The evolution of sex dimorphism in recombination (original) (raw)

Abstract

Sex dimorphism in recombination is widespread on both sex chromosomes and autosomes. Various hypotheses have been proposed to explain these dimorphisms. Yet no theoretical model has been explored to determine how heterochiasmy--the autosomal dimorphism--could evolve. The model presented here shows three circumstances in which heterochiasmy is likely to evolve: (i) a male-female difference in haploid epistasis, (ii) a male-female difference in cis-epistasis minus trans-epistasis in diploids, or (iii) a difference in epistasis between combinations of genes inherited maternally or paternally. These results hold even if sources of linkage disequilibria besides epistasis, such as migration or Hill-Robertson interference, are considered and shed light on previous verbal models of sex dimorphism in recombination rates. Intriguingly, these results may also explain why imprinted regions on the autosomes of humans or sheep are particularly heterochiasmate.

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Selected References

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  1. Bartolomei M. S., Tilghman S. M. Genomic imprinting in mammals. Annu Rev Genet. 1997;31:493–525. doi: 10.1146/annurev.genet.31.1.493. [DOI] [PubMed] [Google Scholar]
  2. Barton N. H. A general model for the evolution of recombination. Genet Res. 1995 Apr;65(2):123–145. doi: 10.1017/s0016672300033140. [DOI] [PubMed] [Google Scholar]
  3. Barton N. H., Charlesworth B. Why sex and recombination? Science. 1998 Sep 25;281(5385):1986–1990. [PubMed] [Google Scholar]
  4. Barton N. H., Turelli M. Natural and sexual selection on many loci. Genetics. 1991 Jan;127(1):229–255. doi: 10.1093/genetics/127.1.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Burns J. L., Jackson D. A., Hassan A. B. A view through the clouds of imprinting. FASEB J. 2001 Aug;15(10):1694–1703. doi: 10.1096/fj.010085rev. [DOI] [PubMed] [Google Scholar]
  6. Charlesworth D., Charlesworth B. Sex differences in fitness and selection for centric fusions between sex-chromosomes and autosomes. Genet Res. 1980 Apr;35(2):205–214. doi: 10.1017/s0016672300014051. [DOI] [PubMed] [Google Scholar]
  7. Charlesworth Deborah. Plant sex determination and sex chromosomes. Heredity (Edinb) 2002 Feb;88(2):94–101. doi: 10.1038/sj.hdy.6800016. [DOI] [PubMed] [Google Scholar]
  8. Christians E., Boiani M., Garagna S., Dessy C., Redi C. A., Renard J. P., Zuccotti M. Gene expression and chromatin organization during mouse oocyte growth. Dev Biol. 1999 Mar 1;207(1):76–85. doi: 10.1006/dbio.1998.9157. [DOI] [PubMed] [Google Scholar]
  9. Korol A. B., Iliadi K. G. Increased recombination frequencies resulting from directional selection for geotaxis in Drosophila. Heredity (Edinb) 1994 Jan;72(Pt 1):64–68. doi: 10.1038/hdy.1994.7. [DOI] [PubMed] [Google Scholar]
  10. Kramer J. A., Krawetz S. A. RNA in spermatozoa: implications for the alternative haploid genome. Mol Hum Reprod. 1997 Jun;3(6):473–478. doi: 10.1093/molehr/3.6.473. [DOI] [PubMed] [Google Scholar]
  11. Lenormand T., Otto S. P. The evolution of recombination in a heterogeneous environment. Genetics. 2000 Sep;156(1):423–438. doi: 10.1093/genetics/156.1.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lloyd V. K., Sinclair D. A., Grigliatti T. A. Genomic imprinting and position-effect variegation in Drosophila melanogaster. Genetics. 1999 Apr;151(4):1503–1516. doi: 10.1093/genetics/151.4.1503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McCormick S. Molecular analysis of male gametogenesis in plants. Trends Genet. 1991 Sep;7(9):298–303. doi: 10.1016/0168-9525(91)90312-E. [DOI] [PubMed] [Google Scholar]
  14. Nagylaki T. The evolution of one- and two-locus systems. Genetics. 1976 Jul;83(3 PT2):583–600. [PMC free article] [PubMed] [Google Scholar]
  15. Nei M. Linkage modifications and sex difference in recombination. Genetics. 1969 Nov;63(3):681–699. doi: 10.1093/genetics/63.3.681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Otto S. P., Barton N. H. Selection for recombination in small populations. Evolution. 2001 Oct;55(10):1921–1931. doi: 10.1111/j.0014-3820.2001.tb01310.x. [DOI] [PubMed] [Google Scholar]
  17. Otto S. P., Barton N. H. The evolution of recombination: removing the limits to natural selection. Genetics. 1997 Oct;147(2):879–906. doi: 10.1093/genetics/147.2.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Otto Sarah P., Lenormand Thomas. Resolving the paradox of sex and recombination. Nat Rev Genet. 2002 Apr;3(4):252–261. doi: 10.1038/nrg761. [DOI] [PubMed] [Google Scholar]
  19. Pylkov K. V., Zhivotovsky L. A., Feldman M. W. Migration versus mutation in the evolution of recombination under multilocus selection. Genet Res. 1998 Jun;71(3):247–256. doi: 10.1017/s0016672398003243. [DOI] [PubMed] [Google Scholar]
  20. Pàldi A., Gyapay G., Jami J. Imprinted chromosomal regions of the human genome display sex-specific meiotic recombination frequencies. Curr Biol. 1995 Sep 1;5(9):1030–1035. doi: 10.1016/s0960-9822(95)00207-7. [DOI] [PubMed] [Google Scholar]
  21. Sewell M. M., Sherman B. K., Neale D. B. A consensus map for loblolly pine (Pinus taeda L.). I. Construction and integration of individual linkage maps from two outbred three-generation pedigrees. Genetics. 1999 Jan;151(1):321–330. doi: 10.1093/genetics/151.1.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Singer Amy, Perlman Hodel, Yan YiLin, Walker Charlene, Corley-Smith Graham, Brandhorst Bruce, Postlethwait John. Sex-specific recombination rates in zebrafish (Danio rerio). Genetics. 2002 Feb;160(2):649–657. doi: 10.1093/genetics/160.2.649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Steger K. Transcriptional and translational regulation of gene expression in haploid spermatids. Anat Embryol (Berl) 1999 Jun;199(6):471–487. doi: 10.1007/s004290050245. [DOI] [PubMed] [Google Scholar]
  24. Taylor Loverine P., Hepler Peter K. POLLEN GERMINATION AND TUBE GROWTH. Annu Rev Plant Physiol Plant Mol Biol. 1997 Jun;48(NaN):461–491. doi: 10.1146/annurev.arplant.48.1.461. [DOI] [PubMed] [Google Scholar]
  25. Xu H., Swoboda I., Bhalla P. L., Singh M. B. Male gametic cell-specific gene expression in flowering plants. Proc Natl Acad Sci U S A. 1999 Mar 2;96(5):2554–2558. doi: 10.1073/pnas.96.5.2554. [DOI] [PMC free article] [PubMed] [Google Scholar]