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Thus, one spermatocyte could give rise to two spermatids with either equal or unequal amounts of cytoplasm. It is currently unknown what molecular features accompany these postmeiotic sperm cells especially in species with asymmetric meiosis II such as bees. Here we present testis single-cell RNA sequencing datasets from the honeybee (<jats:italic>Apis mellifera<\/jats:italic>) drones of 3 and 14 days after emergence (3d and 14d). We show that, while 3d testes exhibit active, ongoing spermatogenesis, 14d testes only have late-stage spermatids. We identify a postmeiotic bifurcation in the transcriptional roadmap during spermatogenesis, with cells progressing toward the annotated spermatids (SPT) and small spermatids (sSPT), respectively. Despite an overall similarity in their transcriptomic profiles, sSPTs express the fewest genes and the least RNA content among all the sperm cell types. Intriguingly, sSPTs exhibit a relatively high expression level for Hymenoptera-restricted genes and a high mutation load, suggesting that the special meiosis II during spermatogenesis in the honeybee is accompanied by phylogenetically young gene activities.<\/jats:p>","DOI":"10.1371\/journal.pgen.1011081","type":"journal-article","created":{"date-parts":[[2023,12,4]],"date-time":"2023-12-04T18:32:03Z","timestamp":1701714723000},"page":"e1011081","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["A postmeiotically bifurcated roadmap of honeybee spermatogenesis marked by phylogenetically restricted genes"],"prefix":"10.1371","volume":"19","author":[{"ORCID":"https:\/\/orcid.org\/0009-0004-7316-496X","authenticated-orcid":true,"given":"Zhiyong","family":"Yin","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guiling","family":"Ding","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0001-7000-6403","authenticated-orcid":true,"given":"Yingdi","family":"Xue","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xianghui","family":"Yu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jie","family":"Dong","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5373-6108","authenticated-orcid":true,"given":"Jiaxing","family":"Huang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1609-3294","authenticated-orcid":true,"given":"Jun","family":"Ma","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7114-8078","authenticated-orcid":true,"given":"Feng","family":"He","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2023,12,4]]},"reference":[{"key":"pgen.1011081.ref001","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.cois.2015.04.018","article-title":"Haplodiploidy and the reproductive ecology of Arthropods","volume":"9","author":"AG De La Filia","year":"2015","journal-title":"Curr Opin Insect Sci"},{"key":"pgen.1011081.ref002","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1086\/663683","article-title":"Haplodiploidy and the Evolution of Eusociality","volume":"179","author":"A Gardner","year":"2012","journal-title":"Split Sex Ratios. 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Meves","year":"1907","journal-title":"Archiv f mikrosk Anat."},{"key":"pgen.1011081.ref010","first-page":"222","article-title":"Cytological Studies in Hymenoptera: Part II: Cytology of parthenogenesis in the carpenter-bee, Xylocopa fenesterata Fabre.","volume":"30","author":"CG Kumbkarni","year":"1965","journal-title":"Caryologia"},{"key":"pgen.1011081.ref011","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/S0022-5320(68)80014-0","article-title":"An electron microscope study of the process of differentiation during spermatogenesis in the drone honey bee (Apis mellifera L.) with special reference to centriole replication and elimination.","volume":"24","author":"TR Hoage","year":"1968","journal-title":"Journal of Ultrastructure Research."},{"key":"pgen.1011081.ref012","doi-asserted-by":"crossref","DOI":"10.7476\/9788539304301","volume-title":"Abelhas: morfologia e fun\u00e7\u00e3o de sistemas","author":"C. 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Hayashi","year":"2019","journal-title":"Apidologie"},{"key":"pgen.1011081.ref036","doi-asserted-by":"crossref","first-page":"538","DOI":"10.1016\/j.jinsphys.2009.01.012","article-title":"Honey bee males and queens use glandular secretions to enhance sperm viability before and after storage","volume":"55","author":"SPA Den Boer","year":"2009","journal-title":"J Insect Physiol"},{"key":"pgen.1011081.ref037","doi-asserted-by":"crossref","first-page":"348","DOI":"10.1016\/j.stem.2010.02.016","article-title":"HOW Is Required for Stem Cell Maintenance in the Drosophila Testis and for the Onset of Transit-Amplifying Divisions.","volume":"6","author":"AC Monk","year":"2010","journal-title":"Cell Stem Cell"},{"key":"pgen.1011081.ref038","doi-asserted-by":"crossref","first-page":"2777","DOI":"10.1242\/jcs.01123","article-title":"A screen for modifiers of RacGAP(84C) gain-of-function in the Drosophila eye revealed the LIM kinase Cdi\/TESK1 as a downstream effector of Rac1 during 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Witt","year":"2019","journal-title":"eLife"},{"key":"pgen.1011081.ref051","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1534\/genetics.105.051557","article-title":"The mushroom body defect Gene Product Is an Essential Component of the Meiosis II Spindle Apparatus in Drosophila Oocytes","volume":"173","author":"JX Yu","year":"2006","journal-title":"Genetics"},{"key":"pgen.1011081.ref052","doi-asserted-by":"crossref","first-page":"2171","DOI":"10.1016\/j.jprot.2010.09.002","article-title":"The Drosophila melanogaster sperm proteome-II (DmSP-II).","volume":"73","author":"ER Wasbrough","year":"2010","journal-title":"Journal of Proteomics"},{"key":"pgen.1011081.ref053","doi-asserted-by":"crossref","first-page":"1682","DOI":"10.1126\/science.1196380","article-title":"New Genes in Drosophila Quickly Become Essential","volume":"330","author":"S Chen","year":"2010","journal-title":"Science"},{"key":"pgen.1011081.ref054","doi-asserted-by":"crossref","first-page":"2104","DOI":"10.1093\/molbev\/msab011","article-title":"Transcription Factors Drive Opposite Relationships between Gene Age and Tissue Specificity in Male and Female Drosophila Gonads.","volume":"38","author":"E Witt","year":"2021","journal-title":"Molecular Biology and Evolution"},{"key":"pgen.1011081.ref055","doi-asserted-by":"crossref","first-page":"134","DOI":"10.1186\/s12915-022-01339-7","article-title":"Transcriptional and post-transcriptional regulation of young genes in plants.","volume":"20","author":"VK Raxwal","year":"2022","journal-title":"BMC Biol."},{"key":"pgen.1011081.ref056","doi-asserted-by":"crossref","first-page":"1431","DOI":"10.1016\/j.cell.2014.08.009","article-title":"Determination and Inference of Eukaryotic Transcription Factor Sequence Specificity","volume":"158","author":"MT 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