Comparison of Rates and Patterns of Meiotic Recombination between Human and Chimpanzee


Despite the high sequence similarity between the human and chimpanzee genomes, little conservation of recombination rates exists on a kilobase scale. In contrast, recombination rates are highly conserved on a larger scale, consistent with an influence of karyotype structure. In both species, recombination mainly occurs in recombination hotspots that are marked by histone‐methylation through PRDM9. A specific sequence motif was found enriched in hotspots in humans and may direct PRDM9 to the respective regions. The fast evolutionary change of fine‐scale recombination rates is paralleled by a fast sequence evolution of the nucleotide‐binding domain of PRDM9. Accordingly, the human hotspot motif is not enriched in chimpanzee recombination hotspots. As hotspots are sequence‐based traits that show heritable variation in the population, their specific locations could be influenced by natural selection. Consistently, recombination hotspots are enriched at genes that are under particularly strong selective pressure, such as immune and nervous system genes.

Key Concepts

  • Recombination is a fundamental force in inheritance and evolution.

  • Large‐scale recombination rates are highly conserved between humans and chimpanzees, whereas fine‐scale recombination rates evolve extremely fast.

  • Karyotype structure is a major determinant of large‐scale recombination rates.

  • Recombination mainly occurs in recombination hotspots that are marked by histone‐methylation through PRDM9 both in humans and chimpanzees.

  • A sequence motif is likely to direct PRDM9 to recombination hotspot regions.

  • Fine‐scale recombination rate is correlated with the rate of sequence evolution.

  • Fine‐scale recombination rates are increased around genes with role in the nervous system or the immune system.

Keywords: recombination rate; recombination hotspot; sequence evolution

Figure 1.

Two‐parameter regression of human genetic length over physical length. (a) Analysis at the chromosome scale. (squares) Female, (open circles) male and (solid circles) sex‐averaged genetic length of each chromosome (in centimorgans, cM) is plotted against its physical length (in megabases, Mb). The least‐square regression lines are: y=54.2+1.02x (female), y=42.0+0.52x (male) and y=48.1+0.78x (sex average). (b) Analysis of metacentric chromosome at the chromosome‐arm scale. The best fit regression lines are: y=29.0+1.05x (female), y=27.1+0.48x (male) and y=28.0+0.77x (sex average).

Originally published in Genome Research. Reproduced with permission from Li and Freudenberg . © W. Li and J. Freudenberg.
Figure 2.

Frequency histogram of P‐values for testing the enrichment of recombination hotspots around genes from 1266 GO categories. The excess of P‐values that are close to zero and P‐values that are close to one indicate the existence of GO categories that are enriched or depleted of recombination hotspots. GO categories enriched for recombination hotspots predominantly include genes functioning in the immune and the nervous system.



Auton A, Fledel‐Alon A, Pfeifer S et al. (2012) A fine‐scale chimpanzee genetic map from population sequencing. Science 336(6078): 193–198.

Barlow AL and Hultén MA (1998) Crossing over analysis at pachytene in man. European Journal of Human Genetics 6(4): 350–358.

Baudat F, Buard J, Grey C et al. (2010) PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice. Science 327(5967): 836–840.

Berg IL, Neumann R, Lam KW et al. (2010) PRDM9 variation strongly influences recombination hot‐spot activity and meiotic instability in humans. Nature Genetics 42(10): 859–863.

Botstein D, White RL, Skolnick M and Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. American Journal of Human Genetics 32(3): 314–331.

Broman KW, Murray JC, Sheffield VC, White RL and Weber JL (1998) Comprehensive human genetic maps: individual and sex‐specific variation in recombination. American Journal of Human Genetics 63(3): 861–869.

Charlesworth B (2012) The effects of deleterious mutations on evolution at linked sites. Genetics 190(1): 5–22.

Cheung VG, Burdick JT, Hirschmann D and Morley M (2007) Polymorphic variation in human meiotic recombination. American Journal of Human Genetics 80: 526–530.

Coop G, Wen X, Ober C, Pritchard JK and Przeworski M (2008) High‐resolution mapping of crossovers reveals extensive variation in fine‐scale recombination patterns among humans. Science 319(5868): 1395–1398.

Daly MJ, Rioux JD, Schaffner SF, Hudson TJ and Lander ES (2001) High‐resolution haplotype structure in the human genome. Nature Genetics 29(2): 229–232.

Dib C, Fauré S, Fizames C et al. (1996) A comprehensive genetic map of the human genome based on 5,264 microsatellites. Nature 380(6570): 152–154.

Dorus S, Vallender EJ, Evans PD et al. (2004) Accelerated evolution of nervous system genes in the origin of Homo sapiens. Cell 119(7): 1027–1040.

Dumont BL and Payseur BA (2008) Evolution of the genomic rate of recombination in mammals. Evolution 62(2): 276–294.

Fledel‐Alon A, Wilson DJ, Broman K, et al. (2009) Broad‐scale recombination patterns underlying proper disjunction in humans. PLoS Genetics 5(9): e1000658.

Freudenberg J, Fu YH and Ptacek LJ (2007) Enrichment of HapMap recombination hotspot predictions around human nervous system genes: evidence for positive selection? European Journal of Human Genetics 15(10): 1071–1078.

Galtier N and Duret L (2007) Adaptation or biased gene conversion? Extending the null hypothesis of molecular evolution. Trends in Genetics 23(6): 273–277.

Hellmann I, Prüfer K, Ji H et al. (2005) Why do human diversity levels vary at a megabase scale? Genome Research 15(9): 1222–1231.

Hill WG and Robertson A (1966) The effect of linkage on limits to artificial selection. Genetics Research 8(3): 269–294.

Ijdo JW, Baldini A, Ward DC, Reeders ST and Wells RA (1991) Origin of human chromosome 2: an ancestral telomere‐telomere fusion. Proceedings of the National Academy of Sciences of the USA 88(20): 9051–9055.

International Chimpanzee Sequencing and Analysis Consortium (2005) Initial sequence of the chimpanzee genome and comparison with the human genome. Nature 437(7055): 69–87.

International HapMap Consortium (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449: 851–861.

International Human Genome Sequencing Consortium (2001) Initial sequencing and analysis of the human genome. Nature 409(6822): 860–921.

Jeffreys AJ, Kauppi L and Neumann R (2001) Intensely punctate meiotic recombination in the class II region of the major histocompatibility complex. Nature Genetics 29(2): 217–222.

Jeffreys AJ and Neumann R (2002) Reciprocal crossover asymmetry and meiotic drive in a human recombination hot spot. Nature Genetics 31(3): 267–271.

Keightley PD and Otto SP (2006) Interference among deleterious mutations favours sex and recombination in finite populations. Nature 443(7107): 89–92.

Kong A, Barnard J, Gudbjartsson DF et al. (2004) Recombination rate and reproductive success in humans. Nature Genetics 36(11): 1203–1206.

Kong A, Gudbjartsson DF, Sainz J et al. (2002) A high‐resolution recombination map of the human genome. Nature Genetics 31(3): 241–247.

Kong A, Thorleifsson G, Gudbjartsson DF et al. (2010) Fine‐scale recombination rate differences between sexes, populations and individuals. Nature 467(7319): 1099–1103.

Kong A, Thorleifsson G, Stefansson H et al. (2008) Sequence variants in the RNF212 gene associate with genome‐wide recombination rate. Science 319(5868): 1398–1401.

Kostka D, Hubisz MJ, Siepel A and Pollard KS (2012) The role of GC‐biased gene conversion in shaping the fastest evolving regions of the human genome. Molecular Biology and Evolution 29(3): 1047–1057.

Lenzi ML, Smith J, Snowden T et al. (2005) Extreme heterogeneity in the molecular events leading to the establishment of chiasmata during meiosis i in human oocytes. American Journal of Human Genetics 76(1): 112–127.

Lercher MJ and Hurst LD (2002) Human SNP variability and mutation rate are higher in regions of high recombination. Trends in Genetics 18(7): 337–340.

Li W and Freudenberg J (2009) Two‐parameter characterization of chromosome‐scale recombination rate. Genome Research 19(12): 2300–2307.

Mather K (1937) Crossing over. Biological Reviews of the Cambridge Philosophical Society 13: 258–292.

Meyer M, Kircher M, Gansauge MT et al. (2012) A high‐coverage genome sequence from an archaic Denisovan individual. Science 338(6104): 222–226.

Morgan TH, Sturtevant AH, Muller HJ and Bridge CB (1915) The Mechanism of Mendelian Heredity. New York: Henry Holt.

Muller HJ (1931) Some genetic aspects of sex. American Naturalist 66(703): 118–138.

Muller HJ (1964) The relation of recombination to mutational advance. Mutation Research 1: 2–9.

Myers S, Bottolo L, Freeman C, McVean G and Donnelly P (2005) A fine‐scale map of recombination rates and hotspots across the human genome. Science 310(5746): 321–324.

Myers S, Bowden R, Tumian A et al. (2010) Drive against hotspot motifs in primates implicates the PRDM9 gene in meiotic recombination. Science 327(5967): 876–879.

Nachman MW (2001) Single nucleotide polymorphisms and recombination rate in humans. Trends in Genetics 17(9): 481–485.

Necsulea A, Sémon M, Duret L and Hurst LD (2009) Monoallelic expression and tissue specificity are associated with high crossover rates. Trends in Genetics 25(12): 519–522.

Pardo‐Manuel de Villena F and Sapienza C (2001) Recombination is proportional to the number of chromosome arms in mammals. Mammalian Genome 12(4): 318–322.

Parvanov ED, Petkov PM and Paigen K (2010) Prdm9 controls activation of mammalian recombination hotspots. Science 327(5967): 835.

Ptak SE, Hinds DA, Koehler K et al. (2005) Fine‐scale recombination patterns differ between chimpanzees and humans. Nature Genetics 37(4): 429–434.

Reich DE, Schaffner SF, Daly MJ et al. (2002) Human genome sequence variation and the influence of gene history, mutation and recombination. Nature Genetics 32(1): 135–142.

Rice WR and Chippindale AK (2001) Sexual recombination and the power of natural selection. Science 294(5542): 555–559.

Sandovici I, Kassovska‐Bratinova S, Vaughan JE et al. (2006) Human imprinted chromosomal regions are historical hot‐spots of recombination. PLoS Genetics 2(7): e101.

Spencer CC, Deloukas P, Hunt S et al. (2006) The influence of recombination on human genetic diversity. PLoS Genetics 2(9): e148.

Thomas JH, Emerson RO and Shendure J (2009) Extraordinary molecular evolution in the PRDM9 fertility gene. PLoS One 4(12): e8505.

Winckler W, Myers SR, Richter DJ et al. (2005) Comparison of fine‐scale recombination rates in humans and chimpanzees. Science 308(5718): 107–111.

Further Reading

Clark AG, Wang X and Matise T (2010) Contrasting methods of quantifying fine structure of human recombination. Annual Review of Genomics and Human Genetics 11: 45–64.

Coop G and Przeworski M (2007) An evolutionary view of recombination. Nature Reviews. Genetics 8: 23–34.

Lynn A, Ashley and Hassold T (2004) Variation in human meiotic recombination. Annual Review of Genomics and Human Genetics 5: 317–349.

McVean G (2010) What drives recombination hotspots to repeat DNA in humans? Philosophical Transactions of the Royal Society B: Biological Sciences 365(1544): 1213–1218.

Paigen K and Petkov P (2010) Mammalian recombination hot spots: properties, control and evolution. Nature Reviews Genetics 11(3): 221–233.

Ponting CP (2011) What are the genomic drivers of the rapid evolution of PRDM9? Trends in Genetics 27(5): 165–171.

Rice WR (2002) Experimental tests of the adaptive significance of sexual recombination. Nature Reviews Genetics 3: 241–251.

Smukowski CS and Noor MA (2011) Recombination rate variation in closely related species. Heredity 107(6): 496–508.

Stumpf MP and McVean G (2003) Estimating recombination rates from population genetic data. Nature Reviews Genetics 4: 959–968.

Webster MT and Hurst LD (2012) Direct and indirect consequences of meiotic recombination: implications for genome evolution. Trends in Genetics 28(3): 101–109.

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Freudenberg, Jan(Oct 2013) Comparison of Rates and Patterns of Meiotic Recombination between Human and Chimpanzee. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0020845.pub2]