{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,1,29]],"date-time":"2026-01-29T13:45:16Z","timestamp":1769694316259,"version":"3.49.0"},"reference-count":71,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,3,11]],"date-time":"2019-03-11T00:00:00Z","timestamp":1552262400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2019,3,11]],"date-time":"2019-03-11T00:00:00Z","timestamp":1552262400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Multiple sex chromosome systems have been described for several mammalian orders, with different species from the same genus sharing the same system (e.g., X<jats:sub>1<\/jats:sub>X<jats:sub>2<\/jats:sub>Y or XY<jats:sub>1<\/jats:sub>Y<jats:sub>2<\/jats:sub>). This is important because the translocated autosome may be influenced by the evolution of the recipient sex chromosome, and this may be related to speciation. It is often thought that the translocation of an autosome to a sex chromosome may share a common origin among phylogenetically related species. However, the neo-X chromosomes of <jats:italic>Proechimys goeldii<\/jats:italic> (2n\u2009=\u200924\u2640, 25\u2642\/NFa\u2009=\u200942) and <jats:italic>Proechimys<\/jats:italic> gr. <jats:italic>goeldii<\/jats:italic> (2n\u2009=\u200916\u2640, 17\u2642\/NFa\u2009=\u200914) have distinct sizes and morphologies that have made it difficult to determine whether they have the same or different origins. This study investigates the origins of the XY<jats:sub>1<\/jats:sub>Y<jats:sub>2<\/jats:sub> sex chromosome determination system in <jats:italic>P. goeldii<\/jats:italic> (PGO) and <jats:italic>P<\/jats:italic>. gr. <jats:italic>goeldii<\/jats:italic> (PGG) and elucidates the chromosomal rearrangements in this low-diploid-number group of <jats:italic>Proechimys<\/jats:italic> species. Toward this end, we produced whole-chromosome probes for <jats:italic>P. roberti<\/jats:italic> (PRO; 2n\u2009=\u200930\u2642\/NFa\u2009=\u200954) and <jats:italic>P<\/jats:italic>. <jats:italic>goeldii<\/jats:italic> (2n\u2009=\u200925\u2642\/NFa\u2009=\u200942) and used them in comparative chromosomal mapping. Our analysis reveals that multiple translocations and inversions are responsible for the karyotype diversity of these species, with only three whole-chromosomes conserved between PRO and PGO and eight between PGO and PGG. Our data indicate that multiple sex chromosome systems have originated twice in <jats:italic>Proechimys<\/jats:italic>. As small populations are prone to the fixation of chromosomal rearrangements, we speculate that biological features of Rodentia contribute to this fixation. We also highlight the potential of these rodents as a model for studying sex chromosome evolution.<\/jats:p>","DOI":"10.1038\/s41598-019-40593-8","type":"journal-article","created":{"date-parts":[[2019,3,11]],"date-time":"2019-03-11T11:02:58Z","timestamp":1552302178000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Identification of two independent X-autosome translocations in closely related mammalian (Proechimys) species"],"prefix":"10.1038","volume":"9","author":[{"given":"Willam","family":"Oliveira da Silva","sequence":"first","affiliation":[]},{"given":"Marlyson Jeremias","family":"Rodrigues da Costa","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2951-8877","authenticated-orcid":false,"given":"Julio Cesar","family":"Pieczarka","sequence":"additional","affiliation":[]},{"given":"Jorge","family":"Rissino","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1472-1613","authenticated-orcid":false,"given":"Jorge C.","family":"Pereira","sequence":"additional","affiliation":[]},{"given":"Malcolm Andrew","family":"Ferguson-Smith","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1516-2734","authenticated-orcid":false,"given":"Cleusa Yoshiko","family":"Nagamachi","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2019,3,11]]},"reference":[{"key":"40593_CR1","doi-asserted-by":"crossref","unstructured":"Eldredge, N. Unfinished Synthesis: Biological Hierarchies and Modern Evolutionary Thought. (New York: Oxford University. 1985).","DOI":"10.1093\/oso\/9780195036336.001.0001"},{"key":"40593_CR2","unstructured":"Mayr, E. Systematics and the Origin of Species. (New York: Columbia University Press. 1942)."},{"key":"40593_CR3","doi-asserted-by":"crossref","unstructured":"Mayr, E. Animal Species and Evolution. (Cambridge: Harvard University. 1963).","DOI":"10.4159\/harvard.9780674865327"},{"key":"40593_CR4","unstructured":"Ridley, M. Evolution. (Massachusetts: Blackwell. 2004)."},{"key":"40593_CR5","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1046\/j.1469-8137.2003.00948.x","volume":"161","author":"DE Soltis","year":"2003","unstructured":"Soltis, D. E., Soltis, P. S. & Tate, J. A. Advances in the study of polyploidy since plant speciation. New Phytol. Lancaster 161, 173\u2013191 (2003).","journal-title":"New Phytol. Lancaster"},{"key":"40593_CR6","doi-asserted-by":"crossref","unstructured":"Rieseberg, L. H. Chromosomal rearrangements and speciation. Trends Ecol Evol. London, 16, n.7, p.351\u2013357 (2001).","DOI":"10.1016\/S0169-5347(01)02187-5"},{"key":"40593_CR7","unstructured":"King, M. Species Evolution. The Role of Chromosome Change. (Cambridge: (Cambridge University Press. 1993)."},{"key":"40593_CR8","doi-asserted-by":"publisher","first-page":"1079","DOI":"10.1038\/nature08441","volume":"461","author":"J Kitano","year":"2009","unstructured":"Kitano, J. et al. A role for a neo-sex chromosome in stickleback speciation. Nature. 461, 1079\u20131083 (2009).","journal-title":"Nature."},{"key":"40593_CR9","doi-asserted-by":"publisher","first-page":"965","DOI":"10.1101\/gr.7101908","volume":"18","author":"F Veyrunes","year":"2008","unstructured":"Veyrunes, F. et al. Bird-like sex chromosomes of platypus imply recent origin of mammal sex chromosomes. Genome Res. 18, 965\u2013973 (2008).","journal-title":"Genome Res."},{"key":"40593_CR10","doi-asserted-by":"publisher","first-page":"3198","DOI":"10.1111\/j.1558-5646.2012.01681.x","volume":"66","author":"K Yoshida","year":"2012","unstructured":"Yoshida, K. & Kitano, J. The contribution of female meiotic drive to the evolution of Neo-Sex chromosomes. Evolution. 66, 3198\u20133208 (2012).","journal-title":"Evolution."},{"key":"40593_CR11","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1007\/s10577-013-9365-9","volume":"21","author":"JC Pieczarka","year":"2013","unstructured":"Pieczarka, J. C. et al. A phylogenetic analysis using multidirectional chromosome painting of three species (Uroderma magnirostrum, U. bilobatum and Artibeus obscurus) of subfamily Stenodermatinae (Chiroptera-Phyllostomidae). Chromosom Res. 21, 383\u201392 (2013).","journal-title":"Chromosom Res."},{"key":"40593_CR12","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1007\/s10577-006-1116-8","volume":"15","author":"F Veyrunes","year":"2007","unstructured":"Veyrunes, F., Watson, J., Robinson, T. J. & Britton-Davidian, J. Accumulation of rare sex chromosome rearrangements in the African pygmy mouse, Mus (Nannomys) minutoides: a whole-arm reciprocal translocation (WART) involving an X-autosome fusion. Chromosome Res. 15, 223\u2013230 (2007).","journal-title":"Chromosome Res."},{"key":"40593_CR13","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1007\/s10577-016-9524-x","volume":"24","author":"M Vozdova","year":"2016","unstructured":"Vozdova, M. et al. Meiotic behaviour of evolutionary sex-autosome translocations in Bovidae. Chromosome Res. 24, 325\u201338 (2016).","journal-title":"Chromosome Res."},{"key":"40593_CR14","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1007\/s10577-005-2886-0","volume":"13","author":"JC Pieczarka","year":"2005","unstructured":"Pieczarka, J. C. et al. Reciprocal chromosome painting between two South American bats: Carollia brevicauda and Phyllostomus hastatus (Phyllostomidae, Chiroptera). Chromosom Res. 13, 349\u201347 (2005).","journal-title":"Chromosom Res."},{"key":"40593_CR15","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1186\/s12862-016-0689-x","volume":"16","author":"AJB Gomes","year":"2016","unstructured":"Gomes, A. J. B. et al. Chromosomal phylogeny of Vampyressine bats (Chiroptera, Phyllostomidae) with description of two new sex chromosome systems. BMC Evol Biol. 16, 119, https:\/\/doi.org\/10.1186\/s12862-016-0689-x (2016).","journal-title":"BMC Evol Biol."},{"key":"40593_CR16","doi-asserted-by":"publisher","unstructured":"Ara\u00fajo, N. P., Stanyon, R., Pereira, V. S. & Svartman, M. Interspecific chromosome painting provides clues to the ancestral karyotype of the New World monkey genus Aotus. J. Mammal Evol. 1\u20138, https:\/\/doi.org\/10.1007\/s10914-017-9403-z (2017).","DOI":"10.1007\/s10914-017-9403-z"},{"key":"40593_CR17","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1023\/A:1021520529952","volume":"10","author":"EHC De Oliveira","year":"2002","unstructured":"De Oliveira, E. H. C. et al. The phylogeny of howler monkeys (Alouatta, Platyrrhini): Reconstruction by multicolor cross-species chromosome painting. Chromosome Res. 10, 669\u2013683 (2002).","journal-title":"Chromosome Res."},{"key":"40593_CR18","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1023\/B:CHRO.0000034098.09885.e6","volume":"12","author":"F Veyrunes","year":"2004","unstructured":"Veyrunes, F. et al. Autosome and sex chromosome diversity among the African pygmy mice, subgenus Nannomys (Murinae; Mus). Chromosome Res. 12, 369\u2013382 (2004).","journal-title":"Chromosome Res."},{"key":"40593_CR19","doi-asserted-by":"publisher","first-page":"682","DOI":"10.1590\/S1415-47572005000500007","volume":"28","author":"T Machado","year":"2005","unstructured":"Machado, T., Silva, M. J., Leal-Mesquita, E. R., Carmignotto, A. P. & Yonenaga-Yassuda, Y. Nine karyomorphs for spiny rats of the genus Proechimys (Echimyidae, Rodentia) from North and Central Brazil. Genet. Mol Biol. 28, 682\u2013692 (2005).","journal-title":"Genet. Mol Biol."},{"key":"40593_CR20","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2156-14-21","volume":"14","author":"PJ Amaral","year":"2013","unstructured":"Amaral, P. J. et al. Proechimys (Rodentia, Echimyidae): characterization and taxonomic considerations of a form with a very low diploid number and a multiple sex chromosome system. BMC Genet. 14, 21 (2013).","journal-title":"BMC Genet."},{"key":"40593_CR21","doi-asserted-by":"crossref","unstructured":"Patton, J. L., Pardi\u00f1as, U. F. J. & D\u2019El\u00eda, G. Mammals of South America. Volume 2, Rodents. (The University of Chicago Press 2015).","DOI":"10.7208\/chicago\/9780226169606.001.0001"},{"key":"40593_CR22","doi-asserted-by":"publisher","unstructured":"Rodrigues da Costa, M. J. et al. Cryptic species in Proechimys goeldii (Rodentia, Echimyidae)? A case of molecular and chromosomal differentiation in allopatric populations. Cytogenet. Genome Res, https:\/\/doi.org\/10.1159\/000446562 (2016).","DOI":"10.1159\/000446562"},{"key":"40593_CR23","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1159\/000131880","volume":"35","author":"AG Searle","year":"1983","unstructured":"Searle, A. G., Beechey, C. V., Evans, E. P. & Kirk, M. Two new Xautosome translocations in the mouse. Cytogenet Cell Genet. 35, 279\u2013292 (1983).","journal-title":"Cytogenet Cell Genet."},{"key":"40593_CR24","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1017\/S0016672300029761","volume":"58","author":"C Tease","year":"1991","unstructured":"Tease, C. & Fisher, G. Two new X-autosome Robertsonian translocations in the mouse. I. Meiotic chromosome segregation in male hemizygotes and female heterozygotes. Genet Res. 58, 115\u2013121 (1991).","journal-title":"Genet Res."},{"key":"40593_CR25","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1159\/000338413","volume":"136","author":"J-W Kim","year":"2012","unstructured":"Kim, J.-W. et al. Molecular and clinical characteristics of 26 cases with structural Y chromosome aberrations. Cytogenet Genome Res. 136, 270\u2013277 (2012).","journal-title":"Cytogenet Genome Res."},{"key":"40593_CR26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1080\/00087114.2004.10589365","volume":"57","author":"RCR Noronha","year":"2004","unstructured":"Noronha, R. C. R. et al. Meiotic analyses of the sex chromosomes in Carolliinae-Phyllostomidae (Chiroptera): NOR separates the XY1Y2 into two independent parts. Caryologia. 57, 1\u20139 (2004).","journal-title":"Caryologia."},{"key":"40593_CR27","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1080\/00087114.2001.10589235","volume":"54","author":"RCR Noronha","year":"2001","unstructured":"Noronha, R. C. R., Nagamachi, C. Y., Pieczarka, J. C., Marques-Aguiar, S. & Barros, R. M. S. Sex-autosome translocations: meiotic behavior suggests an inactivation block with permanence of autosomal gene activity in Phyllostomid bats. Caryologia. 54, 267\u2013277 (2001).","journal-title":"Caryologia."},{"key":"40593_CR28","doi-asserted-by":"publisher","first-page":"830","DOI":"10.4238\/2012.April.3.5","volume":"11","author":"ES Eler","year":"2012","unstructured":"Eler, E. S., Da Silva, M. N., Silva, C. E. & Feldberg, E. Comparative cytogenetics of spiny rats of the genus Proechimys (Rodentia, Echimyidae) from the Amazon region. Genet. Mol Res. 11, 830\u2013846 (2012).","journal-title":"Genet. Mol Res."},{"key":"40593_CR29","unstructured":"Mendes-Oliveira, A. C. & Miranda, C. L. Pequenos Mam\u00edferos N\u00e3o-Voadores da Amaz\u00f4nia Brasileira. Rio de Janeiro: Sociedade Brasileira de Mastozoologia S\u00e9rie Livros 2, 336p, (2015)."},{"key":"40593_CR30","first-page":"1","volume":"44","author":"JL Patton","year":"1972","unstructured":"Patton, J. L. & Gardner, L. A. Notes on the systematics of Proechimys (Rodentia: Echimyidae), with emphasis on Peruvian forms. Occas. Pap. Mus. Zool. Louisiana State University. 44, 1\u201330 (1972).","journal-title":"Occas. Pap. Mus. Zool. Louisiana State University."},{"key":"40593_CR31","doi-asserted-by":"publisher","first-page":"475","DOI":"10.1046\/j.1365-294x.1998.00276.x","volume":"7","author":"MN Da Silva","year":"1998","unstructured":"Da Silva, M. N. & Patton, J. L. Molecular phylogeography and the evolution and conservation of Amazonian mammals. Mol Ecol. 7, 475\u2013486 (1998).","journal-title":"Mol Ecol."},{"key":"40593_CR32","first-page":"1500","volume":"29","author":"VM Aniskin","year":"1993","unstructured":"Aniskin, V. M. Three new karyotypes of prickly chinchillas of the family Echimyidae (Rodentia). Genetika. 29, 1500\u20137 (1993).","journal-title":"Genetika."},{"key":"40593_CR33","first-page":"315","volume":"63","author":"JFS Lima","year":"1998","unstructured":"Lima, J. F. S., Langguth, A. & Sousa, L. C. The karyotype of Makalata didelphoides (Rodentia, Echimyidae). Z. S\u00e4ugetierk. 63, 315\u201318 (1998).","journal-title":"Z. S\u00e4ugetierk."},{"key":"40593_CR34","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1206\/0003-0090(2000)244<0001:MOTRJA>2.0.CO;2","volume":"244","author":"JL Patton","year":"2000","unstructured":"Patton, J. L., Silva, M. N. F. & Malcolm, J. R. Mammals of the Rio Juru\u00e1 and the evolutionary and ecological diversification of Amazomia. Bull. Am Mus Nat Hist. 244, 202\u2013292 (2000).","journal-title":"Bull. Am Mus Nat Hist."},{"key":"40593_CR35","first-page":"121","volume":"66","author":"JL Dunnum","year":"2001","unstructured":"Dunnum, J. L., Salazar-Bravo, J. & Yates, T. L. The Bolivian bamboo rat, Dactylomys boliviensis (Rodentia: Echimyidae), a new record for chromosome number in a mammal. Mamm. Biol. 66, 121\u2013126 (2001).","journal-title":"Mamm. Biol."},{"key":"40593_CR36","first-page":"5","volume":"17","author":"R Paresque","year":"2004","unstructured":"Paresque, R., de Souza, W. P., Mendes, S. L. & Fagundes, V. Composic\u00e3o cariot\u00edpica da fauna de roedores e marsupiais de duas \u00e1reas de Mata Atl\u00e2ntica do Esp\u00edrito Santo. Brasil. Bol. Mus. Biol. Mello Leit\u00e3o, nova s\u00e9rie 17, 5\u201333 (2004).","journal-title":"Brasil. Bol. Mus. Biol. Mello Leit\u00e3o, nova s\u00e9rie"},{"key":"40593_CR37","doi-asserted-by":"publisher","first-page":"697","DOI":"10.1590\/S1415-47572008000400016","volume":"31","author":"K Ventura","year":"2008","unstructured":"Ventura, K. et al. Karyotypic analyses and morphological comments on the endemic and endangered Brazilian painted tree rat Callistomys pictus (Rodentia, Echimyidae). Genet. Mol. Biol. 31, 697\u2013703 (2008).","journal-title":"Genet. Mol. Biol."},{"key":"40593_CR38","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1038\/nature03440","volume":"434","author":"MT Ross","year":"2005","unstructured":"Ross, M. T. et al. The DNA sequence of the human X chromosome. Nature 434, 325\u2013337 (2005).","journal-title":"Nature"},{"key":"40593_CR39","doi-asserted-by":"publisher","first-page":"1823","DOI":"10.1242\/dev.000018","volume":"134","author":"JM Turner","year":"2007","unstructured":"Turner, J. M. Meiotic sex chromosome inactivation. Development 134, 1823\u20131831 (2007).","journal-title":"Development"},{"key":"40593_CR40","first-page":"197","volume":"26","author":"S Kasahara","year":"1983","unstructured":"Kasahara, S. & Dutrillaux, B. Chromosome banding patterns of four species of bats, with special reference to a case of X-autosome translocation. Ann G\u00e9n\u00e9t 26, 197\u2013201 (1983).","journal-title":"Ann G\u00e9n\u00e9t"},{"key":"40593_CR41","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1007\/s00412-004-0292-6","volume":"113","author":"G Dobigny","year":"2004","unstructured":"Dobigny, G., Ozouf-Costaz, C., Bonillo, C. & Volobouev, V. Viability of X-autosome translocations in mammals: an epigenomic hypothesis from a rodent case-study. Chromosoma 113, 34\u201341 (2004).","journal-title":"Chromosoma"},{"key":"40593_CR42","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1159\/000200086","volume":"124","author":"RCR Noronha","year":"2009","unstructured":"Noronha, R. C. R., Nagamachi, C. Y., O\u2019Brien, P. C. M., Ferguson-Smith, M. A. & Pieczarka, J. C. Neo-XY body: an analysis of XY1Y2 meiotic behavior in Carollia (Chiroptera, Phyllostomidae) by chromosome painting. Cytogenet. Genome Res. 124, 37\u201343 (2009).","journal-title":"Cytogenet. Genome Res."},{"issue":"11","key":"40593_CR43","doi-asserted-by":"publisher","first-page":"e27239","DOI":"10.1371\/journal.pone.0027239","volume":"6","author":"M Farr\u00e9","year":"2011","unstructured":"Farr\u00e9, M., Bosch, M., L\u00f3pez-Giraldez, F., Ponsa, M. & Ruiz-Herrera, A. Assessing the role of tandem repeats in shaping the genomic architecture of great apes. PLoS ONE 6(11), e27239, https:\/\/doi.org\/10.1371\/journal.pone.0027239 (2011).","journal-title":"PLoS ONE"},{"key":"40593_CR44","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2004-5-4-r23","volume":"5","author":"JA Bailey","year":"2004","unstructured":"Bailey, J. A., Baertsch, R., Kent, W. J., Haussler, D. & Eichler, E. E. Hotspots of mammalian chromosomal evolution. Genome Biol. 5, R23, https:\/\/doi.org\/10.1186\/gb-2004-5-4-r23 (2004).","journal-title":"Genome Biol."},{"key":"40593_CR45","doi-asserted-by":"publisher","first-page":"542","DOI":"10.1016\/j.ygeno.2005.01.012","volume":"85","author":"H Kehrer-Sawatzki","year":"2005","unstructured":"Kehrer-Sawatzki, H., Szamalek, J. M., Tanzer, S., Platzer, M. & Hameister, H. Molecular characterization of the pericentric inversion of chimpanzee chromosome 11 homologous to human chromosome 9. Genomics 85, 542\u2013550 (2005).","journal-title":"Genomics"},{"key":"40593_CR46","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-10-334","volume":"10","author":"MS Longo","year":"2009","unstructured":"Longo, M. S., Carone, D. M., Green, E. D., O\u2019Neill, M. J. & O\u2019Neill, R. J. Distinct retroelement classes define evolutionary breakpoints demarcating sites of evolutionary novelty. BMC Genomics. 10, 334, https:\/\/doi.org\/10.1186\/1471-2164-10-334 (2009).","journal-title":"BMC Genomics."},{"key":"40593_CR47","doi-asserted-by":"publisher","first-page":"507","DOI":"10.1101\/gr.1975204","volume":"14","author":"G Bourque","year":"2004","unstructured":"Bourque, G., Pevzner, P. A. & Tesler, G. Reconstructing the genomic architecture of ancestral mammals: lessons from human, mouse, and rat genomes. Genome Res. 14, 507\u2013516 (2004).","journal-title":"Genome Res."},{"key":"40593_CR48","doi-asserted-by":"publisher","first-page":"7672","DOI":"10.1073\/pnas.1330369100","volume":"100","author":"P Pevzner","year":"2003","unstructured":"Pevzner, P. & Tesler, G. Human and mouse genomic sequences reveal extensive breakpoint reuse in mammalian evolution. PNAS 100, 7672\u20137677 (2003).","journal-title":"PNAS"},{"key":"40593_CR49","doi-asserted-by":"publisher","first-page":"770","DOI":"10.1101\/gr.086546.108","volume":"19","author":"DM Larkin","year":"2009","unstructured":"Larkin, D. M. et al. Breakpoint regions and homologous synteny blocks in chromosomes have different evolutionary histories. Genome Res. 19, 770\u2013777 (2009).","journal-title":"Genome Res."},{"key":"40593_CR50","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1515\/mamm.1995.59.1.51","volume":"59","author":"HG Bergallo","year":"1995","unstructured":"Bergallo, H. G. Comparative life-history characteristics of two species of rats, Proechimys iheringi and Oryzomys intermedium in an Atlantic Forest of Brazil. Mammalia 59, 51\u201364 (1995).","journal-title":"Mammalia"},{"key":"40593_CR51","doi-asserted-by":"publisher","first-page":"3331","DOI":"10.1098\/rstb.2009.0140","volume":"364","author":"FH Bronson","year":"2009","unstructured":"Bronson, F. H. Climate change and seasonal reproduction in mammals. Phil. Trans. R. Soc. B 364, 3331\u20133340, https:\/\/doi.org\/10.1098\/rstb.2009.0140 (2009).","journal-title":"Phil. Trans. R. Soc. B"},{"key":"40593_CR52","doi-asserted-by":"publisher","first-page":"3356","DOI":"10.1242\/jeb.105908","volume":"217","author":"SS Hillman","year":"2014","unstructured":"Hillman, S. S., Drewes, R. C., Hedrick, M. S. & Hancock, T. V. Physiological vagility and its relationship to dispersal and neutral genetic heterogeneity in vertebrates. J. Exp. Biol. 217, 3356\u20133364 (2014).","journal-title":"J. Exp. Biol."},{"key":"40593_CR53","doi-asserted-by":"publisher","first-page":"3942","DOI":"10.1073\/pnas.74.9.3942","volume":"74","author":"GL Bush","year":"1977","unstructured":"Bush, G. L., Case, S. M., Wilson, A. C. & Patton, J. L. Rapid speciation and chromosomal evolution in mammals. PNAS. 74, 3942\u20133946 (1977).","journal-title":"PNAS."},{"key":"40593_CR54","doi-asserted-by":"publisher","first-page":"234","DOI":"10.1111\/j.1558-5646.1979.tb04678.x","volume":"33","author":"R Lande","year":"1979","unstructured":"Lande, R. Effective deme sizes during long-term evolution estimated from rates of chromosomal rearrangement. Evolution 33, 234\u2013251 (1979).","journal-title":"Evolution"},{"key":"40593_CR55","doi-asserted-by":"publisher","first-page":"323","DOI":"10.1038\/hdy.1985.43","volume":"54","author":"R Lande","year":"1985","unstructured":"Lande, R. The fixation of chromosomal rearrangements in a subdivided population with local extinction and colonization. Heredity 54, 323\u2013332 (1985).","journal-title":"Heredity"},{"key":"40593_CR56","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1093\/genetics\/159.3.1179","volume":"159","author":"F Pardo-Manuel de Villena","year":"2001","unstructured":"Pardo-Manuel de Villena, F. & Sapienza, C. Female meiosis drives karyotypic evolution in mammals. Genetics 159, 1179\u20131189 (2001).","journal-title":"Genetics"},{"key":"40593_CR57","doi-asserted-by":"publisher","first-page":"510","DOI":"10.1086\/284008","volume":"120","author":"JB Walsh","year":"1982","unstructured":"Walsh, J. B. Rate of accumulation of reproductive isolation by chromosomal rearrangements. Am. Nat. 120, 510\u2013532 (1982).","journal-title":"Am. Nat."},{"key":"40593_CR58","doi-asserted-by":"publisher","first-page":"330","DOI":"10.1016\/S0169-5347(01)02177-2","volume":"16","author":"M Turelli","year":"2001","unstructured":"Turelli, M., Barton, N. H. & Coyne, J. A. Theory and speciation. Trends Ecol Evol. 16, 330\u2013343 (2001).","journal-title":"Trends Ecol Evol."},{"key":"40593_CR59","doi-asserted-by":"publisher","first-page":"322","DOI":"10.1111\/j.1558-5646.1981.tb04890.x","volume":"35","author":"PW Hedrick","year":"1981","unstructured":"Hedrick, P. W. The establishment of chromosomal variants. Evolution 35, 322\u2013332 (1981).","journal-title":"Evolution"},{"key":"40593_CR60","doi-asserted-by":"publisher","first-page":"8245","DOI":"10.1073\/pnas.83.21.8245","volume":"83","author":"R Baker","year":"1986","unstructured":"Baker, R., Robert, J. & Bickham, J. W. Speciation by monobrachial centric fusions. PNAS, Washington 83, 8245\u20138248 (1986).","journal-title":"PNAS, Washington"},{"key":"40593_CR61","doi-asserted-by":"publisher","first-page":"425","DOI":"10.2307\/1564953","volume":"28","author":"CFB Haddad","year":"1994","unstructured":"Haddad, C. F. B., Pombal, J. R., Jos\u00e9, P. & Batistic, R. F. Natural hybridization between diploid and tetraploid species of leaf-frogs, genus Phyllomedusa (Amphibia). J Herpetol. 28, 425\u2013430 (1994).","journal-title":"J Herpetol."},{"key":"40593_CR62","unstructured":"Barros, R. M. S. Variabilidade cromoss\u00f4mica em Proechimys e Oryzomys (Rodentia) da Amaz\u00f4nia, PhD. Dissertation, p. 184 (University of S\u00e3o Paulo, S\u00e3o Paulo, 1978)."},{"key":"40593_CR63","unstructured":"Silva, J. M. C., Rylands, A. B. & Fonseca, G. A. B. O destino das \u00e1reas de endemismo. Megadiversidade. 1(2005)."},{"key":"40593_CR64","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1098\/rspb.2011.1120","volume":"279","author":"CC Ribas","year":"2011","unstructured":"Ribas, C. C., Aleixo, A., Nogueira, A. C. R., Miyaki, C. Y. & Cracraft, J. A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years. Proc. R. Soc. B. 279, 681\u20139 (2011).","journal-title":"Proc. R. Soc. B."},{"key":"40593_CR65","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1590\/1809-4392201401953","volume":"45","author":"M Santos-Filho","year":"2015","unstructured":"Santos-Filho, M., De L\u00e1zari, P. R., Sousa, C. P. F. & Canale, G. R. Trap efficiency evaluation for small mammals in the southern Amazon. Acta Amaz. 45, 187\u2013194 (2015).","journal-title":"Acta Amaz."},{"key":"40593_CR66","first-page":"503","volume":"18","author":"E Morielle-Versute","year":"1995","unstructured":"Morielle-Versute, E. & Varella-Garcia, M. A simple and fast procedure to grow bat fibroblasts from lung biopsies for cytogenetic studies. Rev. Bras. Genet. 18, 503\u2013505 (1995).","journal-title":"Rev. Bras. Genet."},{"key":"40593_CR67","doi-asserted-by":"publisher","first-page":"642","DOI":"10.1007\/BF00357691","volume":"103","author":"F Yang","year":"1995","unstructured":"Yang, F., Carter, N. P., Shi, L. & Ferguson-Smith, M. A. A comparative study of karyotypes of muntjacs by chromosome painting. Chromosoma 103, 642\u2013652 (1995).","journal-title":"Chromosoma"},{"key":"40593_CR68","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1002\/gcc.2870040311","volume":"4","author":"H Telenius","year":"1992","unstructured":"Telenius, H. et al. Cytogenetic analysis by chromosome painting using DOP-PCR amplified flow-sorted chromosomes. Genes Chromosomes Cancer 4, 257\u2013263 (1992).","journal-title":"Genes Chromosomes Cancer"},{"key":"40593_CR69","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1007\/s004120050222","volume":"106","author":"F Yang","year":"1997","unstructured":"Yang, F. et al. Chromosomal evolution of the chinese muntjac (Muntiacus reevesi). Chromosoma 106, 37\u201343 (1997).","journal-title":"Chromosoma"},{"key":"40593_CR70","first-page":"282","volume":"31","author":"AT Sumner","year":"1971","unstructured":"Sumner, A. T., Evans, H. J. & Buckland, R. A. New technique for distinguishing between human chromosomes. Nature 31, 282 (1971).","journal-title":"Nature"},{"key":"40593_CR71","doi-asserted-by":"crossref","unstructured":"Wienberg, J., Adamski, E., Yang, F., M\u00fcller, S. & Ferguson-Smith, M. A. Chromosome painting without competitor DNA. Technical Tips Online, (http:\/\/www.elsevier.com\/locate\/tto) T40065 (1997).","DOI":"10.1016\/S1366-2120(08)70014-X"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-40593-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-40593-8","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-40593-8.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,17]],"date-time":"2022-12-17T07:27:19Z","timestamp":1671262039000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-019-40593-8"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,3,11]]},"references-count":71,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2019,12]]}},"alternative-id":["40593"],"URL":"https:\/\/doi.org\/10.1038\/s41598-019-40593-8","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,3,11]]},"assertion":[{"value":"1 June 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 February 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 March 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"4047"}}