Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2004 Aug 7;271(Suppl 5):S306–S309. doi: 10.1098/rsbl.2004.0169

Sexy sons: a dead end for cytoplasmic genes.

Jeanne A Zeh 1
PMCID: PMC1810078  PMID: 15504002

Abstract

Critics of sexual conflict theory argue that females may gain a net reproductive benefit from mating with manipulative males because the direct costs that they suffer may be offset by the production of sexy, i.e. manipulative, sons. However, this exclusive focus on nuclear gene effects represents an incomplete view of female fitness. Females differ fundamentally from males in transmitting not only nuclear genes but also a wide range of cytoplasmic genetic elements (CGEs) that can have profound effects, from male killing to influencing development of the nervous system and cognitive ability. Maternal transmission of CGEs has two major implications for sexual selection. First, the evolution of male fitness traits, such as sperm competitive ability, may be constrained because response to selection on mitochondrial genomes can occur only through the female line. Second, CGEs bear the direct costs of male manipulation but gain no indirect benefits when females produce sexy sons. This should result in perpetual antagonistic coevolution between nuclear genes involved in male manipulation and CGEs that promote female resistance to male sexually selected traits. Explicit consideration of the consequences of selection acting on CGEs is therefore necessary for a better understanding of the relationship between sexual selection and sexual conflict.

Full Text

The Full Text of this article is available as a PDF (74.5 KB).

Selected References

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

  1. Budar F., Pelletier G. Male sterility in plants: occurrence, determinism, significance and use. C R Acad Sci III. 2001 Jun;324(6):543–550. doi: 10.1016/s0764-4469(01)01324-5. [DOI] [PubMed] [Google Scholar]
  2. Cameron E., Day T., Rowes L. Sexual conflict and indirect benefits. J Evol Biol. 2003 Sep;16(5):1055–1060. doi: 10.1046/j.1420-9101.2003.00584.x. [DOI] [PubMed] [Google Scholar]
  3. Charlat Sylvain, Hurst Gregory D. D., Merçot Hervé. Evolutionary consequences of Wolbachia infections. Trends Genet. 2003 Apr;19(4):217–223. doi: 10.1016/S0168-9525(03)00024-6. [DOI] [PubMed] [Google Scholar]
  4. Cordero C., Eberhard W. G. Female choice of sexually antagonistic male adaptations: a critical review of some current research. J Evol Biol. 2003 Jan;16(1):1–6. doi: 10.1046/j.1420-9101.2003.00506.x. [DOI] [PubMed] [Google Scholar]
  5. Cosmides L. M., Tooby J. Cytoplasmic inheritance and intragenomic conflict. J Theor Biol. 1981 Mar 7;89(1):83–129. doi: 10.1016/0022-5193(81)90181-8. [DOI] [PubMed] [Google Scholar]
  6. Eberhard W. G. Evolutionary consequences of intracellular organelle competition. Q Rev Biol. 1980 Sep;55(3):231–249. doi: 10.1086/411855. [DOI] [PubMed] [Google Scholar]
  7. Froman David P., Pizzari Tommaso, Feltmann Allen J., Castillo-Juarez Hector, Birkhead Tim R. Sperm mobility: mechanisms of fertilizing efficiency, genetic variation and phenotypic relationship with male status in the domestic fowl, Gallus gallus domesticus. Proc Biol Sci. 2002 Mar 22;269(1491):607–612. doi: 10.1098/rspb.2001.1925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hosken D. J., Blanckenhorn W. U., Garner T. W. J. Heteropopulation males have a fertilization advantage during sperm competition in the yellow dung fly (Scathophaga stercoraria). Proc Biol Sci. 2002 Aug 22;269(1501):1701–1707. doi: 10.1098/rspb.2002.2094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jeyaprakash A., Hoy M. A. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol. 2000 Aug;9(4):393–405. doi: 10.1046/j.1365-2583.2000.00203.x. [DOI] [PubMed] [Google Scholar]
  10. Jiggins F. M., Hurst G. D., Majerus M. E. Sex-ratio-distorting Wolbachia causes sex-role reversal in its butterfly host. Proc Biol Sci. 2000 Jan 7;267(1438):69–73. doi: 10.1098/rspb.2000.0968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kokko Hanna, Brooks Robert, McNamara John M., Houston Alasdair I. The sexual selection continuum. Proc Biol Sci. 2002 Jul 7;269(1498):1331–1340. doi: 10.1098/rspb.2002.2020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Pizzari T., Birkhead T. R. The sexually-selected sperm hypothesis: sex-biased inheritance and sexual antagonism. Biol Rev Camb Philos Soc. 2002 May;77(2):183–209. doi: 10.1017/s1464793101005863. [DOI] [PubMed] [Google Scholar]
  13. Pizzari Tommaso, Snook Rhonda R. Perspective: sexual conflict and sexual selection: chasing away paradigm shifts. Evolution. 2003 Jun;57(6):1223–1236. doi: 10.1111/j.0014-3820.2003.tb00331.x. [DOI] [PubMed] [Google Scholar]
  14. Roubertoux Pierre L., Sluyter Frans, Carlier Michèle, Marcet Brice, Maarouf-Veray Fatima, Chérif Chabane, Marican Charlotte, Arrechi Patricia, Godin Fabienne, Jamon Marc. Mitochondrial DNA modifies cognition in interaction with the nuclear genome and age in mice. Nat Genet. 2003 Aug 17;35(1):65–69. doi: 10.1038/ng1230. [DOI] [PubMed] [Google Scholar]
  15. Stewart D. T., Kenchington E. R., Singh R. K., Zouros E. Degree of selective constraint as an explanation of the different rates of evolution of gender-specific mitochondrial DNA lineages in the mussel mytilus. Genetics. 1996 Jul;143(3):1349–1357. doi: 10.1093/genetics/143.3.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Werren J. H., Hurst G. D., Zhang W., Breeuwer J. A., Stouthamer R., Majerus M. E. Rickettsial relative associated with male killing in the ladybird beetle (Adalia bipunctata). J Bacteriol. 1994 Jan;176(2):388–394. doi: 10.1128/jb.176.2.388-394.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Zouros E., Oberhauser Ball A., Saavedra C., Freeman K. R. An unusual type of mitochondrial DNA inheritance in the blue mussel Mytilus. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7463–7467. doi: 10.1073/pnas.91.16.7463. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES