Genetics, Vol. 160, 1231-1241, March 2002, Copyright © 2002

A Coalescent-Based Method for Detecting and Estimating Recombination From Gene Sequences

Gil McVeana, Philip Awadallab, and Paul Fearnheada
a Department of Statistics, University of Oxford, Oxford OX1 3TG, United Kingdom
b Section of Evolution and Ecology, University of California, Davis, California 95616

Corresponding author: Gil McVean, 1 S. Parks Rd., Oxford OX1 3TG, United Kingdom., mcvean{at}stats.ox.ac.uk (E-mail)

Communicating editor: J. HEY

Determining the amount of recombination in the genealogical history of a sample of genes is important to both evolutionary biology and medical population genetics. However, recurrent mutation can produce patterns of genetic diversity similar to those generated by recombination and can bias estimates of the population recombination rate. HUDSON 2001 Down has suggested an approximate-likelihood method based on coalescent theory to estimate the population recombination rate, 4Ner, under an infinite-sites model of sequence evolution. Here we extend the method to the estimation of the recombination rate in genomes, such as those of many viruses and bacteria, where the rate of recurrent mutation is high. In addition, we develop a powerful permutation-based method for detecting recombination that is both more powerful than other permutation-based methods and robust to misspecification of the model of sequence evolution. We apply the method to sequence data from viruses, bacteria, and human mitochondrial DNA. The extremely high level of recombination detected in both HIV1 and HIV2 sequences demonstrates that recombination cannot be ignored in the analysis of viral population genetic data.




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K. K. Shimizu, J. M. Cork, A. L. Caicedo, C. A. Mays, R. C. Moore, K. M. Olsen, S. Ruzsa, G. Coop, C. D. Bustamante, P. Awadalla, et al.
Darwinian Selection on a Selfing Locus
Science, December 17, 2004; 306(5704): 2081 - 2084.
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 Mol Biol EvolHome page
G. Piganeau, M. Gardner, and A. Eyre-Walker
A Broad Survey of Recombination in Animal Mitochondria
Mol. Biol. Evol., December 1, 2004; 21(12): 2319 - 2325.
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C. R. Linder and L. H. Rieseberg
Reconstructing patterns of reticulate evolution in plants.
Am. J. Botany, October 1, 2004; 91: 1700 - 1708.
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S. R. Bordenstein and J. J. Wernegreen
Bacteriophage Flux in Endosymbionts (Wolbachia): Infection Frequency, Lateral Transfer, and Recombination Rates
Mol. Biol. Evol., October 1, 2004; 21(10): 1981 - 1991.
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D. Shriner, A. G. Rodrigo, D. C. Nickle, and J. I. Mullins
Pervasive Genomic Recombination of HIV-1 in Vivo
Genetics, August 1, 2004; 167(4): 1573 - 1583.
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P. Fearnhead, R. M. Harding, J. A. Schneider, S. Myers, and P. Donnelly
Application of Coalescent Methods to Reveal Fine-Scale Rate Variation and Recombination Hotspots
Genetics, August 1, 2004; 167(4): 2067 - 2081.
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J. M. Burrows, L. Bromham, M. Woolfit, G. Piganeau, J. Tellam, G. Connolly, N. Webb, L. Poulsen, L. Cooper, S. R. Burrows, et al.
Selection Pressure-Driven Evolution of the Epstein-Barr Virus-Encoded Oncogene LMP1 in Virus Isolates from Southeast Asia
J. Virol., July 1, 2004; 78(13): 7131 - 7137.
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P. Lemey, O. G. Pybus, A. Rambaut, A. J. Drummond, D. L. Robertson, P. Roques, M. Worobey, and A.-M. Vandamme
The Molecular Population Genetics of HIV-1 Group O
Genetics, July 1, 2004; 167(3): 1059 - 1068.
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J. D. Wall
Estimating Recombination Rates Using Three-Site Likelihoods
Genetics, July 1, 2004; 167(3): 1461 - 1473.
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D. T. Haydon, A. D. S. Bastos, and P. Awadalla
Low linkage disequilibrium indicative of recombination in foot-and-mouth disease virus gene sequence alignments
J. Gen. Virol., May 1, 2004; 85(5): 1095 - 1100.
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S. F. Sarkar and D. S. Guttman
Evolution of the Core Genome of Pseudomonas syringae, a Highly Clonal, Endemic Plant Pathogen
Appl. Envir. Microbiol., April 1, 2004; 70(4): 1999 - 2012.
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E. S. Balakirev and F. J. Ayala
Nucleotide Variation in the tinman and bagpipe Homeobox Genes of Drosophila melanogaster
Genetics, April 1, 2004; 166(4): 1845 - 1856.
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 Hum Mol GenetHome page
X. Ke, S. Hunt, W. Tapper, R. Lawrence, G. Stavrides, J. Ghori, P. Whittaker, A. Collins, A. P. Morris, D. Bentley, et al.
The impact of SNP density on fine-scale patterns of linkage disequilibrium
Hum. Mol. Genet., March 15, 2004; 13(6): 577 - 588.
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E. S. Balakirev and F. J. Ayala
Nucleotide Variation of the Est-6 Gene Region in Natural Populations of Drosophila melanogaster
Genetics, December 1, 2003; 165(4): 1901 - 1914.
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N. Li and M. Stephens
Modeling Linkage Disequilibrium and Identifying Recombination Hotspots Using Single-Nucleotide Polymorphism Data
Genetics, December 1, 2003; 165(4): 2213 - 2233.
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D. Charlesworth, C. Bartolome, M. H. Schierup, and B. K. Mable
Haplotype Structure of the Stigmatic Self-Incompatibility Gene in Natural Populations of Arabidopsis lyrata
Mol. Biol. Evol., November 1, 2003; 20(11): 1741 - 1753.
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S. D. Polley, W. Chokejindachai, and D. J. Conway
Allele Frequency-Based Analyses Robustly Map Sequence Sites Under Balancing Selection in a Malaria Vaccine Candidate Antigen
Genetics, October 1, 2003; 165(2): 555 - 561.
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D. Charlesworth, B. K. Mable, M. H. Schierup, C. Bartolome, and P. Awadalla
Diversity and Linkage of Genes in the Self-Incompatibility Gene Family in Arabidopsis lyrata
Genetics, August 1, 2003; 164(4): 1519 - 1535.
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M. Anisimova, R. Nielsen, and Z. Yang
Effect of Recombination on the Accuracy of the Likelihood Method for Detecting Positive Selection at Amino Acid Sites
Genetics, July 1, 2003; 164(3): 1229 - 1236.
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E. S. Balakirev, V. R. Chechetkin, V. V. Lobzin, and F. J. Ayala
DNA Polymorphism in the {beta}-Esterase Gene Cluster of Drosophila melanogaster
Genetics, June 1, 2003; 164(2): 533 - 544.
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