Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2001 Feb 22;268(1465):399–405. doi: 10.1098/rspb.2000.1392

Genetic divergence of the seminal signal-receptor system in houseflies: the footprints of sexually antagonistic coevolution?

J A Andrés 1, G Arnqvist 1
PMCID: PMC1088620  PMID: 11270437

Abstract

To understand fully the significance of cryptic female choice, we need to focus on each of those postmating processes in females which create variance in fitness among males. Earlier studies have focused almost exclusively on the proportion of a female's eggs fertilized by different males (sperm precedence). Yet, variance in male postmating reproductive success may also arise from differences in ability to stimulate female oviposition and to delay female remating. Here, we present a series of reciprocal mating experiments among genetically differentiated wild-type strains of the housefly Musca domestica. We compared the effects of male and female genotype on oviposition and remating by females. The genotype of each sex affected both female oviposition and remating rates, demonstrating that the signal-receptor system involved has indeed diverged among these strains. Further, there was a significant interaction between the effects of male and female genotype on oviposition rate. We discuss ways in which the pattern of such interactions provides insights into the coevolutionary mechanism involved. Females in our experiments generally exhibited the weakest, rather than the strongest, response to males with which they are coevolved. These results support the hypothesis that coevolution of male seminal signals and female receptors is sexually antagonistic.

Full Text

The Full Text of this article is available as a PDF (156.4 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams T. S., Nelson D. R. Bioassay of crude extracts for the factor that prevents second matings in female musca domestica. Ann Entomol Soc Am. 1968 Jan;61(1):112–116. doi: 10.1093/aesa/61.1.112. [DOI] [PubMed] [Google Scholar]
  2. Aguadé M. Different forces drive the evolution of the Acp26Aa and Acp26Ab accessory gland genes in the Drosophila melanogaster species complex. Genetics. 1998 Nov;150(3):1079–1089. doi: 10.1093/genetics/150.3.1079. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Aguadé M. Positive selection drives the evolution of the Acp29AB accessory gland protein in Drosophila. Genetics. 1999 Jun;152(2):543–551. doi: 10.1093/genetics/152.2.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Arnqvist G, Nilsson T. The evolution of polyandry: multiple mating and female fitness in insects. Anim Behav. 2000 Aug;60(2):145–164. doi: 10.1006/anbe.2000.1446. [DOI] [PubMed] [Google Scholar]
  5. Birkhead T. R. Defining and demonstrating postcopulatory female choice--again. Evolution. 2000 Jun;54(3):1057–1060. doi: 10.1111/j.0014-3820.2000.tb00108.x. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. 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]
  8. Chapman T., Neubaum D. M., Wolfner M. F., Partridge L. The role of male accessory gland protein Acp36DE in sperm competition in Drosophila melanogaster. Proc Biol Sci. 2000 Jun 7;267(1448):1097–1105. doi: 10.1098/rspb.2000.1114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Civetta A., Clark A. G. Chromosomal effects on male and female components of sperm precedence in Drosophila. Genet Res. 2000 Apr;75(2):143–151. doi: 10.1017/s0016672399004292. [DOI] [PubMed] [Google Scholar]
  10. Civetta A., Singh R. S. High divergence of reproductive tract proteins and their association with postzygotic reproductive isolation in Drosophila melanogaster and Drosophila virilis group species. J Mol Evol. 1995 Dec;41(6):1085–1095. doi: 10.1007/BF00173190. [DOI] [PubMed] [Google Scholar]
  11. Clark A. G., Aguadé M., Prout T., Harshman L. G., Langley C. H. Variation in sperm displacement and its association with accessory gland protein loci in Drosophila melanogaster. Genetics. 1995 Jan;139(1):189–201. doi: 10.1093/genetics/139.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clark A. G., Begun D. J. Female genotypes affect sperm displacement in Drosophila. Genetics. 1998 Jul;149(3):1487–1493. doi: 10.1093/genetics/149.3.1487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Clark A. G., Begun D. J., Prout T. Female x male interactions in Drosophila sperm competition. Science. 1999 Jan 8;283(5399):217–220. doi: 10.1126/science.283.5399.217. [DOI] [PubMed] [Google Scholar]
  14. Fukui H. H., Gromko M. H. Genetic basis for remating in Drosophila melanogaster. VI. Recombination analysis. Behav Genet. 1991 Mar;21(2):199–209. doi: 10.1007/BF01066336. [DOI] [PubMed] [Google Scholar]
  15. Gromko M. H., Newport M. E. Genetic basis for remating in Drosophila melanogaster. II. Response to selection based on the behavior of one sex. Behav Genet. 1988 Sep;18(5):621–632. doi: 10.1007/BF01082313. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Hughes K. A. Quantitative genetics of sperm precedence in Drosophila melanogaster. Genetics. 1997 Jan;145(1):139–151. doi: 10.1093/genetics/145.1.139. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. KEIDING J., AREVAD K. PROCEDURE AND EQUIPMENT FOR REARING A LARGE NUMBER OF HOUSEFLY STRAINS. Bull World Health Organ. 1964;31:527–528. [PMC free article] [PubMed] [Google Scholar]
  19. Keller L. Evolutionary biology. All's fair when love is war. Nature. 1995 Jan 19;373(6511):190–191. doi: 10.1038/373190a0. [DOI] [PubMed] [Google Scholar]
  20. Leopold R. A., Terranova A. C., Swilley E. M. Mating refusal in Musca domestica: effects of repeated mating and decerebration upon frequency and duration of copulation. J Exp Zool. 1971 Mar;176(3):353–359. doi: 10.1002/jez.1401760310. [DOI] [PubMed] [Google Scholar]
  21. doi: 10.1098/rspb.1997.0206. [DOI] [PMC free article] [Google Scholar]
  22. doi: 10.1098/rstb.1997.0061. [DOI] [PMC free article] [Google Scholar]
  23. Parker G. A., Partridge L. Sexual conflict and speciation. Philos Trans R Soc Lond B Biol Sci. 1998 Feb 28;353(1366):261–274. doi: 10.1098/rstb.1998.0208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pitnick S., Brown W. D. Criteria for demonstrating female sperm choice. Evolution. 2000 Jun;54(3):1052–1056. doi: 10.1111/j.0014-3820.2000.tb00107.x. [DOI] [PubMed] [Google Scholar]
  25. Pizzari T., Birkhead T. R. Female feral fowl eject sperm of subdominant males. Nature. 2000 Jun 15;405(6788):787–789. doi: 10.1038/35015558. [DOI] [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. Riemann J. G., Moen D. J., Thorson B. J. Female monogamy and its control in houselfies. J Insect Physiol. 1967 Jan;13(3):407–418. doi: 10.1016/0022-1910(67)90081-9. [DOI] [PubMed] [Google Scholar]
  28. Riemann J. G., Thorson B. J. Effect of male accessory material on oviposition and mating by female house flies. Ann Entomol Soc Am. 1969 Jul;62(4):828–834. doi: 10.1093/aesa/62.4.828. [DOI] [PubMed] [Google Scholar]
  29. Service P. M., Vossbrink R. E. Genetic variation in "first" male effects on egg laying and remating by female Drosophila melanogaster. Behav Genet. 1996 Jan;26(1):39–48. doi: 10.1007/BF02361157. [DOI] [PubMed] [Google Scholar]
  30. Sgrò CM, Chapman T, Partridge L. Sex-specific selection on time to remate in Drosophila melanogaster. Anim Behav. 1998 Nov;56(5):1267–1278. doi: 10.1006/anbe.1998.0900. [DOI] [PubMed] [Google Scholar]
  31. Terranova A. C., Leopold R. A., Degrugillier M. E., Johnson J. R. Electrophoresis of the male accessory secretion and its fate in the mated female. J Insect Physiol. 1972 Aug;18(8):1573–1591. doi: 10.1016/0022-1910(72)90235-1. [DOI] [PubMed] [Google Scholar]
  32. Thomas S., Singh R. S. A comprehensive study of genic variation in natural populations of Drosophila melanogaster. VII. Varying rates of genic divergence as revealed by two-dimensional electrophoresis. Mol Biol Evol. 1992 May;9(3):507–525. doi: 10.1093/oxfordjournals.molbev.a040738. [DOI] [PubMed] [Google Scholar]
  33. Tsaur S. C., Ting C. T., Wu C. I. Positive selection driving the evolution of a gene of male reproduction, Acp26Aa, of Drosophila: II. Divergence versus polymorphism. Mol Biol Evol. 1998 Aug;15(8):1040–1046. doi: 10.1093/oxfordjournals.molbev.a026002. [DOI] [PubMed] [Google Scholar]
  34. Van Vianen A., Bijlsma R. The adult component of selection in Drosophila melanogaster: some aspects of early-remating activity of females. Heredity (Edinb) 1993 Sep;71(Pt 3):269–276. doi: 10.1038/hdy.1993.135. [DOI] [PubMed] [Google Scholar]
  35. Wolfner M. F., Harada H. A., Bertram M. J., Stelick T. J., Kraus K. W., Kalb J. M., Lung Y. O., Neubaum D. M., Park M., Tram U. New genes for male accessory gland proteins in Drosophila melanogaster. Insect Biochem Mol Biol. 1997 Oct;27(10):825–834. doi: 10.1016/s0965-1748(97)00056-8. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES