61. Van Vianen, A., and R. Bijlsma. 1993. The adult component of selection in Drosophila melanogaster: some aspects of early-remating activity in females. Heredity 71:269-276.
62. Watson, P. J. 1991. Multiple paternity as genetic bet-hedging in female sierra dome spiders, Linyphia litigosa (Linyphiidae). Anim. Behav. 41:343-360.
63. _. 1998. Multi-male mating and female choice increase off-spring growth in the spider Neriene litigiosa (Linyphiidae). Anim. Behav. 55:387-403.
64. Williams, G. C. 1975. Sex and Evolution. Princeton Univ. Press, Princeton, NJ.
65. Wilson, K., and I. C. W. Hardy. 2002. Statistical analysis of sex ratios: an introduction. Pp. 48-92 in I. C. W. Hardy, ed. Sex ratios: concepts and research methods. Cambridge Univ. Press, Cambridge, U.K.
66. Wolfner, M. F. 1997. Tokens of love: functions and regulation of Drosophila male accessory gland products. Insect Biochem. Mol. Biol. 27:179-192.
67. Yasui, Y. 1997. A "good sperm" model can explain the evolution of costly, multiple mating by females. Am. Nat. 149:573-584.
68. _. 1998. The "genetic benefits" of female multiple mating reconsidered. Trends Ecol. Evol. 13:246-250.
69. Zeh, J. A. 1997. Polyandry and enhanced reproductive success in the harlequin-beetle-riding pseudoscorpion. Behav. Ecol. Sociobiol. 40:111-118.
70. Zeh, J. A. and D. W. Zeh. 1996. The evolution of polyandry. I. Intragenomic conflict and genetic incompatability. Proc. R. Soc. Lond. B 263:1711-1717.
71. _. 1997. The evolution of polyandry II: post-copulatory defences against genetic incompatibility. Proc. R. Soc. Lond. B 264:69-75.
72. _. 2001. Reproductive mode and the genetic benefits of polyandry. Anim. Behav. 61:1051-1063.
73. _. 2003. Toward a new sexual selection paradigm: polyandry, conflict, and incompatibility. Ethology 109:929-950.