{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,3]],"date-time":"2026-10-03T03:28:25Z","timestamp":1790998105889,"version":"4.1.0"},"reference-count":80,"publisher":"National Academy of Sciences","issue":"9","license":[{"start":{"date-parts":[[2026,2,25]],"date-time":"2026-02-25T00:00:00Z","timestamp":1771977600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007795","name":"Stowers Institute for Medical Research","doi-asserted-by":"publisher","award":["N\/A"],"award-info":[{"award-number":["N\/A"]}],"id":[{"id":"10.13039\/100007795","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100009633","name":"HHS | NIH | Eunice Kennedy Shriver National Institute of Child Health and Human Development","doi-asserted-by":"publisher","award":["HD009019-01"],"award-info":[{"award-number":["HD009019-01"]}],"id":[{"id":"10.13039\/100009633","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003246","name":"Nederlandse Organisatie voor Wetenschappelijk Onderzoek","doi-asserted-by":"publisher","award":["VI.Veni.202.223"],"award-info":[{"award-number":["VI.Veni.202.223"]}],"id":[{"id":"10.13039\/501100003246","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":[[2026,3,3]]},"abstract":"<jats:p>\n                    The goal of meiosis is typically to produce haploid gametes (eggs or sperm). Failure to do so is catastrophic for fertility. However, Lepidopteran (moths and butterflies) males produce two sperm morphs: nucleated (eupyrene) sperm and anucleated (apyrene) sperm, both of which are essential for fertilization. The meiotic differences in the two types of spermatogenesis are unclear, and our knowledge of the molecular differences between eupyrene and apyrene spermatogenesis is extremely limited in all systems. The only factor identified as being required for apyrene spermatogenesis is\n                    <jats:italic toggle=\"yes\">Sex-lethal<\/jats:italic>\n                    (\n                    <jats:italic toggle=\"yes\">Sxl<\/jats:italic>\n                    ). Here, we show through cytological analysis of meiotic events that there are several key differences in the genesis of apyrene and eupyrene sperm. Specifically, during meiosis I, apyrene spermatocytes fail to decondense and pair their chromosomes during meiotic prophase I. Telomeres fail to localize to the nuclear periphery, and full-length synaptonemal complex does not form. We also find evidence of an abnormal second cell division during apyrene meiosis. RNA sequencing of both eupyrene- and apyrene-producing testes reveals distinct changes in transcriptional programs, including down-regulation of a myriad of cell division genes during apyrene meiosis. By comparing wildtype and\n                    <jats:italic toggle=\"yes\">Sxl<\/jats:italic>\n                    -knockout apyrene testes, we found that\n                    <jats:italic toggle=\"yes\">Sxl<\/jats:italic>\n                    is not required for regulating the expression of the cell division genes but instead may play a role in blocking hormone signaling from altering testis cell identity. Together, our findings reveal significant insights into two converging molecular pathways that promote the formation of dimorphic sperm in Lepidoptera.\n                  <\/jats:p>","DOI":"10.1073\/pnas.2520991123","type":"journal-article","created":{"date-parts":[[2026,2,25]],"date-time":"2026-02-25T16:52:02Z","timestamp":1772038322000},"update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":3,"title":["Programmed meiotic errors facilitate dichotomous sperm production in the silkworm,\n                    <i>Bombyx mori<\/i>"],"prefix":"10.1073","volume":"123","author":[{"given":"Leif","family":"Benner","sequence":"first","affiliation":[{"name":"Unit on Chromosome Dynamics, Division of Development Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH","place":["Bethesda"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0006-4500-2570","authenticated-orcid":false,"given":"Makenzie","family":"Richmond","sequence":"additional","affiliation":[{"name":"Stowers Institute for Medical Research","place":["Kansas City"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Youbin","family":"Xiang","sequence":"additional","affiliation":[{"name":"Stowers Institute for Medical Research","place":["Kansas City"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7129-9500","authenticated-orcid":false,"given":"LingSze","family":"Lee","sequence":"additional","affiliation":[{"name":"Unit on Chromosome Dynamics, Division of Development Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH","place":["Bethesda"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Clio B.","family":"Hockens","sequence":"additional","affiliation":[{"name":"Unit on Chromosome Dynamics, Division of Development Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH","place":["Bethesda"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tianwei","family":"Li","sequence":"additional","affiliation":[{"name":"Molecular Genomics Core, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH","place":["Bethesda"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1292-8426","authenticated-orcid":false,"given":"Zulin","family":"Yu","sequence":"additional","affiliation":[{"name":"Stowers Institute for Medical Research","place":["Kansas City"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8385-2775","authenticated-orcid":false,"given":"Dai","family":"Tsuchiya","sequence":"additional","affiliation":[{"name":"Stowers Institute for Medical Research","place":["Kansas City"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shengping","family":"Huang","sequence":"additional","affiliation":[{"name":"Stowers Institute for Medical Research","place":["Kansas City"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3540-7727","authenticated-orcid":false,"given":"Eelco C.","family":"Tromer","sequence":"additional","affiliation":[{"name":"Cell Biochemistry, Groningen Biomolecular Sciences & Biotechnology Institute, Faculty of Science and Engineering, University of Groningen","place":["Linneausborg, Groningen, the Netherlands"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"R. Scott","family":"Hawley","sequence":"additional","affiliation":[{"name":"Stowers Institute for Medical Research","place":["Kansas City"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2489-4016","authenticated-orcid":false,"given":"Leah F.","family":"Rosin","sequence":"additional","affiliation":[{"name":"Unit on Chromosome Dynamics, Division of Development Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, NIH","place":["Bethesda"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2026,2,25]]},"reference":[{"key":"e_1_3_4_1_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02977916"},{"key":"e_1_3_4_2_2","doi-asserted-by":"publisher","DOI":"10.1017\/S0967199402002046"},{"key":"e_1_3_4_3_2","first-page":"206","volume-title":"Advances in Insect Physiology","author":"Friedl\u00e4nder M.","year":"2005","unstructured":"M. Friedl\u00e4nder, R. K. Seth, S. E. Reynolds, \u201cEupyrene and Apyrene Sperm: Dichotomous Spermatogenesis in Lepidoptera\u201d in Advances in Insect Physiology, S. J. Simpson, Ed. (Academic Press, 2005), pp. 206\u2013308."},{"key":"e_1_3_4_4_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1009700"},{"key":"e_1_3_4_5_2","doi-asserted-by":"publisher","DOI":"10.1303\/aez.12.142"},{"key":"e_1_3_4_6_2","doi-asserted-by":"publisher","DOI":"10.1303\/aez.13.91"},{"key":"e_1_3_4_7_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.1051580106"},{"key":"e_1_3_4_8_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF01282550"},{"key":"e_1_3_4_9_2","doi-asserted-by":"publisher","DOI":"10.1002\/1097-4687(200011)246:2<53::AID-JMOR1>3.0.CO;2-P"},{"key":"e_1_3_4_10_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41421-020-00194-6"},{"key":"e_1_3_4_11_2","doi-asserted-by":"publisher","DOI":"10.1016\/0022-1910(84)90030-1"},{"key":"e_1_3_4_12_2","doi-asserted-by":"publisher","DOI":"10.1016\/0022-1910(81)90060-3"},{"key":"e_1_3_4_13_2","doi-asserted-by":"publisher","DOI":"10.1128\/MMBR.67.3.343-359.2003"},{"key":"e_1_3_4_14_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.1820101116"},{"key":"e_1_3_4_15_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.1086605"},{"key":"e_1_3_4_16_2","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a016626"},{"key":"e_1_3_4_17_2","doi-asserted-by":"publisher","DOI":"10.1093\/g3journal\/jkad058"},{"key":"e_1_3_4_18_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-021-26033-0"},{"key":"e_1_3_4_19_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.devcel.2023.10.009"},{"key":"e_1_3_4_20_2","doi-asserted-by":"crossref","unstructured":"G. Cheng High resolution maps of chromatin reorganization through mouse meiosis reveal novel features of the 3D meiotic structure. BioRxiv [Preprint] (2024). https:\/\/doi.org\/10.1101\/2024.03.25.586627 (Accessed 16 September 2025).","DOI":"10.1101\/2024.03.25.586627"},{"key":"e_1_3_4_21_2","doi-asserted-by":"publisher","DOI":"10.1139\/z82-166"},{"key":"e_1_3_4_22_2","first-page":"1","volume-title":"International Review of Cytology","author":"Wolf K. W.","year":"1994","unstructured":"K. W. Wolf, \u201cThe unique structure of lepidopteran spindles\u201d in International Review of Cytology, K. W. Jeon, J. Jarvik, Eds. (Academic Press, 1994), pp. 1\u201348."},{"key":"e_1_3_4_23_2","doi-asserted-by":"publisher","DOI":"10.1093\/aesa\/90.2.223"},{"key":"e_1_3_4_24_2","doi-asserted-by":"publisher","DOI":"10.1007\/s00412-002-0204-6"},{"key":"e_1_3_4_25_2","doi-asserted-by":"publisher","DOI":"10.3390\/genes1030495"},{"key":"e_1_3_4_26_2","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.84138"},{"key":"e_1_3_4_27_2","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.10168"},{"key":"e_1_3_4_28_2","doi-asserted-by":"publisher","DOI":"10.1186\/s12915-024-01916-y"},{"key":"e_1_3_4_29_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1010600"},{"key":"e_1_3_4_30_2","doi-asserted-by":"publisher","DOI":"10.1098\/rsob.240002"},{"key":"e_1_3_4_31_2","doi-asserted-by":"publisher","DOI":"10.1038\/nrg2723"},{"key":"e_1_3_4_32_2","doi-asserted-by":"publisher","DOI":"10.1534\/genetics.117.300081"},{"key":"e_1_3_4_33_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.ceb.2018.01.005"},{"key":"e_1_3_4_34_2","doi-asserted-by":"publisher","DOI":"10.1098\/rstb.1977.0022"},{"key":"e_1_3_4_35_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00293453"},{"key":"e_1_3_4_36_2","doi-asserted-by":"publisher","DOI":"10.3390\/genes13020200"},{"key":"e_1_3_4_37_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1007382"},{"key":"e_1_3_4_38_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1011329"},{"key":"e_1_3_4_39_2","doi-asserted-by":"publisher","DOI":"10.1038\/emboj.2012.90"},{"key":"e_1_3_4_40_2","doi-asserted-by":"publisher","DOI":"10.3389\/fmolb.2024.1366113"},{"key":"e_1_3_4_41_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/25.17.3389"},{"key":"e_1_3_4_42_2","doi-asserted-by":"publisher","DOI":"10.1006\/jmbi.1994.1104"},{"key":"e_1_3_4_43_2","doi-asserted-by":"publisher","DOI":"10.1017\/CBO9780511790492"},{"key":"e_1_3_4_44_2","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gki408"},{"key":"e_1_3_4_45_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2017.12.007"},{"key":"e_1_3_4_46_2","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.2688"},{"key":"e_1_3_4_47_2","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-024-59487-5"},{"key":"e_1_3_4_48_2","doi-asserted-by":"publisher","DOI":"10.1016\/0022-1910(88)90200-4"},{"key":"e_1_3_4_49_2","doi-asserted-by":"publisher","DOI":"10.1016\/0022-1910(94)00125-Z"},{"key":"e_1_3_4_50_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1440-169X.1969.00008.x"},{"key":"e_1_3_4_51_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cbpc.2004.09.009"},{"key":"e_1_3_4_52_2","doi-asserted-by":"publisher","DOI":"10.1073\/pnas.2336088100"},{"key":"e_1_3_4_53_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.276.5309.114"},{"key":"e_1_3_4_54_2","doi-asserted-by":"publisher","DOI":"10.1111\/j.1432-1033.2004.04233.x"},{"key":"e_1_3_4_55_2","doi-asserted-by":"publisher","DOI":"10.1242\/dev.118.3.977"},{"key":"e_1_3_4_56_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00292742"},{"key":"e_1_3_4_57_2","doi-asserted-by":"publisher","DOI":"10.1534\/genetics.108.093112"},{"key":"e_1_3_4_58_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.devcel.2010.11.019"},{"key":"e_1_3_4_59_2","doi-asserted-by":"publisher","DOI":"10.1093\/genetics\/109.3.529"},{"key":"e_1_3_4_60_2","doi-asserted-by":"publisher","DOI":"10.1006\/dbio.1994.1032"},{"key":"e_1_3_4_61_2","doi-asserted-by":"publisher","DOI":"10.1242\/dev.122.12.4065"},{"key":"e_1_3_4_62_2","doi-asserted-by":"publisher","DOI":"10.1038\/ng1232"},{"key":"e_1_3_4_63_2","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.046706"},{"key":"e_1_3_4_64_2","first-page":"88","article-title":"CDK2 regulates nuclear envelope protein dynamics and telomere attachment in mouse meiotic prophase","volume":"128","author":"Viera A.","year":"2015","unstructured":"A. Viera , CDK2 regulates nuclear envelope protein dynamics and telomere attachment in mouse meiotic prophase. J. Cell Sci. 128, 88\u201399 (2015).","journal-title":"J. Cell Sci."},{"key":"e_1_3_4_65_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.devcel.2007.10.003"},{"key":"e_1_3_4_66_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.abk2432"},{"key":"e_1_3_4_67_2","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.200501042"},{"key":"e_1_3_4_68_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2008.04.050"},{"key":"e_1_3_4_69_2","doi-asserted-by":"publisher","DOI":"10.3390\/genes13050901"},{"key":"e_1_3_4_70_2","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1011111"},{"key":"e_1_3_4_71_2","doi-asserted-by":"publisher","DOI":"10.3389\/fcell.2017.00109"},{"key":"e_1_3_4_72_2","doi-asserted-by":"publisher","DOI":"10.1016\/S0960-9822(02)00894-1"},{"key":"e_1_3_4_73_2","doi-asserted-by":"publisher","DOI":"10.1126\/science.aal1647"},{"key":"e_1_3_4_74_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00329771"},{"key":"e_1_3_4_75_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF02932921"},{"key":"e_1_3_4_76_2","doi-asserted-by":"publisher","DOI":"10.1007\/BF00120178"},{"key":"e_1_3_4_77_2","doi-asserted-by":"publisher","DOI":"10.1046\/j.1440-169X.1998.t01-4-00006.x"},{"key":"e_1_3_4_78_2","doi-asserted-by":"publisher","DOI":"10.1111\/phen.12141"},{"key":"e_1_3_4_79_2","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2023.12.018"},{"key":"e_1_3_4_80_2","unstructured":"M. Richmond Y. Xiang SIMR-ODR. Stowers Institute. https:\/\/www.stowers.org\/research\/publications\/LIBPB-2548. Deposited 30 June 2024."}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.2520991123","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,3,7]],"date-time":"2026-03-07T16:52:23Z","timestamp":1772902343000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/10.1073\/pnas.2520991123"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,25]]},"references-count":80,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2026,3,3]]}},"alternative-id":["10.1073\/pnas.2520991123"],"URL":"https:\/\/doi.org\/10.1073\/pnas.2520991123","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,25]]},"assertion":[{"value":"2025-08-04","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-01-26","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-02-25","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e2520991123"}}