{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,24]],"date-time":"2026-04-24T19:53:37Z","timestamp":1777060417355,"version":"3.51.4"},"reference-count":53,"publisher":"Springer Science and Business Media LLC","issue":"4","license":[{"start":{"date-parts":[[2002,4,1]],"date-time":"2002-04-01T00:00:00Z","timestamp":1017619200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Nat Rev Genet"],"published-print":{"date-parts":[[2002,4]]},"DOI":"10.1038\/nrg761","type":"journal-article","created":{"date-parts":[[2002,7,26]],"date-time":"2002-07-26T08:56:51Z","timestamp":1027673811000},"page":"252-261","source":"Crossref","is-referenced-by-count":694,"title":["Resolving the paradox of sex and recombination"],"prefix":"10.1038","volume":"3","author":[{"given":"Sarah P.","family":"Otto","sequence":"first","affiliation":[]},{"given":"Thomas","family":"Lenormand","sequence":"additional","affiliation":[]}],"member":"297","reference":[{"key":"BFnrg761_CR1","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1038\/373241a0","volume":"373","author":"T Chapman","year":"1995","unstructured":"Chapman, T., Liddle, L. F., Kalb, J. M., Wolfner, M. F. & Partridge, L. Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products. Nature 373, 241\u2013244 (1995).","journal-title":"Nature"},{"key":"BFnrg761_CR2","doi-asserted-by":"publisher","first-page":"634","DOI":"10.1038\/35084593","volume":"2","author":"RJ Redfield","year":"2001","unstructured":"Redfield, R. J. Do bacteria have sex? Nature Rev. Genet. 2, 634\u2013639 (2001).","journal-title":"Nature Rev. Genet."},{"key":"BFnrg761_CR3","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1016\/S0966-842X(01)02079-0","volume":"9","author":"S Karlin","year":"2001","unstructured":"Karlin, S. Detecting anomalous gene clusters and pathogenicity islands in diverse bacterial genomes. Trends Microbiol. 9, 335\u2013343 (2001).","journal-title":"Trends Microbiol."},{"key":"BFnrg761_CR4","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1146\/annurev.ge.27.120193.001315","volume":"27","author":"MG Kidwell","year":"1993","unstructured":"Kidwell, M. G. Lateral transfer in natural populations of eukaryotes. Annu. Rev. Genet. 27, 235\u2013256 (1993).","journal-title":"Annu. Rev. Genet."},{"key":"BFnrg761_CR5","doi-asserted-by":"publisher","first-page":"1769","DOI":"10.1093\/oxfordjournals.molbev.a026275","volume":"17","author":"AP de Koning","year":"2000","unstructured":"de Koning, A. P., Brinkman, F. S., Jones, S. J. & Keeling, P. J. Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis. Mol. Biol. Evol. 17, 1769\u20131773 (2000).","journal-title":"Mol. Biol. Evol."},{"key":"BFnrg761_CR6","doi-asserted-by":"publisher","first-page":"research0013.1","DOI":"10.1186\/gb-2000-1-6-research0013","volume":"1","author":"YI Wolf","year":"2000","unstructured":"Wolf, Y. I., Kondrashov, A. S. & Koonin, E. V. Interkingdom gene fusions. Genome Biol. 1, research0013.1\u20130013.13 (2000).","journal-title":"Genome Biol."},{"key":"BFnrg761_CR7","volume-title":"The Masterpiece of Nature: The Evolution and Genetics of Sexuality","author":"G Bell","year":"1982","unstructured":"Bell, G. The Masterpiece of Nature: The Evolution and Genetics of Sexuality (Univ. California Press, Berkeley, 1982).A classic text that explores the vast array of ways in which organisms reproduce and the reasons for this diversity."},{"key":"BFnrg761_CR8","first-page":"19","volume-title":"Evolution and Cytology of Unisexual Vertebrates","author":"R Vrijenhoek","year":"1989","unstructured":"Vrijenhoek, R., Dawley, R., Cole, C. & Bogart, J. in Evolution and Cytology of Unisexual Vertebrates (eds Dawley, R. & Bogart, J.) 19\u201323 (Univ. State New York, New York, 1989)."},{"key":"BFnrg761_CR9","volume-title":"The Diversity of Life","author":"EO Wilson","year":"1992","unstructured":"Wilson, E. O. The Diversity of Life (W. W. Norton, New York, 1992)."},{"key":"BFnrg761_CR10","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/0169-5347(96)81040-8","volume":"11","author":"OP Judson","year":"1996","unstructured":"Judson, O. P. & Normark, B. B. Ancient asexual scandals. Trends Ecol. Evol. 11, 41\u201346 (1996).","journal-title":"Trends Ecol. Evol."},{"key":"BFnrg761_CR11","doi-asserted-by":"publisher","first-page":"1211","DOI":"10.1126\/science.288.5469.1211","volume":"288","author":"D Mark Welch","year":"2000","unstructured":"Mark Welch, D. & Meselson, M. Evidence for the evolution of bdelloid rotifers without sexual reproduction or genetic exchange. Science 288, 1211\u20131215 (2000).","journal-title":"Science"},{"key":"BFnrg761_CR12","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1016\/S0020-7519(97)00181-1","volume":"28","author":"ML Sogin","year":"1998","unstructured":"Sogin, M. L. & Silberman, J. D. Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int. J. Parasitol. 28, 11\u201320 (1998).","journal-title":"Int. J. Parasitol."},{"key":"BFnrg761_CR13","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1111\/j.1550-7408.2000.tb00028.x","volume":"47","author":"L Morin","year":"2000","unstructured":"Morin, L. Long branch attraction effects and the status of 'basal eukaryotes': phylogeny and structural analysis of the ribosomal RNA gene cluster of the free-living diplomonad Trepomonas agilis. J. Eukaryot. Microbiol. 47, 167\u2013177 (2000).","journal-title":"J. Eukaryot. Microbiol."},{"key":"BFnrg761_CR14","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1016\/0169-5347(92)90205-P","volume":"7","author":"LD Hurst","year":"1992","unstructured":"Hurst, L. D., Hamilton, W. D. & Ladle, R. J. Covert sex. Trends Ecol. Evol. 7, 144\u2013145 (1992).","journal-title":"Trends Ecol. Evol."},{"key":"BFnrg761_CR15","doi-asserted-by":"publisher","first-page":"770","DOI":"10.1073\/pnas.93.2.770","volume":"93","author":"A Burt","year":"1996","unstructured":"Burt, A., Carter, D. A., Koenig, G. L., White, T. J. & Taylor, J. W. Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis. Proc. Natl Acad. Sci. USA 93, 770\u2013773 (1996).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnrg761_CR16","volume-title":"The Evolution of Sex","author":"RE Michod","year":"1988","unstructured":"Michod, R. E. & Levin, B. R. The Evolution of Sex (Sinauer Press, Sunderland, Massachusetts, 1988).An excellent review and source book for theoretical and empirical studies of the evolution of sex, with chapters written by authors from a variety of perspectives."},{"key":"BFnrg761_CR17","doi-asserted-by":"publisher","first-page":"372","DOI":"10.1093\/oxfordjournals.jhered.a111358","volume":"84","author":"AS Kondrashov","year":"1993","unstructured":"Kondrashov, A. S. Classification of hypotheses on the advantage of amphimixis. J. Hered. 84, 372\u2013387 (1993).","journal-title":"J. Hered."},{"key":"BFnrg761_CR18","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1146\/annurev.genet.30.1.261","volume":"30","author":"MW Feldman","year":"1997","unstructured":"Feldman, M. W., Otto, S. P. & Christiansen, F. B. Population genetic perspectives on the evolution of recombination. Annu. Rev. Genet. 30, 261\u2013295 (1997).","journal-title":"Annu. Rev. Genet."},{"key":"BFnrg761_CR19","doi-asserted-by":"crossref","first-page":"519","DOI":"10.1093\/genetics\/101.3-4.519","volume":"101","author":"DA Hickey","year":"1982","unstructured":"Hickey, D. A. Selfish DNA: a sexually-transmitted nuclear parasite. Genetics 101, 519\u2013531 (1982).","journal-title":"Genetics"},{"key":"BFnrg761_CR20","doi-asserted-by":"publisher","first-page":"605","DOI":"10.1016\/S1097-2765(00)00059-9","volume":"6","author":"V Reinke","year":"2000","unstructured":"Reinke, V. et al. A global profile of germline gene expression in C. elegans. Mol. Cell 6, 605\u2013616 (2000).","journal-title":"Mol. Cell"},{"key":"BFnrg761_CR21","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1086\/283734","volume":"117","author":"H Bernstein","year":"1981","unstructured":"Bernstein, H., Byers, G. S. & Michod, R. E. Evolution of sexual reproduction: importance of DNA repair, complementation, and variation. Am. Nat. 117, 537\u2013549 (1981).","journal-title":"Am. Nat."},{"key":"BFnrg761_CR22","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1093\/genetics\/133.4.755","volume":"133","author":"RJ Redfield","year":"1993","unstructured":"Redfield, R. J. Evolution of natural transformation: testing the DNA repair hypothesis in Bacillus subtilis and Haemophilus influenzae. Genetics 133, 755\u2013761 (1993).","journal-title":"Genetics"},{"key":"BFnrg761_CR23","doi-asserted-by":"publisher","first-page":"460","DOI":"10.1038\/268460a0","volume":"268","author":"P Thuriaux","year":"1977","unstructured":"Thuriaux, P. Is recombination confined to structural genes on the eukaryotic genome? Nature 268, 460\u2013462 (1977).","journal-title":"Nature"},{"key":"BFnrg761_CR24","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1146\/annurev.ge.10.120176.000413","volume":"10","author":"BS Baker","year":"1976","unstructured":"Baker, B. S., Carpenter, A. T. C., Esposito, M. S., Esposito, R. E. & Sandler, L. The genetic control of meiosis. Annu. Rev. Genet. 10, 53\u2013134 (1976).","journal-title":"Annu. Rev. Genet."},{"key":"BFnrg761_CR25","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1016\/0168-9525(93)90249-H","volume":"9","author":"RS Hawley","year":"1993","unstructured":"Hawley, R. S. & Theurkauf, W. E. Requiem for distributive segregation: achiasmate segregation in Drosophila females. Trends Genet. 9, 310\u2013317 (1993).","journal-title":"Trends Genet."},{"key":"BFnrg761_CR26","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1093\/genetics\/49.1.109","volume":"49","author":"JR Merriam","year":"1964","unstructured":"Merriam, J. R. & Frost, J. N. Exchange and nondisjunction of the X chromosomes in female Drosophila melanogaster. Genetics 49, 109\u2013122 (1964).","journal-title":"Genetics"},{"key":"BFnrg761_CR27","doi-asserted-by":"crossref","first-page":"887","DOI":"10.1093\/genetics\/136.3.887","volume":"136","author":"AM Villeneuve","year":"1994","unstructured":"Villeneuve, A. M. A cis-acting locus that promotes crossing over between X chromosomes in Caenorhabditis elegans. Genetics 136, 887\u2013902 (1994).","journal-title":"Genetics"},{"key":"BFnrg761_CR28","doi-asserted-by":"publisher","first-page":"1495","DOI":"10.1093\/hmg\/5.Supplement_1.1495","volume":"5","author":"KE Koehler","year":"1996","unstructured":"Koehler, K. E., Hawley, R. S., Sherman, S. & Hassold, T. Recombination and nondisjunction in humans and flies. Hum. Mol. Genet. 5, 1495\u20131504 (1996).","journal-title":"Hum. Mol. Genet."},{"key":"BFnrg761_CR29","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1046\/j.1420-9101.1991.4020259.x","volume":"4","author":"A Burt","year":"1991","unstructured":"Burt, A., Bell, G. & Harvey, P. H. Sex differences in recombination. J. Evol. Biol. 4, 259\u2013277 (1991).","journal-title":"J. Evol. Biol."},{"key":"BFnrg761_CR30","doi-asserted-by":"publisher","first-page":"1921","DOI":"10.1111\/j.0014-3820.2001.tb01310.x","volume":"55","author":"SP Otto","year":"2001","unstructured":"Otto, S. P. & Barton, N. H. Selection for recombination in small populations. Evolution 55, 1921\u20131931 (2001).An investigation of the relative importance of drift and epistasis to the evolution of sex and recombination with the use of a modifier model with directional selection.","journal-title":"Evolution"},{"key":"BFnrg761_CR31","doi-asserted-by":"publisher","first-page":"241","DOI":"10.1038\/nrg760","volume":"3","author":"WR Rice","year":"2002","unstructured":"Rice, W. R. Experimental tests of the adaptive significance of sexual reproduction. Nature Rev. Genet. 3, 241\u2013251 (2002).","journal-title":"Nature Rev. Genet."},{"key":"BFnrg761_CR32","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1093\/genetics\/117.3.559","volume":"117","author":"L Altenberg","year":"1987","unstructured":"Altenberg, L. & Feldman, M. W. Selection, generalized transmission and the evolution of modifier genes. I. The reduction principle. Genetics 117, 559\u2013572 (1987).","journal-title":"Genetics"},{"key":"BFnrg761_CR33","first-page":"430","volume":"21","author":"MW Feldman","year":"1972","unstructured":"Feldman, M. W. Selection for linkage modification. I. Random mating populations. Theor. Popul. Biol. 21, 430\u2013439 (1972).","journal-title":"Theor. Popul. Biol."},{"key":"BFnrg761_CR34","doi-asserted-by":"publisher","first-page":"4838","DOI":"10.1073\/pnas.77.8.4838","volume":"77","author":"MW Feldman","year":"1980","unstructured":"Feldman, M. W., Christiansen, F. B. & Brooks, L. D. Evolution of recombination in a constant environment. Proc. Natl Acad. Sci. USA 77, 4838\u20134841 (1980).The first theoretical analysis to show that higher rates of recombination could evolve when deleterious mutations exhibit negative fitness interactions.","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFnrg761_CR35","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1017\/S0016672300026392","volume":"44","author":"AS Kondrashov","year":"1984","unstructured":"Kondrashov, A. S. Deleterious mutations as an evolutionary factor. I. The advantage of recombination. Genet. Res. 44, 199\u2013217 (1984).","journal-title":"Genet. Res."},{"key":"BFnrg761_CR36","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1017\/S0016672300025532","volume":"55","author":"B Charlesworth","year":"1990","unstructured":"Charlesworth, B. Mutation\u2013selection balance and the evolutionary advantage of sex and recombination. Genet. Res. 55, 199\u2013221 (1990).","journal-title":"Genet. Res."},{"key":"BFnrg761_CR37","doi-asserted-by":"publisher","first-page":"123","DOI":"10.1017\/S0016672300033140","volume":"65","author":"NH Barton","year":"1995","unstructured":"Barton, N. H. A general model for the evolution of recombination. Genet. Res. 65, 123\u2013144 (1995).A ground-breaking theoretical study that generalized models of the evolution of recombination to a genome-wide level and to include several forms of selection.","journal-title":"Genet. Res."},{"key":"BFnrg761_CR38","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1006\/tpbi.1997.1301","volume":"51","author":"SP Otto","year":"1997","unstructured":"Otto, S. P. & Feldman, M. W. Deleterious mutations, variable epistatic interactions, and the evolution of recombination. Theor. Popul. Biol. 51, 134\u2013147 (1997).","journal-title":"Theor. Popul. Biol."},{"key":"BFnrg761_CR39","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1016\/0040-5809(70)90043-2","volume":"1","author":"I Eshel","year":"1970","unstructured":"Eshel, I. & Feldman, M. W. On the evolutionary effect of recombination. Theor. Popul. Biol. 1, 88\u2013100 (1970).","journal-title":"Theor. Popul. Biol."},{"key":"BFnrg761_CR40","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1093\/genetics\/156.3.1419","volume":"156","author":"JR Chasnov","year":"2000","unstructured":"Chasnov, J. R. Mutation\u2013selection balance, dominance and the maintenance of sex. Genetics 156, 1419\u20131425 (2000).","journal-title":"Genetics"},{"key":"BFnrg761_CR41","doi-asserted-by":"crossref","first-page":"913","DOI":"10.1093\/genetics\/158.2.913","volume":"158","author":"AF Agrawal","year":"2001","unstructured":"Agrawal, A. F. & Chasnov, J. R. Recessive mutations and the maintenance of sex in structured populations. Genetics 158, 913\u2013917 (2001).","journal-title":"Genetics"},{"key":"BFnrg761_CR42","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1146\/annurev.ge.11.120177.000405","volume":"11","author":"MJ Simmons","year":"1977","unstructured":"Simmons, M. J. & Crow, J. F. Mutations affecting fitness in Drosophila populations. Annu. Rev. Genet. 11, 49\u201378 (1977).","journal-title":"Annu. Rev. Genet."},{"key":"BFnrg761_CR43","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1086\/303247","volume":"154","author":"AD Peters","year":"1999","unstructured":"Peters, A. D. & Lively, C. M. The Red Queen and fluctuating epistasis: a population genetic analysis of antagonistic coevolution. Am. Nat. 154, 393\u2013405 (1999).","journal-title":"Am. Nat."},{"key":"BFnrg761_CR44","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1093\/genetics\/156.1.423","volume":"156","author":"T Lenormand","year":"2000","unstructured":"Lenormand, T. & Otto, S. P. The evolution of recombination in a heterogeneous environment. Genetics 156, 423\u2013438 (2000).","journal-title":"Genetics"},{"key":"BFnrg761_CR45","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1017\/S0016672398003243","volume":"71","author":"KV Pylkov","year":"1998","unstructured":"Pylkov, K. V., Zhivotovsky, L. A. & Feldman, M. W. Migration versus mutation in the evolution of recombination under multilocus selection. Genet. Res. 71, 247\u2013256 (1998).","journal-title":"Genet. Res."},{"key":"BFnrg761_CR46","doi-asserted-by":"publisher","first-page":"269","DOI":"10.1017\/S0016672300010156","volume":"8","author":"WG Hill","year":"1966","unstructured":"Hill, W. G. & Robertson, A. The effect of linkage on the limits to artificial selection. Genet. Res. 8, 269\u2013294 (1966).This paper showed that, in finite populations, selection at a locus is less efficient when neighboring loci are also under selection because of increased variation in the reproductive success of an allele (that is, increased random genetic drift).","journal-title":"Genet. Res."},{"key":"BFnrg761_CR47","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1093\/genetics\/147.2.879","volume":"147","author":"SP Otto","year":"1997","unstructured":"Otto, S. P. & Barton, N. H. The evolution of recombination: removing the limits to natural selection. Genetics 147, 879\u2013906 (1997).","journal-title":"Genetics"},{"key":"BFnrg761_CR48","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1017\/S001667239800367X","volume":"73","author":"DD Gessler","year":"1999","unstructured":"Gessler, D. D. & Xu, S. On the evolution of recombination and meiosis. Genet. Res. 73, 119\u2013131 (1999).","journal-title":"Genet. Res."},{"key":"BFnrg761_CR49","doi-asserted-by":"crossref","first-page":"597","DOI":"10.1093\/genetics\/137.2.597","volume":"137","author":"JR Peck","year":"1994","unstructured":"Peck, J. R. A ruby in the rubbish: beneficial mutations, deleterious mutations and the evolution of sex. Genetics 137, 597\u2013606 (1994).","journal-title":"Genetics"},{"key":"BFnrg761_CR50","volume-title":"\u00c9volution de la Recombinaison en Populations Subdivis\u00e9es: \u00c9tude par Simulation de l'Influence de la Structure sur la S\u00e9lection pour la Recombinaison via l'Effet Hill\u2013Robertson","author":"G Martin","year":"2001","unstructured":"Martin, G. \u00c9volution de la Recombinaison en Populations Subdivis\u00e9es: \u00c9tude par Simulation de l'Influence de la Structure sur la S\u00e9lection pour la Recombinaison via l'Effet Hill\u2013Robertson (DEA, Biologi\u00e9, Universit\u00e9 Montpellier II, Montpellier, 2001)."},{"key":"BFnrg761_CR51","volume-title":"The History of Sexuality. I. An Introduction","author":"M Foucault","year":"1978","unstructured":"Foucault, M. The History of Sexuality. I. An Introduction (Vintage Books, New York, 1978)."},{"key":"BFnrg761_CR52","doi-asserted-by":"publisher","first-page":"604","DOI":"10.1111\/j.1558-5646.1998.tb01658.x","volume":"52","author":"RS Howard","year":"1998","unstructured":"Howard, R. S. & Lively, C. M. The maintenance of sex by parasitism and mutation accumulation under epistatic fitness functions. Evolution 52, 604\u2013610 (1998).","journal-title":"Evolution"},{"key":"BFnrg761_CR53","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1093\/genetics\/57.3.625","volume":"57","author":"M Nei","year":"1967","unstructured":"Nei, M. Modification of linkage intensity by natural selection. Genetics 57, 625\u2013641 (1967).","journal-title":"Genetics"}],"container-title":["Nature Reviews Genetics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/www.nature.com\/articles\/nrg761.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nrg761","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/www.nature.com\/articles\/nrg761.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,5,19]],"date-time":"2023-05-19T03:36:04Z","timestamp":1684467364000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/nrg761"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2002,4]]},"references-count":53,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2002,4]]}},"alternative-id":["BFnrg761"],"URL":"https:\/\/doi.org\/10.1038\/nrg761","relation":{},"ISSN":["1471-0056","1471-0064"],"issn-type":[{"value":"1471-0056","type":"print"},{"value":"1471-0064","type":"electronic"}],"subject":[],"published":{"date-parts":[[2002,4]]}}}