{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,8]],"date-time":"2026-09-08T23:49:47Z","timestamp":1788911387671,"version":"build-2803163510"},"reference-count":30,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2020,1,23]],"date-time":"2020-01-23T00:00:00Z","timestamp":1579737600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2020,1,23]],"date-time":"2020-01-23T00:00:00Z","timestamp":1579737600000},"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>All songbirds studied to date have an additional Germline Restricted Chromosome (GRC), which is not present in somatic cells. GRCs show a wide variation in genetic content and little homology between species. To check how this divergence affected the meiotic behavior of the GRC, we examined synapsis, recombination and copy number variation for GRCs in the closely related sand and pale martins (<jats:italic>Riparia riparia<\/jats:italic> and <jats:italic>R. diluta<\/jats:italic>) in comparison with distantly related estrildid finches. Using immunolocalization of meiotic proteins and FISH with GRC-specific DNA probes, we found a striking similarity in the meiotic behavior of GRCs between martins and estrildid finches despite the millions of years of independent evolution. GRCs are usually present in two copies in female and in one copy in male pachytene cells. However, we detected polymorphism in female and mosaicism in male martins for the number of GRCs. In martin and zebra finch females, two GRCs synapse along their whole length, but recombine predominately at their ends. We suggest that the shared features of the meiotic behavior of GRCs have been supported by natural selection in favor of a preferential segregation of GRCs to the eggs.<\/jats:p>","DOI":"10.1038\/s41598-020-58032-4","type":"journal-article","created":{"date-parts":[[2020,1,23]],"date-time":"2020-01-23T11:02:58Z","timestamp":1579777378000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":34,"title":["Germline-restricted chromosome (GRC) in the sand martin and the pale martin (Hirundinidae, Aves): synapsis, recombination and copy number variation"],"prefix":"10.1038","volume":"10","author":[{"given":"Lyubov P.","family":"Malinovskaya","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kira S.","family":"Zadesenets","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tatyana V.","family":"Karamysheva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ekaterina A.","family":"Akberdina","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena A.","family":"Kizilova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Margarita V.","family":"Romanenko","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elena P.","family":"Shnaider","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariya M.","family":"Scherbakova","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Igor G.","family":"Korobitsyn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nikolai B.","family":"Rubtsov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pavel M.","family":"Borodin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8933-8336","authenticated-orcid":false,"given":"Anna A.","family":"Torgasheva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2020,1,23]]},"reference":[{"key":"58032_CR1","doi-asserted-by":"crossref","first-page":"1570","DOI":"10.1073\/pnas.1906803116","volume":"116","author":"B Hansson","year":"2019","unstructured":"Hansson, B. On the origin and evolution of germline chromosomes in songbirds. Proc. Natl. Acad. Sci. 116, 1570\u20131572 (2019).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"58032_CR2","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1023\/A:1009234912307","volume":"6","author":"MI Pigozzi","year":"1998","unstructured":"Pigozzi, M. I. & Solari, A. J. Germ cell restriction and regular transmission of an accessory chromosome that mimics a sex body in the zebra finch. Taeniopygia guttata. Chromosom. Res. 6, 105\u2013113 (1998).","journal-title":"Taeniopygia guttata. Chromosom. Res."},{"key":"58032_CR3","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1007\/s00412-005-0025-5","volume":"114","author":"MI Pigozzi","year":"2005","unstructured":"Pigozzi, M. I. & Solari, A. J. The germ-line-restricted chromosome in the zebra finch: Recombination in females and elimination in males. Chromosoma 114, 403\u2013409 (2005).","journal-title":"Chromosoma"},{"key":"58032_CR4","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1007\/s00412-014-0451-3","volume":"123","author":"L del Priore","year":"2014","unstructured":"del Priore, L. & Pigozzi, M. I. Histone modifications related to chromosome silencing and elimination during male meiosis in Bengalese finch. Chromosoma 123, 293\u2013302 (2014).","journal-title":"Chromosoma"},{"key":"58032_CR5","doi-asserted-by":"crossref","first-page":"11845","DOI":"10.1073\/pnas.1817373116","volume":"116","author":"AA Torgasheva","year":"2019","unstructured":"Torgasheva, A. A. et al. Germline-restricted chromosome (GRC) is widespread among songbirds. Proc. Natl. Acad. Sci. USA 116, 11845\u201311850 (2019).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"58032_CR6","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-13427-4","volume":"10","author":"CM Kinsella","year":"2019","unstructured":"Kinsella, C. M. et al. Programmed DNA elimination of germline development genes in songbirds. Nat. Commun. 10, 5468 (2019).","journal-title":"Nat. Commun."},{"key":"58032_CR7","doi-asserted-by":"publisher","first-page":"1620","DOI":"10.1016\/j.cub.2018.03.067","volume":"28","author":"MK Biederman","year":"2018","unstructured":"Biederman, M. K. et al. Discovery of the first germline-restricted gene by subtractive transcriptomic analysis in the zebra finch, Taeniopygia guttata. Curr. Biol. 28, 1620\u20131627 (2018).","journal-title":"Curr. Biol."},{"issue":"7","key":"58032_CR8","doi-asserted-by":"publisher","first-page":"1812","DOI":"10.1093\/molbev\/msx116","volume":"34","author":"S Kumar","year":"2017","unstructured":"Kumar, S., Stecher, G., Suleski, M. & Hedges, S. B. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34(7), 1812\u20131819 (2017).","journal-title":"Mol. Biol. Evol."},{"key":"58032_CR9","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/j.ympev.2008.03.030","volume":"48","author":"A Pavlova","year":"2008","unstructured":"Pavlova, A., Zink, R. M., Drovetski, S. V. & Rohwer, S. Pleistocene evolution of closely related sand martins Riparia riparia and R. diluta. Mol. Phylogenet. Evol. 48, 61\u201373 (2008).","journal-title":"Mol. Phylogenet. Evol."},{"key":"58032_CR10","first-page":"321","volume":"9","author":"Q-W Li","year":"1988","unstructured":"Li, Q.-W. & Bian, X.-Z. Studies on the karyotypes of birds II. The 19 species of 12 families of passerine birds (Passeriformes, Aves). Zool. Res. 9, 321\u2013326 (1988).","journal-title":"Zool. Res."},{"key":"58032_CR11","doi-asserted-by":"publisher","first-page":"311","DOI":"10.1007\/s00412-010-0258-9","volume":"119","author":"S Schoenmakers","year":"2010","unstructured":"Schoenmakers, S., Wassenaar, E., Laven, J. S. E., Grootegoed, J. A. & Baarends, W. M. Meiotic silencing and fragmentation of the male germline restricted chromosome in zebra finch. Chromosoma 119, 311\u2013324 (2010).","journal-title":"Chromosoma"},{"key":"58032_CR12","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1242\/jcs.65.1.249","volume":"65","author":"P Goetz","year":"1984","unstructured":"Goetz, P., Chandley, A. C. & Speed, R. M. Morphological and temporal sequence of meiotic prophase development at puberty in the male mouse. J. Cell Sci. 65, 249\u2013263 (1984).","journal-title":"J. Cell Sci."},{"key":"58032_CR13","doi-asserted-by":"publisher","first-page":"791","DOI":"10.1002\/bies.201600025","volume":"38","author":"F Bertocchini","year":"2016","unstructured":"Bertocchini, F. & Chuva de Sousa Lopes, S. M. Germline development in amniotes: A paradigm shift in primordial germ cell specification. BioEssays 38, 791\u2013800 (2016).","journal-title":"BioEssays"},{"key":"58032_CR14","doi-asserted-by":"publisher","first-page":"1675","DOI":"10.1098\/rstb.2007.0006","volume":"363","author":"J Rutkowska","year":"2008","unstructured":"Rutkowska, J. & Badyaev, A. V. Meiotic drive and sex determination: molecular and cytological mechanisms of sex ratio adjustment in birds. Philos. Trans. R. Soc. London B Biol. Sci. 363, 1675\u20131686 (2008).","journal-title":"Philos. Trans. R. Soc. London B Biol. Sci."},{"key":"58032_CR15","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":"58032_CR16","doi-asserted-by":"publisher","first-page":"210","DOI":"10.3389\/fpls.2017.00210","volume":"8","author":"A Houben","year":"2017","unstructured":"Houben, A. B chromosomes \u2013 a matter of chromosome drive. Front. Plant Sci. 8, 210 (2017).","journal-title":"Front. Plant Sci."},{"key":"58032_CR17","doi-asserted-by":"crossref","first-page":"1179","DOI":"10.1093\/genetics\/159.3.1179","volume":"159","author":"FPM De Villena","year":"2001","unstructured":"De Villena, F. P. M. & Sapienza, C. Female meiosis drives karyotypic evolution in mammals. Genetics 159, 1179\u20131189 (2001).","journal-title":"Genetics"},{"key":"58032_CR18","doi-asserted-by":"crossref","unstructured":"Camacho, J. P. M., Chromosomes, B. In The Evolution of the Genome (ed. Gregory, T.R.) 223\u2013286 223\u2013286 (Elsevier, San Diego, 2005).","DOI":"10.1016\/B978-012301463-4\/50006-1"},{"key":"58032_CR19","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1042\/BST0340569","volume":"34","author":"HS Malik","year":"2006","unstructured":"Malik, H. S. & Bayes, J. J. Genetic conflicts during meiosis and the evolutionary origins of centromere complexity. Biochem. Soc. Trans. 34, 569\u2013573 (2006).","journal-title":"Biochem. Soc. Trans."},{"key":"58032_CR20","doi-asserted-by":"publisher","DOI":"10.1186\/jbiol11","volume":"3","author":"PB Talbert","year":"2004","unstructured":"Talbert, P. B., Bryson, T. D. & Henikoff, S. Adaptive evolution of centromere proteins in plants and animals. J. Biol. 3, 18 (2004).","journal-title":"J. Biol."},{"key":"58032_CR21","doi-asserted-by":"publisher","first-page":"885","DOI":"10.1016\/0092-8674(91)90313-N","volume":"64","author":"ATC Carpenter","year":"1991","unstructured":"Carpenter, A. T. C. Distributive segregation: motors in the polar wind? Cell 64, 885\u2013890 (1991).","journal-title":"Cell"},{"key":"58032_CR22","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":"58032_CR23","doi-asserted-by":"publisher","first-page":"280","DOI":"10.1038\/35066065","volume":"2","author":"T Hassold","year":"2001","unstructured":"Hassold, T. & Hunt, P. To err (meiotically) is human: the genesis of human aneuploidy. Nat. Rev. Genet. 2, 280\u2013291 (2001).","journal-title":"Nat. Rev. Genet."},{"key":"58032_CR24","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1093\/genetics\/139.3.1159","volume":"139","author":"DD Sears","year":"1995","unstructured":"Sears, D. D., Hegemann, J. H., Shero, J. H. & Hieter, P. Cis-acting determinants affecting centromere function, sister-chromatid cohesion and reciprocal recombination during meiosis in Saccharomyces cerevisiae. Genetics 139, 1159\u20131173 (1995).","journal-title":"Genetics"},{"key":"58032_CR25","doi-asserted-by":"publisher","first-page":"e312","DOI":"10.1371\/journal.pbio.0020312","volume":"2","author":"PDN Hebert","year":"2004","unstructured":"Hebert, P. D. N., Stoeckle, M. Y., Zemlak, T. S. & Francis, C. M. Identification of birds through DNA barcodes. PLOS Biol. 2, e312 (2004).","journal-title":"PLOS Biol."},{"key":"58032_CR26","doi-asserted-by":"crossref","unstructured":"Ratnasingham, S. & Hebert, P. D. N. bold: The Barcode of Life Data System (http:\/\/www.barcodinglife.org). Mol. Ecol. Notes 7, 355\u2013364 (2007).","DOI":"10.1111\/j.1471-8286.2007.01678.x"},{"key":"58032_CR27","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1023\/A:1018445520117","volume":"5","author":"AHFM Peters","year":"1997","unstructured":"Peters, A. H. F. M., Plug, A. W., Van Vugt, M. J. & De Boer, P. A drying-down technique for the spreading of mammalian meiocytes from the male and female germline. Chromosom. Res. 5, 66\u201368 (1997).","journal-title":"Chromosom. Res."},{"key":"58032_CR28","doi-asserted-by":"publisher","first-page":"1014","DOI":"10.1007\/BF01953855","volume":"36","author":"WM Howell","year":"1980","unstructured":"Howell, W. M. & Black, D. A. Controlled silver-staining of nucleolus organizer regions with a protective colloidal developer: a 1-step method. Experientia 36, 1014\u20131015 (1980).","journal-title":"Experientia"},{"key":"58032_CR29","doi-asserted-by":"crossref","first-page":"1569","DOI":"10.1093\/genetics\/151.4.1569","volume":"151","author":"LK Anderson","year":"1999","unstructured":"Anderson, L. K., Reeves, A., Webb, L. M. & Ashley, T. Distribution of crossing over on mouse synaptonemal complexes using immunofluorescent localization of MLH1 protein. Genetics 151, 1569\u20131579 (1999).","journal-title":"Genetics"},{"key":"58032_CR30","doi-asserted-by":"publisher","first-page":"439","DOI":"10.1139\/g01-037","volume":"44","author":"A Reeves","year":"2001","unstructured":"Reeves, A. MicroMeasure: a new computer program for the collection and analysis of cytogenetic data. Genome 44, 439\u2013443 (2001).","journal-title":"Genome"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-58032-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-58032-4","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-58032-4.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,6]],"date-time":"2022-12-06T06:09:10Z","timestamp":1670306950000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-020-58032-4"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,1,23]]},"references-count":30,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2020,12]]}},"alternative-id":["58032"],"URL":"https:\/\/doi.org\/10.1038\/s41598-020-58032-4","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,1,23]]},"assertion":[{"value":"12 September 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 January 2020","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 January 2020","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"1058"}}