{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,9]],"date-time":"2026-03-09T21:24:39Z","timestamp":1773091479761,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pgen.1008959","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2020,11,24]],"date-time":"2020-11-24T00:00:00Z","timestamp":1606176000000}}],"reference-count":111,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2020,11,12]],"date-time":"2020-11-12T00:00:00Z","timestamp":1605139200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003329","name":"Ministerio de Econom\u00eda y Competitividad","doi-asserted-by":"publisher","award":["CGL2014-53106-P"],"award-info":[{"award-number":["CGL2014-53106-P"]}],"id":[{"id":"10.13039\/501100003329","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["SEXYMUS 10-JCJC-1605"],"award-info":[{"award-number":["SEXYMUS 10-JCJC-1605"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["ANR-16-IDEX-0006"],"award-info":[{"award-number":["ANR-16-IDEX-0006"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009515","name":"Fondation Simone et Cino Del Duca","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100009515","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001711","name":"Schweizerischer Nationalfonds zur F\u00f6rderung der Wissenschaftlichen Forschung","doi-asserted-by":"publisher","award":["31003A 166323"],"award-info":[{"award-number":["31003A 166323"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004895","name":"European Social Fund","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100004895","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001665","name":"Agence Nationale de la Recherche","doi-asserted-by":"publisher","award":["18-CE02-0018-01"],"award-info":[{"award-number":["18-CE02-0018-01"]}],"id":[{"id":"10.13039\/501100001665","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"abstract":"<jats:p>\n                    Sex chromosomes of eutherian mammals are highly different in size and gene content, and share only a small region of homology (pseudoautosomal region, PAR). They are thought to have evolved through an addition-attrition cycle involving the addition of autosomal segments to sex chromosomes and their subsequent differentiation. The events that drive this process are difficult to investigate because sex chromosomes in almost all mammals are at a very advanced stage of differentiation. Here, we have taken advantage of a recent translocation of an autosome to both sex chromosomes in the African pygmy mouse\n                    <jats:italic>Mus minutoides<\/jats:italic>\n                    , which has restored a large segment of homology (neo-PAR). By studying meiotic sex chromosome behavior and identifying fully sex-linked genetic markers in the neo-PAR, we demonstrate that this region shows unequivocal signs of early sex-differentiation. First, synapsis and resolution of DNA damage intermediates are delayed in the neo-PAR during meiosis. Second, recombination is suppressed or largely reduced in a large portion of the neo-PAR. However, the inactivation process that characterizes sex chromosomes during meiosis does not extend to this region. Finally, the sex chromosomes show a dual mechanism of association at metaphase-I that involves the formation of a chiasma in the neo-PAR and the preservation of an ancestral achiasmate mode of association in the non-homologous segments. We show that the study of meiosis is crucial to apprehend the onset of sex chromosome differentiation, as it introduces structural and functional constrains to sex chromosome evolution. Synapsis and DNA repair dynamics are the first processes affected in the incipient differentiation of X and Y chromosomes, and they may be involved in accelerating their evolution. This provides one of the very first reports of early steps in neo-sex chromosome differentiation in mammals, and for the first time a cellular framework for the addition-attrition model of sex chromosome evolution.\n                  <\/jats:p>","DOI":"10.1371\/journal.pgen.1008959","type":"journal-article","created":{"date-parts":[[2020,11,12]],"date-time":"2020-11-12T13:52:40Z","timestamp":1605189160000},"page":"e1008959","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":18,"title":["Meiosis reveals the early steps in the evolution of a neo-XY sex chromosome pair in the African pygmy mouse Mus minutoides"],"prefix":"10.1371","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9707-1635","authenticated-orcid":true,"given":"Ana","family":"Gil-Fern\u00e1ndez","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6282-0472","authenticated-orcid":true,"given":"Paul A.","family":"Saunders","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0711-8979","authenticated-orcid":true,"given":"Marta","family":"Mart\u00edn-Ruiz","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9394-5625","authenticated-orcid":true,"given":"Marta","family":"Ribagorda","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6673-5996","authenticated-orcid":true,"given":"Pablo","family":"L\u00f3pez-Jim\u00e9nez","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daniel L.","family":"Jeffries","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1158-6903","authenticated-orcid":true,"given":"Mar\u00eda Teresa","family":"Parra","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3602-4130","authenticated-orcid":true,"given":"Alberto","family":"Viera","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7516-809X","authenticated-orcid":true,"given":"Julio S.","family":"Rufas","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7756-6323","authenticated-orcid":true,"given":"Nicolas","family":"Perrin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Frederic","family":"Veyrunes","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8381-324X","authenticated-orcid":true,"given":"Jes\u00fas","family":"Page","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2020,11,12]]},"reference":[{"key":"pgen.1008959.ref001","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-642-88178-7","volume-title":"Sex chromosomes and sex linked genes","author":"S. Ohno","year":"1967"},{"issue":"2","key":"pgen.1008959.ref002","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1038\/nrg3366","article-title":"Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration","volume":"14","author":"D. Bachtrog","year":"2013","journal-title":"Nat Rev Genet"},{"issue":"2","key":"pgen.1008959.ref003","doi-asserted-by":"crossref","first-page":"118","DOI":"10.1038\/sj.hdy.6800697","article-title":"Steps in the evolution of heteromorphic sex chromosomes","volume":"95","author":"D Charlesworth","year":"2005","journal-title":"Heredity"},{"issue":"5","key":"pgen.1008959.ref004","doi-asserted-by":"crossref","first-page":"331","DOI":"10.2307\/1312947","article-title":"Evolution of the Y Sex Chromosome in Animals: Y chromosomes evolve through the degeneration of autosomes","volume":"46","author":"WR Rice","year":"1996","journal-title":"BioScience"},{"issue":"6","key":"pgen.1008959.ref005","doi-asserted-by":"crossref","first-page":"578","DOI":"10.1016\/j.gde.2006.10.007","article-title":"A dynamic view of sex chromosome evolution","volume":"16","author":"D. 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Achiasmatic sex chromosomes in Pitymys duodecimcostatus: mechanisms of association and segregation","volume":"56","author":"A Carnero","year":"1991","journal-title":"Cytogenet Cell Genet"},{"issue":"5","key":"pgen.1008959.ref015","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1007\/s00412-012-0374-9","article-title":"A synaptonemal complex-derived mechanism for meiotic segregation precedes the evolutionary loss of homology between sex chromosomes in arvicolid mammals","volume":"121","author":"R de la Fuente","year":"2012","journal-title":"Chromosoma"},{"key":"pgen.1008959.ref016","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/j.actao.2012.01.001","article-title":"Systematics and evolution of the African pygmy mice, subgenus Nannomys: A review","volume":"42","author":"J Britton-Davidian","year":"2012","journal-title":"Acta 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Rahn","year":"2016","journal-title":"Chromosoma"},{"issue":"3","key":"pgen.1008959.ref020","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1007\/s10577-016-9524-x","article-title":"Meiotic behaviour of evolutionary sex-autosome translocations in Bovidae","volume":"24","author":"M Vozdova","year":"2016","journal-title":"Chromosome Res"},{"issue":"1\u20133","key":"pgen.1008959.ref021","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1159\/000080825","article-title":"Fine structure and meiotic behaviour of the male multiple sex chromosomes in the genus Alouatta","volume":"108","author":"AJ Solari","year":"2005","journal-title":"Cytogenetic and Genome Research"},{"issue":"1","key":"pgen.1008959.ref022","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/s10577-011-9268-6","article-title":"The Y chromosome of the Okinawa spiny rat, Tokudaia muenninki, was rescued through fusion with an autosome","volume":"20","author":"C Murata","year":"2012","journal-title":"Chromosome Res"},{"issue":"5","key":"pgen.1008959.ref023","doi-asserted-by":"crossref","first-page":"901","DOI":"10.1016\/j.cell.2006.02.024","article-title":"Sex Chromosome Specialization and Degeneration in Mammals","volume":"124","author":"JAM Graves","year":"2006","journal-title":"Cell"},{"issue":"1","key":"pgen.1008959.ref024","doi-asserted-by":"crossref","first-page":"12087","DOI":"10.1038\/ncomms12087","article-title":"How to make a sex chromosome","volume":"7","author":"AE Wright","year":"2016","journal-title":"Nature communications"},{"key":"pgen.1008959.ref025","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1146\/annurev.genet.33.1.603","article-title":"Meiotic chromosomes: integrating structure and function","volume":"33","author":"D Zickler","year":"1999","journal-title":"Annu Rev Genet"},{"issue":"3","key":"pgen.1008959.ref026","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1038\/ng0796-336","article-title":"Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over","volume":"13","author":"SM Baker","year":"1996","journal-title":"Nat Genet"},{"issue":"16","key":"pgen.1008959.ref027","doi-asserted-by":"crossref","first-page":"7203","DOI":"10.1128\/MCB.25.16.7203-7215.2005","article-title":"Surveillance of different recombination defects in mouse spermatocytes yields distinct responses despite elimination at an identical developmental stage","volume":"25","author":"M Barchi","year":"2005","journal-title":"Mol Cell Biol"},{"issue":"5","key":"pgen.1008959.ref028","doi-asserted-by":"crossref","first-page":"989","DOI":"10.1016\/S1097-2765(00)00098-8","article-title":"Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11","volume":"6","author":"F Baudat","year":"2000","journal-title":"Mol Cell"},{"issue":"6","key":"pgen.1008959.ref029","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1038\/ncb1135","article-title":"Cohesin SMC1 beta is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination","volume":"6","author":"E Revenkova","year":"2004","journal-title":"Nat Cell Biol"},{"issue":"5","key":"pgen.1008959.ref030","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1016\/S1097-2765(00)00097-6","article-title":"The mouse Spo11 gene is required for meiotic chromosome synapsis","volume":"6","author":"PJ Romanienko","year":"2000","journal-title":"Mol Cell"},{"issue":"1","key":"pgen.1008959.ref031","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S1097-2765(00)80404-9","article-title":"The murine SCP3 gene is required for synaptonemal complex assembly, chromosome synapsis, and male fertility","volume":"5","author":"L Yuan","year":"2000","journal-title":"Mol 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Kauppi","year":"2012","journal-title":"Annals of the New York Academy of Sciences"},{"issue":"3","key":"pgen.1008959.ref036","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1007\/s00412-012-0364-y","article-title":"Inactivation or non-reactivation: what accounts better for the silence of sex chromosomes during mammalian male meiosis?","volume":"121","author":"J Page","year":"2012","journal-title":"Chromosoma"},{"issue":"1","key":"pgen.1008959.ref037","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1016\/j.yexcr.2004.03.008","article-title":"The XY body: a specialized meiotic chromatin domain","volume":"296","author":"MA Handel","year":"2004","journal-title":"Experimental Cell Research"},{"issue":"12","key":"pgen.1008959.ref038","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1002\/bies.950141205","article-title":"Sex-chromosome pairing and activity during mammalian meiosis","volume":"14","author":"MA Handel","year":"1992","journal-title":"Bioessays"},{"issue":"23","key":"pgen.1008959.ref039","doi-asserted-by":"crossref","first-page":"2135","DOI":"10.1016\/j.cub.2004.11.032","article-title":"BRCA1, histone H2AX phosphorylation, and male meiotic sex chromosome inactivation","volume":"14","author":"JM Turner","year":"2004","journal-title":"Curr Biol"},{"issue":"2","key":"pgen.1008959.ref040","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1007\/BF00328392","article-title":"End association and segregation of the achiasmatic X and Y chromosomes of the sand rat, Psammomys obesus","volume":"78","author":"T Ashley","year":"1980","journal-title":"Chromosoma"},{"issue":"1","key":"pgen.1008959.ref041","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1111\/j.1601-5223.1995.00017.x","article-title":"Pattern of X-Y chromosome pairing in microtine rodents","volume":"123","author":"PM Borodin","year":"1995","journal-title":"Hereditas"},{"issue":"Pt 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Charlesworth","year":"2017","journal-title":"Philosophical Transactions of the Royal Society B: Biological Sciences."},{"issue":"6","key":"pgen.1008959.ref046","doi-asserted-by":"crossref","first-page":"R98","DOI":"10.1186\/gb-2008-9-6-r98","article-title":"Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes","volume":"9","author":"Q Zhou","year":"2008","journal-title":"Genome Biol"},{"issue":"1\u20134","key":"pgen.1008959.ref047","doi-asserted-by":"crossref","first-page":"33","DOI":"10.1159\/000063030","article-title":"X-Autosome translocations, meiotic synapsis, chromosome evolution and speciation","volume":"96","author":"T. 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Monesi","year":"1965","journal-title":"Chromosoma"},{"issue":"Pt 15","key":"pgen.1008959.ref061","doi-asserted-by":"crossref","first-page":"3233","DOI":"10.1242\/jcs.02466","article-title":"SPO11 is required for sex-body formation, and Spo11 heterozygosity rescues the prophase arrest of Atm-\/- spermatocytes","volume":"118","author":"MA Bellani","year":"2005","journal-title":"J Cell Sci"},{"issue":"4","key":"pgen.1008959.ref062","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1093\/genetics\/151.4.1569","article-title":"Distribution of Crossing Over on Mouse Synaptonemal Complexes Using Immunofluorescent Localization of MLH1 Protein.","volume":"151","author":"LK Anderson","year":"1999","journal-title":"Genetics"},{"issue":"6","key":"pgen.1008959.ref063","doi-asserted-by":"crossref","first-page":"1353","DOI":"10.1086\/344714","article-title":"Male mouse recombination maps for each autosome identified by chromosome painting","volume":"71","author":"L Froenicke","year":"2002","journal-title":"American journal of human genetics"},{"issue":"1","key":"pgen.1008959.ref064","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1111\/jeb.12747","article-title":"High-density linkage maps fail to detect any genetic component to sex determination in a Rana temporaria family","volume":"29","author":"A Brelsford","year":"2016","journal-title":"Journal of evolutionary biology"},{"issue":"5","key":"pgen.1008959.ref065","doi-asserted-by":"crossref","first-page":"1296","DOI":"10.1093\/molbev\/msv023","article-title":"Restriction Site-Associated DNA Sequencing (RAD-seq) Reveals an Extraordinary Number of Transitions among Gecko Sex-Determining Systems.","volume":"32","author":"T Gamble","year":"2015","journal-title":"Mol Biol Evol"},{"issue":"1","key":"pgen.1008959.ref066","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1038\/hdy.2015.10","article-title":"Transition in sexual system and sex chromosome evolution in the tadpole shrimp Triops cancriformis","volume":"115","author":"TC Mathers","year":"2015","journal-title":"Heredity"},{"issue":"4","key":"pgen.1008959.ref067","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1111\/jeb.13242","article-title":"Dynamic sex chromosomes in Old World chameleons (Squamata: Chamaeleonidae).","volume":"31","author":"SV Nielsen","year":"2018","journal-title":"Journal of evolutionary biology"},{"issue":"4","key":"pgen.1008959.ref068","doi-asserted-by":"crossref","first-page":"752","DOI":"10.1111\/1755-0998.12624","article-title":"Identifying homomorphic sex chromosomes from wild-caught adults with limited genomic resources","volume":"17","author":"A Brelsford","year":"2017","journal-title":"Mol Ecol Resour"},{"issue":"1604","key":"pgen.1008959.ref069","doi-asserted-by":"crossref","first-page":"2925","DOI":"10.1098\/rspb.2006.3670","article-title":"Phylogenomics of the genus Mus (Rodentia; 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Schimenti","year":"2005","journal-title":"Nat Genet"},{"issue":"1","key":"pgen.1008959.ref077","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1038\/ng1484","article-title":"Silencing of unsynapsed meiotic chromosomes in the mouse","volume":"37","author":"JM Turner","year":"2005","journal-title":"Nat Genet"},{"issue":"6","key":"pgen.1008959.ref078","doi-asserted-by":"crossref","first-page":"642","DOI":"10.1038\/ng1368","article-title":"The mouse X chromosome is enriched for sex-biased genes not subject to selection by meiotic sex chromosome inactivation","volume":"36","author":"PP Khil","year":"2004","journal-title":"Nat Genet"},{"issue":"2","key":"pgen.1008959.ref079","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1007\/BF00356023","article-title":"Sex chromosomes, recombination, and chromatin conformation","volume":"102","author":"BD McKee","year":"1993","journal-title":"Chromosoma"},{"issue":"2","key":"pgen.1008959.ref080","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.tem.2004.01.007","article-title":"X chromosomes, retrogenes and their role in male reproduction","volume":"15","author":"JP Wang","year":"2004","journal-title":"Trends Endocrinol Metab"},{"issue":"1403","key":"pgen.1008959.ref081","doi-asserted-by":"crossref","first-page":"1563","DOI":"10.1098\/rstb.2000.0717","article-title":"The degeneration of Y chromosomes","volume":"355","author":"B Charlesworth","year":"2000","journal-title":"Philos Trans R Soc Lond B Biol Sci"},{"issue":"9","key":"pgen.1008959.ref082","doi-asserted-by":"crossref","first-page":"e1000186","DOI":"10.1371\/journal.pgen.1000186","article-title":"MUS81 Generates a Subset of MLH1-MLH3\u2013Independent Crossovers in Mammalian Meiosis.","volume":"4","author":"JK Holloway","year":"2008","journal-title":"PLoS Genetics"},{"issue":"10","key":"pgen.1008959.ref083","doi-asserted-by":"crossref","first-page":"3155","DOI":"10.1111\/j.1558-5646.2012.01661.x","article-title":"The evolution of XY recombination: sexually antagonistic selection versus deleterious mutation load","volume":"66","author":"C Grossen","year":"2012","journal-title":"Evolution; international journal of organic evolution"},{"issue":"1684","key":"pgen.1008959.ref084","first-page":"1049","article-title":"A novel sex determination system in a close relative of the house mouse.","volume":"277","author":"F Veyrunes","year":"2010","journal-title":"Proceedings Biological sciences."},{"issue":"6","key":"pgen.1008959.ref085","doi-asserted-by":"crossref","first-page":"1987","DOI":"10.1534\/g3.119.400242","article-title":"Little Evidence of Antagonistic Selection in the Evolutionary Strata of Fungal Mating-Type Chromosomes (Microbotryum lychnidis-dioicae).","volume":"9","author":"AL Bazzicalupo","year":"2019","journal-title":"G3"},{"issue":"7","key":"pgen.1008959.ref086","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1016\/j.tig.2018.04.001","article-title":"Why Do Sex Chromosomes Stop Recombining?","volume":"34","author":"S Ponnikas","year":"2018","journal-title":"Trends Genet"},{"issue":"4","key":"pgen.1008959.ref087","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1007\/BF00292848","article-title":"Synaptonemal complex analysis of mouse chromosomal rearrangements. IV. Synapsis and synaptic adjustment in two paracentric inversions","volume":"84","author":"MJ Moses","year":"1982","journal-title":"Chromosoma"},{"issue":"4","key":"pgen.1008959.ref088","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1111\/j.1558-5646.1987.tb05864.x","article-title":"The accumulation of sexually antagonistic genes as a selective agent promoting the evolution of reduced recombination between primitive sex chromosomes","volume":"41","author":"WR Rice","year":"1987","journal-title":"Evolution; international journal of organic evolution"},{"issue":"7","key":"pgen.1008959.ref089","doi-asserted-by":"crossref","first-page":"2119","DOI":"10.1111\/evo.12387","article-title":"XY females do better than the xx in the African pygmy mouse, Mus minutoides","volume":"68","author":"PA Saunders","year":"2014","journal-title":"Evolution; international journal of organic evolution"},{"issue":"1786","key":"pgen.1008959.ref090","first-page":"20140297","article-title":"Genetic 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ANKRD31 Regulates Spatiotemporal Patterning of Meiotic Recombination Initiation and Ensures Recombination between X and Y Sex Chromosomes","volume":"74","author":"F Papanikos","year":"2019","journal-title":"Molecular Cell"},{"issue":"1","key":"pgen.1008959.ref094","doi-asserted-by":"crossref","first-page":"e1007439","DOI":"10.1371\/journal.pgen.1007439","article-title":"Transition from a meiotic to a somatic-like DNA damage response during the pachytene stage in mouse meiosis","volume":"15","author":"A Enguita-Marruedo","year":"2019","journal-title":"PLoS Genetics"},{"issue":"2","key":"pgen.1008959.ref095","doi-asserted-by":"crossref","first-page":"R30","DOI":"10.1186\/gb-2008-9-2-r30","article-title":"Genomic degradation of a young Y chromosome in Drosophila miranda","volume":"9","author":"D Bachtrog","year":"2008","journal-title":"Genome 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Zhou","year":"2012","journal-title":"Science"},{"issue":"2","key":"pgen.1008959.ref099","doi-asserted-by":"crossref","first-page":"793","DOI":"10.1534\/genetics.104.039073","article-title":"The program of sex chromosome pairing in meiosis is highly conserved across marsupial species: implications for sex chromosome evolution","volume":"170","author":"J Page","year":"2005","journal-title":"Genetics"},{"issue":"Pt 3","key":"pgen.1008959.ref100","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1242\/jcs.00252","article-title":"The pairing of X and Y chromosomes during meiotic prophase in the marsupial species Thylamys elegans is maintained by a dense plate developed from their axial elements","volume":"116","author":"J Page","year":"2003","journal-title":"J Cell Sci"},{"issue":"3","key":"pgen.1008959.ref101","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1007\/s00412-006-0059-3","article-title":"Sex chromosomes, synapsis, and cohesins: a complex 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Wolf","year":"1988","journal-title":"Chromosoma"},{"issue":"1","key":"pgen.1008959.ref105","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1023\/A:1018445520117","article-title":"A drying-down technique for the spreading of mammalian meiocytes from the male and female germline","volume":"5","author":"AH Peters","year":"1997","journal-title":"Chromosome Res"},{"issue":"8","key":"pgen.1008959.ref106","doi-asserted-by":"crossref","first-page":"639","DOI":"10.1023\/A:1009209628300","article-title":"Squash procedure for protein immunolocalization in meiotic cells","volume":"6","author":"J Page","year":"1998","journal-title":"Chromosome Res"},{"key":"pgen.1008959.ref107","unstructured":"Andrews S. 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