{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,18]],"date-time":"2026-04-18T02:07:53Z","timestamp":1776478073068,"version":"3.51.2"},"reference-count":73,"publisher":"Proceedings of the National Academy of Sciences","issue":"15","license":[{"start":{"date-parts":[[2024,4,1]],"date-time":"2024-04-01T00:00:00Z","timestamp":1711929600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["DEB-1655683"],"award-info":[{"award-number":["DEB-1655683"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000011","name":"Howard Hughes Medical Institute","doi-asserted-by":"publisher","award":["NA"],"award-info":[{"award-number":["NA"]}],"id":[{"id":"10.13039\/100000011","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"Deutsche Forschungsgemeinschaft","doi-asserted-by":"publisher","award":["WO 1426\/2-1"],"award-info":[{"award-number":["WO 1426\/2-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2024,4,9]]},"abstract":"<jats:p>Genomes are typically mosaics of regions with different evolutionary histories. When speciation events are closely spaced in time, recombination makes the regions sharing the same history small, and the evolutionary history changes rapidly as we move along the genome. When examining rapid radiations such as the early diversification of Neoaves 66 Mya, typically no consistent history is observed across segments exceeding kilobases of the genome. Here, we report an exception. We found that a 21-Mb region in avian genomes, mapped to chicken chromosome 4, shows an extremely strong and discordance-free signal for a history different from that of the inferred species tree. Such a strong discordance-free signal, indicative of suppressed recombination across many millions of base pairs, is not observed elsewhere in the genome for any deep avian relationships. Although long regions with suppressed recombination have been documented in recently diverged species, our results pertain to relationships dating circa 65 Mya. We provide evidence that this strong signal may be due to an ancient rearrangement that blocked recombination and remained polymorphic for several million years prior to fixation. We show that the presence of this region has misled previous phylogenomic efforts with lower taxon sampling, showing the interplay between taxon and locus sampling. We predict that similar ancient rearrangements may confound phylogenetic analyses in other clades, pointing to a need for new analytical models that incorporate the possibility of such events.<\/jats:p>","DOI":"10.1073\/pnas.2319506121","type":"journal-article","created":{"date-parts":[[2024,4,1]],"date-time":"2024-04-01T19:04:10Z","timestamp":1711998250000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":34,"title":["A region of suppressed recombination misleads neoavian phylogenomics"],"prefix":"10.1073","volume":"121","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-5410-1518","authenticated-orcid":false,"given":"Siavash","family":"Mirarab","sequence":"first","affiliation":[{"name":"Electrical and Computer Engineering Department, University of California, San Diego, CA 95032"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0515-0628","authenticated-orcid":false,"given":"Iker","family":"Rivas-Gonz\u00e1lez","sequence":"additional","affiliation":[{"name":"Bioinformatics Research Centre, Aarhus University, Aarhus 8000, Denmark"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2462-7348","authenticated-orcid":false,"given":"Shaohong","family":"Feng","sequence":"additional","affiliation":[{"name":"Center for Evolutionary &amp; Organismal Biology, Zhejiang University School of Medicine, Hangzhou 310058, China"},{"name":"Liangzhu Laboratory, Zhejiang University, Hangzhou 311121, China"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6009-9581","authenticated-orcid":false,"given":"Josefin","family":"Stiller","sequence":"additional","affiliation":[{"name":"Section for Ecology &amp; Evolution, Department of Biology, University of Copenhagen, K\u00f8benhavn 2100, Denmark"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9181-8689","authenticated-orcid":false,"given":"Qi","family":"Fang","sequence":"additional","affiliation":[{"name":"BGI-Research, Shenzhen 518083, China"}]},{"given":"Uyen","family":"Mai","sequence":"additional","affiliation":[{"name":"Electrical and Computer Engineering Department, University of California, San Diego, CA 95032"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2280-9404","authenticated-orcid":false,"given":"Glenn","family":"Hickey","sequence":"additional","affiliation":[{"name":"Genomics Institute, University of California, Santa Cruz, CA 96064"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9441-1155","authenticated-orcid":false,"given":"Guangji","family":"Chen","sequence":"additional","affiliation":[{"name":"Center for Evolutionary &amp; Organismal Biology, Zhejiang University School of Medicine, Hangzhou 310058, China"},{"name":"Liangzhu Laboratory, Zhejiang University, Hangzhou 311121, China"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-6639-8791","authenticated-orcid":false,"given":"Nadolina","family":"Brajuka","sequence":"additional","affiliation":[{"name":"Vertebrate Genome Lab, Rockefeller University, New York, NY 10065"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6450-7551","authenticated-orcid":false,"given":"Olivier","family":"Fedrigo","sequence":"additional","affiliation":[{"name":"Vertebrate Genome Lab, Rockefeller University, New York, NY 10065"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7554-5991","authenticated-orcid":false,"given":"Giulio","family":"Formenti","sequence":"additional","affiliation":[{"name":"Vertebrate Genome Lab, Rockefeller University, New York, NY 10065"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2958-5183","authenticated-orcid":false,"given":"Jochen B. W.","family":"Wolf","sequence":"additional","affiliation":[{"name":"Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximillians-Universit\u00e4t, Munich 82152, Germany"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2237-513X","authenticated-orcid":false,"given":"Kerstin","family":"Howe","sequence":"additional","affiliation":[{"name":"Tree of Life Division, Wellcome Sanger Institute, Cambridge CB10 1RQ, United Kingdom"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1328-1732","authenticated-orcid":false,"given":"Agostinho","family":"Antunes","sequence":"additional","affiliation":[{"name":"Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Porto 4099-002, Portugal"},{"name":"Department of Biology, Faculty of Sciences, University of Porto, Porto 4099-002, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5028-1790","authenticated-orcid":false,"given":"Mikkel H.","family":"Schierup","sequence":"additional","affiliation":[{"name":"Bioinformatics Research Centre, Aarhus University, Aarhus 8000, Denmark"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8863-3539","authenticated-orcid":false,"given":"Benedict","family":"Paten","sequence":"additional","affiliation":[{"name":"Genomics Institute, University of California, Santa Cruz, CA 96064"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8931-5049","authenticated-orcid":false,"given":"Erich D.","family":"Jarvis","sequence":"additional","affiliation":[{"name":"Vertebrate Genome Lab, Rockefeller University, New York, NY 10065"}]},{"given":"Guojie","family":"Zhang","sequence":"additional","affiliation":[{"name":"Center for Evolutionary &amp; Organismal Biology, Zhejiang University School of Medicine, Hangzhou 310058, China"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1643-5212","authenticated-orcid":false,"given":"Edward L.","family":"Braun","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Florida, Gainesville, FL 32611"}]}],"member":"341","published-online":{"date-parts":[[2024,4]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/46.3.523"},{"key":"e_1_3_4_2_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1558-5646.2008.00549.x"},{"key":"e_1_3_4_3_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature02053"},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1250463"},{"key":"e_1_3_4_5_2","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/syx041"},{"key":"e_1_3_4_6_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ympev.2014.10.022"},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.0030007"},{"key":"e_1_3_4_8_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tree.2007.01.012"},{"key":"e_1_3_4_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tree.2009.01.009"},{"key":"e_1_3_4_10_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1253451"},{"key":"e_1_3_4_11_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.tig.2013.05.007"},{"key":"e_1_3_4_12_2","first-page":"568","article-title":"Relationships between gene trees and species trees","volume":"5","author":"Pamilo P.","year":"1988","unstructured":"P. Pamilo, M. Nei, Relationships between gene trees and species trees. Mol. Biol. Evol. 5, 568\u2013583 (1988).","journal-title":"Mol. Biol. Evol."},{"key":"e_1_3_4_13_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-ecolsys-012121-095340"},{"key":"e_1_3_4_14_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature11041"},{"key":"e_1_3_4_15_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-018-0717-x"},{"key":"e_1_3_4_16_2","doi-asserted-by":"publisher","DOI":"10.1525\/auk.2011.128.4.620"},{"key":"e_1_3_4_17_2","doi-asserted-by":"publisher","DOI":"10.1006\/tpbi.2001.1568"},{"key":"e_1_3_4_18_2","doi-asserted-by":"publisher","DOI":"10.1101\/gr.101410.109"},{"key":"e_1_3_4_19_2","doi-asserted-by":"publisher","DOI":"10.1093\/gbe\/evu157"},{"key":"e_1_3_4_20_2","doi-asserted-by":"crossref","unstructured":"E. L. Braun J. Cracraft P. Houde \u201cResolving the avian tree of life from top to bottom: The promise and potential boundaries of the phylogenomic era\u201d in Avian Genomics in Ecology and Evolution (Springer International Publishing Cham 2019) pp. 151\u2013210.","DOI":"10.1007\/978-3-030-16477-5_6"},{"key":"e_1_3_4_21_2","unstructured":"J. Stiller et al. Complexity of avian evolution revealed by family-level genomes. Nature (in press) A copy provided for reviewers (2024)."},{"key":"e_1_3_4_22_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1002224"},{"key":"e_1_3_4_23_2","doi-asserted-by":"publisher","DOI":"10.3390\/d12040164"},{"key":"e_1_3_4_24_2","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/syq100"},{"key":"e_1_3_4_25_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature15697"},{"key":"e_1_3_4_26_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msaa191"},{"key":"e_1_3_4_27_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.avrs.2022.100027"},{"key":"e_1_3_4_28_2","doi-asserted-by":"publisher","DOI":"10.3390\/birds2010001"},{"key":"e_1_3_4_29_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ympev.2018.03.033"},{"key":"e_1_3_4_30_2","doi-asserted-by":"publisher","DOI":"10.1080\/10635150600697358"},{"key":"e_1_3_4_31_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-021-03451-0"},{"key":"e_1_3_4_32_2","doi-asserted-by":"publisher","DOI":"10.1109\/TCBB.2017.2757930"},{"key":"e_1_3_4_33_2","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/syv021"},{"key":"e_1_3_4_34_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1157704"},{"key":"e_1_3_4_35_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ympev.2013.05.029"},{"key":"e_1_3_4_36_2","doi-asserted-by":"publisher","DOI":"10.1101\/gr.103663.109"},{"key":"e_1_3_4_37_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msab277"},{"key":"e_1_3_4_38_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1002660"},{"key":"e_1_3_4_39_2","doi-asserted-by":"publisher","DOI":"10.1111\/mec.12415"},{"key":"e_1_3_4_40_2","doi-asserted-by":"publisher","DOI":"10.1038\/sj.gene.6364336"},{"key":"e_1_3_4_41_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1365-294X.2012.05501.x"},{"key":"e_1_3_4_42_2","doi-asserted-by":"crossref","unstructured":"X. Shen C. T. Hittinger A. Rokas Contentious relationships in phylogenomic studies can be driven by a handful of genes. Nat. Ecol. Evol. 1 0126 (2017).","DOI":"10.1038\/s41559-017-0126"},{"key":"e_1_3_4_43_2","unstructured":"E. B. Ford Genetic Polymorphism (1965)."},{"key":"e_1_3_4_44_2","doi-asserted-by":"publisher","DOI":"10.1038\/hdy.2014.20"},{"key":"e_1_3_4_45_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2015.11.069"},{"key":"e_1_3_4_46_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature11832"},{"key":"e_1_3_4_47_2","doi-asserted-by":"publisher","DOI":"10.1038\/ng.3443"},{"key":"e_1_3_4_48_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-022-01661-x"},{"key":"e_1_3_4_49_2","doi-asserted-by":"publisher","DOI":"10.1534\/genetics.105.047985"},{"key":"e_1_3_4_50_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2018.04.072"},{"key":"e_1_3_4_51_2","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2007-8-11-r236"},{"key":"e_1_3_4_52_2","doi-asserted-by":"publisher","DOI":"10.1093\/genetics\/53.2.327"},{"key":"e_1_3_4_53_2","doi-asserted-by":"publisher","DOI":"10.1093\/sysbio\/28.1.49"},{"key":"e_1_3_4_54_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msw079"},{"key":"e_1_3_4_55_2","doi-asserted-by":"publisher","DOI":"10.3390\/genes9030132"},{"key":"e_1_3_4_56_2","doi-asserted-by":"publisher","DOI":"10.1534\/genetics.109.103010"},{"key":"e_1_3_4_57_2","unstructured":"I. Rivas-Gonz\u00e1lez rivasiker\/autocoalhmm: v1.0.0 (2022)."},{"key":"e_1_3_4_58_2","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate: A practical and powerful approach to multiple testing","volume":"57","author":"Benjamini Y.","year":"1995","unstructured":"Y. Benjamini, Y. Hochberg, Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. 57, 289\u2013300 (1995).","journal-title":"J. R. Stat. Soc."},{"key":"e_1_3_4_59_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41586-020-2871-y"},{"key":"e_1_3_4_60_2","doi-asserted-by":"crossref","unstructured":"S. D. Goenka Y. Turakhia B. Paten M. Horowitz \u201cSegAlign: A scalable GPU-based whole genome aligner\u201d in SC20: International Conference for High Performance Computing Networking Storage and Analysis (IEEE Atlanta GA USA 2020) pp. 1\u201313.","DOI":"10.1109\/SC41405.2020.00043"},{"key":"e_1_3_4_61_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btt128"},{"key":"e_1_3_4_62_2","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btv646"},{"key":"e_1_3_4_63_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/mst010"},{"key":"e_1_3_4_64_2","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a026334"},{"key":"e_1_3_4_65_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msaa015"},{"key":"e_1_3_4_66_2","doi-asserted-by":"publisher","DOI":"10.12688\/wellcomeopenres.17060.1"},{"key":"e_1_3_4_67_2","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-15-53"},{"key":"e_1_3_4_68_2","doi-asserted-by":"publisher","DOI":"10.1101\/gr.236273.118"},{"key":"e_1_3_4_69_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msm088"},{"key":"e_1_3_4_70_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkad347"},{"key":"e_1_3_4_71_2","doi-asserted-by":"publisher","DOI":"10.1089\/omi.2011.0118"},{"key":"e_1_3_4_72_2","unstructured":"J. Stiller . Raw data for Mirarab et al. 2024 in PNAS: \"A region of suppressed recombination misleads neoavian phylogenomics\". FigShare. https:\/\/doi.org\/10.6084\/m9.figshare.25285408.v1. Deposited 25 February 2024."},{"key":"e_1_3_4_73_2","unstructured":"S. Mirarab et al. Data and analyses from Mirarab et al PNAS 2024 paper. Zenodo. https:\/\/zenodo.org\/doi\/10.5281\/zenodo.10699423. Deposited 23 February 2024."}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.2319506121","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,11,15]],"date-time":"2024-11-15T12:27:17Z","timestamp":1731673637000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/10.1073\/pnas.2319506121"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,4]]},"references-count":73,"journal-issue":{"issue":"15","published-print":{"date-parts":[[2024,4,9]]}},"alternative-id":["10.1073\/pnas.2319506121"],"URL":"https:\/\/doi.org\/10.1073\/pnas.2319506121","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,4]]},"assertion":[{"value":"2023-11-14","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-02-07","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2024-04-01","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e2319506121"}}