{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T18:51:01Z","timestamp":1791399061011,"version":"4.3.3"},"reference-count":54,"publisher":"American Association for the Advancement of Science (AAAS)","issue":"41","funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R01-GM74108"],"award-info":[{"award-number":["R01-GM74108"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000011","name":"Howard Hughes Medical Institute","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100000011","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100001021","name":"Damon Runyon Cancer Research Foundation","doi-asserted-by":"publisher","award":["DRG 2438-21"],"award-info":[{"award-number":["DRG 2438-21"]}],"id":[{"id":"10.13039\/100001021","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100020595","name":"National Science and Technology Council","doi-asserted-by":"publisher","award":["NSTC 115-2311-B-001 -002 -MY3"],"award-info":[{"award-number":["NSTC 115-2311-B-001 -002 -MY3"]}],"id":[{"id":"10.13039\/100020595","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001869","name":"Academia Sinica","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001869","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.science.org"],"crossmark-restriction":true},"short-container-title":["Sci. Adv."],"published-print":{"date-parts":[[2026,10,9]]},"abstract":"<jats:p>\n                    Many animal species replace histones with protamines during spermatogenesis. Although essential for sperm function, protamines evolve rapidly for reasons that remain unknown. Using in vivo gene replacement, we examined the causes and consequences of the rapid evolution of\n                    <jats:italic toggle=\"yes\">Mst77F<\/jats:italic>\n                    , a protamine essential for male fertility in\n                    <jats:italic toggle=\"yes\">Drosophila melanogaster<\/jats:italic>\n                    (\n                    <jats:italic toggle=\"yes\">D. melanogaster<\/jats:italic>\n                    ). Replacing\n                    <jats:italic toggle=\"yes\">Mst77F<\/jats:italic>\n                    with divergent orthologs caused DNA compaction defects in X-bearing sperm, resulting in fewer mature X-bearing sperm and male-biased progeny. Reducing\n                    <jats:italic toggle=\"yes\">D. melanogaster Mst77F<\/jats:italic>\n                    dosage caused the same bias, whereas increasing the dosage of\n                    <jats:italic toggle=\"yes\">Mst77F<\/jats:italic>\n                    orthologs rescued it. Engineered sex chromosome fusions revealed that\n                    <jats:italic toggle=\"yes\">Mst77F<\/jats:italic>\n                    protects the\n                    <jats:italic toggle=\"yes\">D. melanogaster<\/jats:italic>\n                    X chromosome from a killer-target meiotic drive system in a dosage- and sequence-dependent manner. Unlike in\n                    <jats:italic toggle=\"yes\">D. melanogaster<\/jats:italic>\n                    ,\n                    <jats:italic toggle=\"yes\">Mst77F<\/jats:italic>\n                    was dispensable for fertility in\n                    <jats:italic toggle=\"yes\">Drosophila yakuba<\/jats:italic>\n                    (\n                    <jats:italic toggle=\"yes\">D. yakuba<\/jats:italic>\n                    ) but remained important for suppressing sex ratio distortion. Our findings show that relentless pressure to suppress sex chromosome meiotic drive underlies the rapid evolution of protamines.\n                  <\/jats:p>","DOI":"10.1126\/sciadv.aeb5514","type":"journal-article","created":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T17:58:33Z","timestamp":1791395913000},"update-policy":"https:\/\/doi.org\/10.34133\/aaas_crossmark","source":"Crossref","is-referenced-by-count":0,"title":["Rapid protamine evolution suppresses meiotic drive in\n                    <i>Drosophila<\/i>"],"prefix":"10.1126","volume":"12","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9361-1190","authenticated-orcid":true,"given":"Ching-Ho","family":"Chang","sequence":"first","affiliation":[{"name":"Division of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."},{"name":"Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan."},{"name":"Molecular and Cell Biology, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan."},{"name":"Graduate Institute of Life Sciences, National Defense Medical Center, Taipei, Taiwan."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aida Flor","family":"A. de la Cruz","sequence":"additional","affiliation":[{"name":"Division of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."},{"name":"Howard Hughes Medical Institute, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hung-Yu","family":"Lai","sequence":"additional","affiliation":[{"name":"Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabel","family":"Mejia Natividad","sequence":"additional","affiliation":[{"name":"Division of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."},{"name":"Howard Hughes Medical Institute, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-5879-8950","authenticated-orcid":true,"given":"Alex","family":"Noyola","sequence":"additional","affiliation":[{"name":"Division of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6352-8863","authenticated-orcid":true,"given":"Elian","family":"Angelo Magsino Abellanosa","sequence":"additional","affiliation":[{"name":"Institute of Molecular Biology, Academia Sinica, Taipei, Taiwan."},{"name":"Molecular and Cell Biology, Taiwan International Graduate Program, Academia Sinica, Taipei, Taiwan."},{"name":"Graduate Institute of Life Sciences, National Defense Medical Center, Taipei, Taiwan."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-9906-6363","authenticated-orcid":true,"given":"Nicolas D.","family":"Lee","sequence":"additional","affiliation":[{"name":"Division of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."},{"name":"Howard Hughes Medical Institute, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6005-0016","authenticated-orcid":true,"given":"Harmit S.","family":"Malik","sequence":"additional","affiliation":[{"name":"Division of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."},{"name":"Howard Hughes Medical Institute, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"221","reference":[{"key":"e_1_3_2_2_2","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.244749"},{"key":"e_1_3_2_3_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.85249"},{"key":"e_1_3_2_4_2","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2007-8-9-227"},{"key":"e_1_3_2_5_2","doi-asserted-by":"publisher","DOI":"10.1007\/978-3-319-92486-1_2"},{"key":"e_1_3_2_6_2","doi-asserted-by":"publisher","DOI":"10.1002\/bies.200900050"},{"key":"e_1_3_2_7_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1742-4658.2006.05461.x"},{"key":"e_1_3_2_8_2","doi-asserted-by":"publisher","DOI":"10.1086\/BBLv224n3p127"},{"key":"e_1_3_2_9_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejcb.2014.10.005"},{"key":"e_1_3_2_10_2","doi-asserted-by":"publisher","DOI":"10.1093\/gbe\/evae260"},{"key":"e_1_3_2_11_2","first-page":"20133359","article-title":"Sexual selection on protamine and transition nuclear protein expression in mouse species","volume":"281","author":"L\u00fcke L.","year":"2014","unstructured":"L. L\u00fcke, P. Campbell, M. Varea S\u00e1nchez, M. W. Nachman, E. R. Roldan, Sexual selection on protamine and transition nuclear protein expression in mouse species. Proc. Biol. Sci. 281, 20133359 (2014).","journal-title":"Proc. Biol. Sci."},{"key":"e_1_3_2_12_2","doi-asserted-by":"publisher","DOI":"10.1038\/35002070"},{"key":"e_1_3_2_13_2","doi-asserted-by":"publisher","DOI":"10.1093\/evolut\/qpae146"},{"key":"e_1_3_2_14_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature18005"},{"key":"e_1_3_2_15_2","doi-asserted-by":"publisher","DOI":"10.1095\/biolreprod.102.015115"},{"key":"e_1_3_2_16_2","doi-asserted-by":"publisher","DOI":"10.1038\/ng0501-82"},{"key":"e_1_3_2_17_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41594-023-01033-4"},{"key":"e_1_3_2_18_2","doi-asserted-by":"publisher","DOI":"10.1038\/35002236"},{"key":"e_1_3_2_19_2","doi-asserted-by":"publisher","DOI":"10.1186\/s12862-016-0588-1"},{"key":"e_1_3_2_20_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msv209"},{"key":"e_1_3_2_21_2","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.molbev.a026307"},{"key":"e_1_3_2_22_2","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.25.14.6165-6177.2005"},{"key":"e_1_3_2_23_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.celrep.2015.11.023"},{"key":"e_1_3_2_24_2","doi-asserted-by":"publisher","DOI":"10.1534\/genetics.115.182436"},{"key":"e_1_3_2_25_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.adh0037"},{"key":"e_1_3_2_26_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-021-01592-z"},{"key":"e_1_3_2_27_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41559-021-01543-8"},{"key":"e_1_3_2_28_2","doi-asserted-by":"publisher","DOI":"10.1534\/g3.115.017277"},{"key":"e_1_3_2_29_2","doi-asserted-by":"publisher","DOI":"10.3390\/genes12111815"},{"key":"e_1_3_2_30_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2220576120"},{"key":"e_1_3_2_31_2","doi-asserted-by":"crossref","unstructured":"R. A. Fisher \u201cChapter 6: Sexual reproduction and sexual selection \u00a7 natural selection and the sex-ratio \u201d in The Genetical Theory of Natural Selection (Clarendon Press 1930) pp. 141.","DOI":"10.5962\/bhl.title.27468"},{"key":"e_1_3_2_32_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.156.3774.477"},{"key":"e_1_3_2_33_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-023-38357-0"},{"key":"e_1_3_2_34_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejcb.2009.09.001"},{"key":"e_1_3_2_35_2","doi-asserted-by":"publisher","DOI":"10.1098\/rsob.160207"},{"key":"e_1_3_2_36_2","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msx116"},{"key":"e_1_3_2_37_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.1001434"},{"key":"e_1_3_2_38_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.71279"},{"key":"e_1_3_2_39_2","doi-asserted-by":"publisher","DOI":"10.1534\/g3.120.401307"},{"key":"e_1_3_2_40_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1009662"},{"key":"e_1_3_2_41_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.26033"},{"key":"e_1_3_2_42_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pbio.3003182"},{"key":"e_1_3_2_43_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.aan0621"},{"key":"e_1_3_2_44_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2408618121"},{"key":"e_1_3_2_45_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-023-43015-6"},{"key":"e_1_3_2_46_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev.ge.14.120180.001005"},{"key":"e_1_3_2_47_2","doi-asserted-by":"publisher","DOI":"10.1038\/nature06341"},{"key":"e_1_3_2_48_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-025-68254-7"},{"key":"e_1_3_2_49_2","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-genet-071719-020301"},{"key":"e_1_3_2_50_2","doi-asserted-by":"publisher","DOI":"10.1534\/g3.116.038885"},{"key":"e_1_3_2_51_2","first-page":"52288","article-title":"Simple method for fluorescence DNA in situ hybridization to squashed chromosomes","volume":"6","author":"Larracuente A. M.","year":"2015","unstructured":"A. M. Larracuente, P. M. Ferree, Simple method for fluorescence DNA in situ hybridization to squashed chromosomes. J. Vis. Exp. 6, 52288 (2015).","journal-title":"J. Vis. Exp."},{"key":"e_1_3_2_52_2","doi-asserted-by":"publisher","DOI":"10.1264\/jsme2.ME20062"},{"key":"e_1_3_2_53_2","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.4197"},{"key":"e_1_3_2_54_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1009655"},{"key":"e_1_3_2_55_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkv015"}],"container-title":["Science Advances"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.science.org\/doi\/pdf\/10.1126\/sciadv.aeb5514","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T18:01:26Z","timestamp":1791396086000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.science.org\/doi\/10.1126\/sciadv.aeb5514"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,10,9]]},"references-count":54,"journal-issue":{"issue":"41","published-print":{"date-parts":[[2026,10,9]]}},"alternative-id":["10.1126\/sciadv.aeb5514"],"URL":"https:\/\/doi.org\/10.1126\/sciadv.aeb5514","relation":{},"ISSN":["2375-2548"],"issn-type":[{"value":"2375-2548","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,10,9]]},"assertion":[{"value":"2025-08-18","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-01","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-10-07","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"eaeb5514"}}