{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T12:33:58Z","timestamp":1781094838084,"version":"3.54.1"},"reference-count":57,"publisher":"Oxford University Press (OUP)","issue":"2","license":[{"start":{"date-parts":[[2017,2,1]],"date-time":"2017-02-01T00:00:00Z","timestamp":1485907200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2017,2,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Inferring the rate of homologous recombination within a bacterial population remains a key challenge in quantifying the basic parameters of bacterial evolution. Due to the high sequence similarity within a clonal population, and unique aspects of bacterial DNA transfer processes, detecting recombination events based on phylogenetic reconstruction is often difficult, and estimating recombination rates using coalescent model-based methods is computationally expensive, and often infeasible for large sequencing data sets. Here, we present an efficient solution by introducing a set of mutational correlation functions computed using pairwise sequence comparison, which characterize various facets of bacterial recombination. We provide analytical expressions for these functions, which precisely recapitulate simulation results of neutral and adapting populations under different coalescent models. We used these to fit correlation functions measured at synonymous substitutions using whole-genome data on Escherichia coli and Streptococcus pneumoniae populations. We calculated and corrected for the effect of sample selection bias, i.e., the uneven sampling of individuals from natural microbial populations that exists in most datasets. Our method is fast and efficient, and does not employ phylogenetic inference or other computationally intensive numerics. By simply fitting analytical forms to measurements from sequence data, we show that recombination rates can be inferred, and the relative ages of different samples can be estimated. Our approach, which is based on population genetic modeling, is broadly applicable to a wide variety of data, and its computational efficiency makes it particularly attractive for use in the analysis of large sequencing datasets.<\/jats:p>","DOI":"10.1534\/genetics.116.189621","type":"journal-article","created":{"date-parts":[[2016,12,23]],"date-time":"2016-12-23T04:13:20Z","timestamp":1482466400000},"page":"891-917","source":"Crossref","is-referenced-by-count":27,"title":["Correlated Mutations and Homologous Recombination Within Bacterial Populations"],"prefix":"10.1093","volume":"205","author":[{"given":"Mingzhi","family":"Lin","sequence":"first","affiliation":[{"name":"Department of Biology and Center for Genomics and Systems Biology , New York University, New York 10003"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edo","family":"Kussell","sequence":"additional","affiliation":[{"name":"Department of Biology and Center for Genomics and Systems Biology , New York University, New York 10003"},{"name":"Department of Physics , New York University, New York 10003"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2017,2,1]]},"reference":[{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1038\/nrmicro2593","article-title":"Biased gene transfer in microbial evolution.","volume":"9","author":"Andam","year":"2011","journal-title":"Nat. Rev. Microbiol."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1534\/genetics.113.157172","article-title":"Inference of the properties of the recombination process from whole bacterial genomes.","volume":"196","author":"Ansari","year":"2014","journal-title":"Genetics"},{"key":"2023030910480337100_","first-page":"e00347","article-title":"Sequential acquisition of virulence and fluoroquinolone resistance has shaped the evolution of Escherichia coli ST131.","volume":"7","author":"Ben Zakour","year":"2016","journal-title":"MBio"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1007\/s002200050450","article-title":"On Ruelle\u2019s probability cascades and an abstract cavity method.","volume":"197","author":"Bolthausen","year":"1998","journal-title":"Commun. Math. Phys."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"041104","DOI":"10.1103\/PhysRevE.76.041104","article-title":"Effect of selection on ancestry: an exactly soluble case and its phenomenological generalization.","volume":"76","author":"Brunet","year":"2007","journal-title":"Phys. Rev. E Stat. Nonlin. Soft Matter Phys."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"061102","DOI":"10.1103\/PhysRevE.78.061102","article-title":"Universal tree structures in directed polymers and models of evolving populations.","volume":"78","author":"Brunet","year":"2008","journal-title":"Phys. Rev. E Stat. Nonlin. Soft Matter Phys."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1038\/ng.2895","article-title":"Dense genomic sampling identifies highways of pneumococcal recombination.","volume":"46","author":"Chewapreecha","year":"2014","journal-title":"Nat. Genet."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"098102","DOI":"10.1103\/PhysRevLett.94.098102","article-title":"Recombination dramatically speeds up evolution of finite populations.","volume":"94","author":"Cohen","year":"2005","journal-title":"Phys. Rev. Lett."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1126\/science.1198545","article-title":"Rapid pneumococcal evolution in response to clinical interventions.","volume":"331","author":"Croucher","year":"2011","journal-title":"Science"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"e15","DOI":"10.1093\/nar\/gku1196","article-title":"Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins.","volume":"43","author":"Croucher","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1534\/genetics.112.147157","article-title":"Genetic diversity and the structure of genealogies in rapidly adapting populations.","volume":"193","author":"Desai","year":"2013","journal-title":"Genetics"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1251","DOI":"10.1534\/genetics.106.063305","article-title":"Inference of bacterial microevolution using multilocus sequence data.","volume":"175","author":"Didelot","year":"2007","journal-title":"Genetics"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1435","DOI":"10.1534\/genetics.110.120121","article-title":"Inference of homologous recombination in bacteria using whole-genome sequences.","volume":"186","author":"Didelot","year":"2010","journal-title":"Genetics"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1186\/1471-2164-13-256","article-title":"Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli.","volume":"13","author":"Didelot","year":"2012","journal-title":"BMC Genomics"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"9070","DOI":"10.1073\/pnas.1510839112","article-title":"Recombinant transfer in the basic genome of Escherichia coli.","volume":"112","author":"Dixit","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1241","DOI":"10.2140\/pjm.1962.12.1241","article-title":"Block diagonally dominant matrices and generalizations of the Gerschgorin circle theorem.","volume":"12","author":"Feingold","year":"1962","journal-title":"Pac. J. Math."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"476","DOI":"10.1126\/science.1127573","article-title":"Recombination and the nature of bacterial speciation.","volume":"315","author":"Fraser","year":"2007","journal-title":"Science"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1126\/science.1159388","article-title":"The bacterial species challenge: making sense of genetic and ecological diversity.","volume":"323","author":"Fraser","year":"2009","journal-title":"Science"},{"key":"2023030910480337100_","unstructured":"Garrison, E., and G. Marth, 2012\u2003Haplotype-based variant detection from short-read sequencing. arXiv: 1207.3907 [q-bio.GN]."},{"key":"2023030910480337100_","first-page":"2039","article-title":"Modelling bacterial speciation.","volume-title":"Philos. Trans. R. Soc. Lond. B. Biol. Sci.","author":"Hanage","year":"2006"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1007\/BF00171824","article-title":"Genetic distance and species formation in evolving populations.","volume":"35","author":"Higgs","year":"1992","journal-title":"J. Mol. Evol."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/0040-5809(83)90013-8","article-title":"Properties of a neutral allele model with intragenic recombination.","volume":"23","author":"Hudson","year":"1983","journal-title":"Theor. Popul. Biol."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"27","DOI":"10.2307\/3213548","article-title":"On the genealogy of large populations.","volume":"19","author":"Kingman","year":"1982","journal-title":"J. Appl. Probab."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"6688","DOI":"10.1093\/nar\/gkn668","article-title":"Genomics of bacteria and archaea: the emerging dynamic view of the prokaryotic world.","volume":"36","author":"Koonin","year":"2008","journal-title":"Nucleic Acids Res."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1128\/MMBR.63.4.751-813.1999","article-title":"Recombinational repair of DNA damage in Escherichia coli and bacteriophage \u03bb.","volume":"63","author":"Kuzminov","year":"1999","journal-title":"Microbiol. Mol. Biol. Rev."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"E2774","DOI":"10.1073\/pnas.1210309109","article-title":"Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing.","volume":"109","author":"Lee","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The sequence alignment\/map format and SAMtools.","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1128\/mr.58.3.563-602.1994","article-title":"Bacterial gene transfer by natural genetic transformation in the environment.","volume":"58","author":"Lorenz","year":"1994","journal-title":"Microbiol. Rev."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"e6","DOI":"10.1093\/nar\/gkr928","article-title":"Detection of recombination events in bacterial genomes from large population samples.","volume":"40","author":"Marttinen","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1098\/rspb.1991.0085","article-title":"The population genetics of bacteria.","volume":"245","author":"Maynard Smith","year":"1991","journal-title":"Proc. Biol. Sci."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1093\/genetics\/160.3.1231","article-title":"A coalescent-based method for detecting and estimating recombination from gene sequences.","volume":"160","author":"McVean","year":"2002","journal-title":"Genetics"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1126\/science.1092500","article-title":"The fine-scale structure of recombination rate variation in the human genome.","volume":"304","author":"McVean","year":"2004","journal-title":"Science"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1017\/S0305004100033193","article-title":"Random processes in genetics.","volume":"54","author":"Moran","year":"1958","journal-title":"Math. Proc. Camb. Philos. Soc."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1073\/pnas.1213113110","article-title":"Genealogies of rapidly adapting populations.","volume":"110","author":"Neher","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1534\/genetics.109.109009","article-title":"Rate of adaptation in large sexual populations.","volume":"184","author":"Neher","year":"2010","journal-title":"Genetics"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"15836","DOI":"10.1073\/pnas.1309697110","article-title":"Coalescence and genetic diversity in sexual populations under selection.","volume":"110","author":"Neher","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"16112","DOI":"10.1073\/pnas.1413272111","article-title":"Transfer of noncoding DNA drives regulatory rewiring in bacteria.","volume":"111","author":"Oren","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"5694","DOI":"10.1073\/pnas.1322678111","article-title":"Global dissemination of a multidrug resistant Escherichia coli clone.","volume":"111","author":"Petty","year":"2014","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1870","DOI":"10.1214\/aop\/1022874819","article-title":"Coalescents with multiple collisions.","volume":"27","author":"Pitman","year":"1999","journal-title":"Ann. Probab."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"e00377","DOI":"10.1128\/mBio.00377-13","article-title":"The epidemic of extended-spectrum-\u03b2-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx.","volume":"4","author":"Price","year":"2013","journal-title":"MBio"},{"key":"2023030910480337100_","volume-title":"R: A Language and Environment for Statistical Computing","author":"R Core Team","year":"2016"},{"key":"2023030910480337100_","first-page":"243","article-title":"The inverses of block tridiagonal matrices.","volume":"179","author":"Ran","year":"2006","journal-title":"Appl. Math. Comput."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"e1004095","DOI":"10.1371\/journal.pcbi.1004095","article-title":"Inferring horizontal gene transfer.","volume":"11","author":"Ravenhall","year":"2015","journal-title":"PLoS Comput. Biol."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1126\/science.aaa4456","article-title":"Fine-scale diversity and extensive recombination in a quasisexual bacterial population occupying a broad niche.","volume":"348","author":"Rosen","year":"2015","journal-title":"Science"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1116","DOI":"10.1239\/jap\/1032374759","article-title":"The general coalescent with asynchronous mergers of ancestral lines.","volume":"36","author":"Sagitov","year":"1999","journal-title":"J. Appl. Probab."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1214\/EJP.v5-68","article-title":"Coalescents with simultaneous multiple collisions.","volume":"5","author":"Schweinsberg","year":"2000","journal-title":"Electron. J. Probab."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1214\/EJP.v17-2378","article-title":"Dynamics of the evolving Bolthausen\u2013Sznitman coalecent.","volume":"17","author":"Schweinsberg","year":"2012","journal-title":"Electron. J. Probab."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1126\/science.1218198","article-title":"Population genomics of early events in the ecological differentiation of bacteria.","volume":"336","author":"Shapiro","year":"2012","journal-title":"Science"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"472","DOI":"10.1038\/nrg3962","article-title":"Horizontal gene transfer: building the web of life.","volume":"16","author":"Soucy","year":"2015","journal-title":"Nat. Rev. Genet."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1038\/nrmicro1234","article-title":"Mechanisms of, and barriers to, horizontal gene transfer between bacteria.","volume":"3","author":"Thomas","year":"2005","journal-title":"Nat. Rev. Microbiol."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"e1000344","DOI":"10.1371\/journal.pgen.1000344","article-title":"Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths.","volume":"5","author":"Touchon","year":"2009","journal-title":"PLoS Genet."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1038\/ismej.2008.93","article-title":"A comparison of homologous recombination rates in bacteria and archaea.","volume":"3","author":"Vos","year":"2009","journal-title":"ISME J."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"e1002740","DOI":"10.1371\/journal.pgen.1002740","article-title":"Limits to the rate of adaptive substitutions in sexual populations.","volume":"8","author":"Weissman","year":"2012","journal-title":"PLoS Genet."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1534\/genetics.113.160705","article-title":"The rate of adaptation in large sexual populations with linear chromosomes.","volume":"196","author":"Weissman","year":"2014","journal-title":"Genetics"},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1093\/gbe\/evs098","article-title":"Quantifying homologous replacement of loci between haloarchaeal species.","volume":"4","author":"Williams","year":"2012","journal-title":"Genome Biol. Evol."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1006\/tpbi.2000.1462","article-title":"A coalescence approach to gene conversion.","volume":"57","author":"Wiuf","year":"2000","journal-title":"Theor. Popul. Biol."},{"key":"2023030910480337100_","doi-asserted-by":"crossref","first-page":"451","DOI":"10.1093\/genetics\/155.1.451","article-title":"The coalescent with gene conversion.","volume":"155","author":"Wiuf","year":"2000","journal-title":"Genetics"}],"container-title":["Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/205\/2\/891\/49468685\/genetics0891.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/205\/2\/891\/49468685\/genetics0891.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,6,21]],"date-time":"2024-06-21T11:04:59Z","timestamp":1718967899000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/genetics\/article\/205\/2\/891\/6066449"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,2,1]]},"references-count":57,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2017,2,1]]},"published-print":{"date-parts":[[2017,2,1]]}},"URL":"https:\/\/doi.org\/10.1534\/genetics.116.189621","relation":{},"ISSN":["1943-2631"],"issn-type":[{"value":"1943-2631","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2017,2,1]]},"published":{"date-parts":[[2017,2,1]]}}}