Abstract
Intergenerational mixing of DNA through meiotic recombinations of homologous chromosomes during gametogenesis is a major event that generates diversity in the eukaryotic genome. We examined genome-wide microsatellite data for 23,066 individuals, providing information on recombination events of 14,140 maternal and paternal meioses each, and found a positive correlation between maternal recombination counts of an offspring and maternal age. We postulated that the recombination rate of eggs does not increase with maternal age, but that the apparent increase is the consequence of selection. Specifically, a high recombination count increased the chance of a gamete becoming a live birth, and this effect became more pronounced with advancing maternal age. Further support for this hypothesis came from our observation that mothers with high oocyte recombination rate tend to have more children. Hence, not only do recombinations have a role in evolution by yielding diverse combinations of gene variants for natural selection, but they are also under selection themselves.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
206,07 € per year
only 17,17 € per issue
Buy this article
- Purchase on SpringerLink
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others
References
Kong, A. et al. A high-resolution recombination map of the human genome. Nat. Genet. 31, 241–247 (2002).
Broman, K.W., Murray, J.C., Sheffield, V.C., White, R.L. & Weber, J.L. Comprehensive human genetic map: individual and sex-specific variation in recombination. Am. J. Hum. Genet. 63, 861–869 (1998).
Henderson, S.A. & Edwards, R.G. Chiasma frequency and maternal age in mammals. Nature 218, 22–28 (1968).
Speed, R.M. & Chandley, A.C. Meiosis in the foetal mouse ovary. II. Oocyte development and age-related aneuploidy. Does a production line exist? Chromosoma 88, 184–189 (1983).
Polani, P.E. & Jagiello, G.M. Chiasmata, meiotic univalents and age in relationship to aneuploid imbalance in mice. Cytogenet. Cell. Genet. 16, 505–529 (1976).
Polani, P.E. & Crolla, J.A. A test of the production line hypothesis of mammalian oogenesis. Hum. Genet. 88, 64–70 (1991).
Tanzi, R.E. et al. A genetic linkage map of human chromosome 21: analysis of recombination as a function of sex and age. Am. J. Hum. Genet. 50, 551–558 (1992).
Haines, J.L. et al. A genetic linkage map of chromosome 21: a look at meiotic phenomena. Prog. Clin. Biol. Res. 384, 51–61 (1993).
Elston, R.C., Lange, K. & Namboodiri, K.K. Age trends in human chiasma frequencies and recombination fractions. II method for analyzing recombination fractions and applications to the ABO:nail-patella Linkage. Am. J. Hum. Genet. 28, 69–76 (1976).
Renwick, J.H. & Schulze, J. Male and female recombination fractions, for the nailpatella:ABO linkage in man. Ann. Hum. Genet. 28, 379–392 (1965).
Weitkamp, L.R. et al. The relation of parental sex and age to recombination in the HLA system. Hum. Hered. 23, 197–205 (1973).
Gulcher, J.R., Kristjansson, K., Gudbjartsson, H. & Stefansson, K. Protection of privacy by third-party encryption in genetic research in Iceland. Eur. J. Hum. Genet. 8, 739–742 (2000).
Little, R.J.A. & Rubin, D.B. Statistical Analysis with Missing Data (John Wiley & Sons, New York, 1987).
Hassold, T.J., Sherman, S. & Hunt, P. Counting cross-overs: characterizing meiotic recombination in mammals. Hum. Mol. Genet. 9, 2409–2419 (2000).
Robinson, W. et al. Maternal meiosis I nondisjunction of chromosome 15: dependence of the maternal age effect on the level of recombination. Hum. Mol. Genet. 7, 1011–1109 (1998).
Hodges, C.A. et al. Experimental evidence that changes in oocyte growth influence meiotic chromosome segregation. Hum. Reproduction. 17, 1171–1180 (2002).
Hunt, P.A. & Hassold, T.J. Sex matters in meiosis. Science 296, 2181–2183 (2002).
Lamb, N.E. et al. Characterization of susceptible chiasma configurations that increase the risk for maternal nondisjuction of chromosome 21. Hum. Mol. Genet. 6, 1391–1399 (1997).
Lynn, A. et al. Covariation of synaptonemal complex length and mammalian meiotic exchange rates. Science 296, 2222–2225 (2002).
Johnson, J., Canning, J., Kaneko, T., Pru, J.K. & Tilly, T.L. Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428, 145–150 (2004).
Lynch, M. & Walsh, B. Genetics and Analysis of Quantitative Traits (Sinauer Associates, Massachusetts, 1998).
Dempster, A.P., Laird, N.M. & Rubin, D.B. Maximum likelihood from incomplete data via the EM algorithm. J. R. Stat. Soc. Ser. B Methodol. 39, 1–38 (1977).
Gudbjartsson, D.F., Jonasson, K., Frigge, M.L. & Kong, A. Allegro, a new computer program for multipoint linkage analysis. Nat. Genet. 25, 12–14 (2000).
McCulloch, C.E. Maximum likelihood algorithms for generalized linear mixed models. J. Am. Stat. Assoc. 92, 162–170 (1997).
Broman, K.W. & Weber, J.L. Characterization of human crossover interference. Am. J. Hum. Genet. 66, 1911–1926 (2000).
Irwin, M., Cox, N.J. & Kong, A. Sequential imputation for multilocus linkage analysis. Proc. Natl. Acad. Sci. USA 91, 11684–11688 (1994).
Quintana, F.A., Liu, J.S. & del Pino, G.E. Monte carlo EM with importance reweighting and its applications in random effects model. Comput. Stat. Data Anal. 29, 429–444 (1999).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
A.K., D.F.G., G.T., G.J., S.S., B.R., J.J., T.T., M.L.F., J.R.G. and K.S. have stocks and equity interests in deCODE Genetics.
Supplementary information
Supplementary Fig. 1
Boxplots of the distribution of maternal recombinations for individual offspring within the grouping of mother's birth age. (PDF 1314 kb)
Supplementary Fig. 2
Paternal recombinations and father's age at birth (PDF 808 kb)
Supplementary Table 1
A description of the 6 cM telomeric regions used in Table 4. (PDF 1179 kb)
Supplementary Table 2
Distribution of the father's age at birth for all offspring. (PDF 823 kb)
Rights and permissions
About this article
Cite this article
Kong, A., Barnard, J., Gudbjartsson, D. et al. Recombination rate and reproductive success in humans. Nat Genet 36, 1203–1206 (2004). https://doi.org/10.1038/ng1445
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/ng1445