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. 2002 Sep 7;269(1502):1821–1828. doi: 10.1098/rspb.2002.2090

Harm to females increases with male body size in Drosophila melanogaster.

Scott Pitnick 1, Francisco García-González 1
PMCID: PMC1691094  PMID: 12350270

Abstract

Previous studies indicate that female Drosophila melanogaster are harmed by their mates through copulation. Here, we demonstrate that the harm that males inflict upon females increases with male size. Specifically, both the lifespan and egg-production rate of females decreased significantly as an increasing function of the body size of their mates. Consequently, females mating with larger males had lower lifetime fitness. The detrimental effect of male size on female longevity was not mediated by male effects on female fecundity, egg-production rate or female-remating behaviour. Similarly, the influence of male size on female lifetime fecundity was independent of the male-size effect on female longevity. There was no relationship between female size and female resistance to male harm. Thus, although increasing male body size is known to enhance male mating success, it has a detrimental effect on the direct fitness of their mates. Our results indicate that this harm is a pleiotropic effect of some other selected function and not an adaptation. To the extent that females prefer to mate with larger males, this choice is harmful, a pattern that is consistent with the theory of sexually antagonistic coevolution.

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Selected References

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  1. Aigaki T., Fleischmann I., Chen P. S., Kubli E. Ectopic expression of sex peptide alters reproductive behavior of female D. melanogaster. Neuron. 1991 Oct;7(4):557–563. doi: 10.1016/0896-6273(91)90368-a. [DOI] [PubMed] [Google Scholar]
  2. Arnqvist Göran, Rowe Locke. Antagonistic coevolution between the sexes in a group of insects. Nature. 2002 Feb 14;415(6873):787–789. doi: 10.1038/415787a. [DOI] [PubMed] [Google Scholar]
  3. Arnqvist Göran, Rowe Locke. Correlated evolution of male and female morphologles in water striders. Evolution. 2002 May;56(5):936–947. doi: 10.1111/j.0014-3820.2002.tb01406.x. [DOI] [PubMed] [Google Scholar]
  4. Chapman T., Hutchings J., Partridge L. No reduction in the cost of mating for Drosophila melanogaster females mating with spermless males. Proc Biol Sci. 1993 Sep 22;253(1338):211–217. doi: 10.1098/rspb.1993.0105. [DOI] [PubMed] [Google Scholar]
  5. Chapman T., Liddle L. F., Kalb J. M., Wolfner M. F., Partridge L. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature. 1995 Jan 19;373(6511):241–244. doi: 10.1038/373241a0. [DOI] [PubMed] [Google Scholar]
  6. Chapman T., Miyatake T., Smith H. K., Partridge L. Interactions of mating, egg production and death rates in females of the Mediterranean fruit fly, Ceratitis capitata. Proc Biol Sci. 1998 Oct 7;265(1408):1879–1894. doi: 10.1098/rspb.1998.0516. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chapman T., Partridge L. Female fitness in Drosophila melanogaster: an interaction between the effect of nutrition and of encounter rate with males. Proc Biol Sci. 1996 Jun 22;263(1371):755–759. doi: 10.1098/rspb.1996.0113. [DOI] [PubMed] [Google Scholar]
  8. Chapman T., Partridge L. Sexual conflict as fuel for evolution. Nature. 1996 May 16;381(6579):189–190. doi: 10.1038/381189a0. [DOI] [PubMed] [Google Scholar]
  9. Chen P. S., Stumm-Zollinger E., Aigaki T., Balmer J., Bienz M., Böhlen P. A male accessory gland peptide that regulates reproductive behavior of female D. melanogaster. Cell. 1988 Jul 29;54(3):291–298. doi: 10.1016/0092-8674(88)90192-4. [DOI] [PubMed] [Google Scholar]
  10. Coyne J. A., Beecham E. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics. 1987 Dec;117(4):727–737. doi: 10.1093/genetics/117.4.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Danielsson I. Antagonistic pre- and post-copulatory sexual selection on male body size in a water strider (Gerris lacustris). Proc Biol Sci. 2001 Jan 7;268(1462):77–81. doi: 10.1098/rspb.2000.1332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Dow M. A., von Schilcher F. Aggression and mating success in Drosophila melanogaster. Nature. 1975 Apr 10;254(5500):511–512. doi: 10.1038/254511a0. [DOI] [PubMed] [Google Scholar]
  13. Gavrilets S., Arnqvist G., Friberg U. The evolution of female mate choice by sexual conflict. Proc Biol Sci. 2001 Mar 7;268(1466):531–539. doi: 10.1098/rspb.2000.1382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heifetz Y., Lung O., Frongillo E. A., Jr, Wolfner M. F. The Drosophila seminal fluid protein Acp26Aa stimulates release of oocytes by the ovary. Curr Biol. 2000 Jan 27;10(2):99–102. doi: 10.1016/s0960-9822(00)00288-8. [DOI] [PubMed] [Google Scholar]
  15. Holland B., Rice W. R. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5083–5088. doi: 10.1073/pnas.96.9.5083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Houle David, Kondrashov Alexey S. Coevolution of costly mate choice and condition-dependent display of good genes. Proc Biol Sci. 2002 Jan 7;269(1486):97–104. doi: 10.1098/rspb.2001.1823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Iliadi K., Iliadi N., Rashkovetsky E., Minkov I., Nevo E., Korol A. Sexual and reproductive behaviour of Drosophila melanogaster from a microclimatically interslope differentiated population of "Evolution Canyon" (Mount Carmel, Israel). Proc Biol Sci. 2001 Nov 22;268(1483):2365–2374. doi: 10.1098/rspb.2001.1822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kalb J. M., DiBenedetto A. J., Wolfner M. F. Probing the function of Drosophila melanogaster accessory glands by directed cell ablation. Proc Natl Acad Sci U S A. 1993 Sep 1;90(17):8093–8097. doi: 10.1073/pnas.90.17.8093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kirkpatrick M., Barton N. H. The strength of indirect selection on female mating preferences. Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1282–1286. doi: 10.1073/pnas.94.4.1282. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lung Oliver, Tram Uyen, Finnerty Casey M., Eipper-Mains Marcie A., Kalb John M., Wolfner Mariana F. The Drosophila melanogaster seminal fluid protein Acp62F is a protease inhibitor that is toxic upon ectopic expression. Genetics. 2002 Jan;160(1):211–224. doi: 10.1093/genetics/160.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Markow T. A. Behavioral and sensory basis of courtship success in Drosophila melanogaster. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6200–6204. doi: 10.1073/pnas.84.17.6200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Markow T. A. Reproductive behavior of Drosophila melanogaster and D. nigrospiracula in the field and in the laboratory. J Comp Psychol. 1988 Jun;102(2):169–173. doi: 10.1037/0735-7036.102.2.169. [DOI] [PubMed] [Google Scholar]
  23. Pitnick S., Brown W. D., Miller G. T. Evolution of female remating behaviour following experimental removal of sexual selection. Proc Biol Sci. 2001 Mar 22;268(1467):557–563. doi: 10.1098/rspb.2000.1400. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pitnick S., Markow T. A. Large-male advantages associated with costs of sperm production in Drosophila hydei, a species with giant sperm. Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9277–9281. doi: 10.1073/pnas.91.20.9277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pitnick S., Miller G. T., Reagan J., Holland B. Males' evolutionary responses to experimental removal of sexual selection. Proc Biol Sci. 2001 May 22;268(1471):1071–1080. doi: 10.1098/rspb.2001.1621. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rice W. R. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature. 1996 May 16;381(6579):232–234. doi: 10.1038/381232a0. [DOI] [PubMed] [Google Scholar]
  27. Rowe Locke, Arnqvist Göran. Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to address evolutionary processes. Evolution. 2002 Apr;56(4):754–767. doi: 10.1111/j.0014-3820.2002.tb01386.x. [DOI] [PubMed] [Google Scholar]
  28. Sawby R., Hughes K. A. Male genotype affects female longevity in Drosophila melanogaster. Evolution. 2001 Apr;55(4):834–839. doi: 10.1554/0014-3820(2001)055[0834:mgafli]2.0.co;2. [DOI] [PubMed] [Google Scholar]
  29. TANTAWY A. O., RAKHA F. A. STUDIES ON NATURAL POPULATIONS OF DROSOPHILA. IV. GENETIC VARIANCES OF AND CORRELATIONS BETWEEN FOUR CHARACTERS IN D. MELANOGASTER AND D. SIMULANS. Genetics. 1964 Dec;50:1349–1355. doi: 10.1093/genetics/50.6.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tantawy A. O., el-Helw M. R. Studies on natural populations of Drosophila. V. Correlated response to selection in Drosophila melanogaster. Genetics. 1966 Jan;53(1):97–110. doi: 10.1093/genetics/53.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]

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