{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,20]],"date-time":"2026-09-20T06:17:01Z","timestamp":1789885021584,"version":"4.0.1"},"reference-count":57,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T00:00:00Z","timestamp":1737504000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100008787","name":"National Institute of Fisheries Science","doi-asserted-by":"crossref","award":["R2025062"],"award-info":[{"award-number":["R2025062"]}],"id":[{"id":"10.13039\/501100008787","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>The present study describes the differentiation process of male germ cells in <jats:italic>Octopus vulgaris<\/jats:italic>, the morphology of sperm in the testis and spermatophore, and the sperm released after the spermatophoric reaction. During spermatogenesis, the male sperm cell gradually elongates from a round shape, with cytoplasm shifting toward the head and the acrosome forming. Additionally, in the spermatid stage, the flagellum develops within the posterior nuclear channel and extends outside the cytoplasm. The sperm is composed of a head and a tail. The head is approximately 17.9 \u03bcm long and consists of a highly electron-dense nucleus and a helical acrosome. The tail is divided into three parts: the mid-piece, principal-piece, and end-piece. The mid-piece forms a mitochondrial sheath with 7\u20138 mitochondria surrounding a \u201c9+2\u201d axoneme. The principal-piece is composed of an axoneme, outer dense fibers, and fibrous sheath, while the end piece lacks outer dense fibers or fibrous sheath. The sperm in the testis and spermatophore, and the sperm released after the spermatophoric reaction have the same structure. However, in the sperm located in the testis and spermatophore, the structure of the acrosome is unclear due to the presence of cytoplasm in the head. In contrast, sperm released after the spermatophoric reaction lack their cytoplasm, revealing the helical acrosome. This unique sperm morphology, adapted for internal fertilization, is thought to be advantageous for fertilization and long-term storage within the female reproductive system.<\/jats:p>","DOI":"10.1371\/journal.pone.0316519","type":"journal-article","created":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T18:37:23Z","timestamp":1737571043000},"page":"e0316519","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":3,"title":["Transformation of sperm structure in Octopus vulgaris: From spermatogenesis to spermatophoric release"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9208-4616","authenticated-orcid":true,"given":"Hyeon Jin","family":"Kim","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jung Jun","family":"Park","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6292-328X","authenticated-orcid":true,"given":"Jung Sick","family":"Lee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,1,22]]},"reference":[{"issue":"1813","key":"pone.0316519.ref001","doi-asserted-by":"crossref","first-page":"20200074","DOI":"10.1098\/rstb.2020.0074","article-title":"Sperm competition and fertilization mode in fishes.","volume":"375","author":"JL Fitzpatrick","year":"2020","journal-title":"Philos Trans R Soc B-Biol Sci"},{"issue":"1","key":"pone.0316519.ref002","first-page":"44","article-title":"Sex differentiation of the rockfish, Sebastes schlegeli.","volume":"29","author":"YD Lee","year":"1996","journal-title":"J Korean Fish Soc."},{"key":"pone.0316519.ref003","first-page":"145","article-title":"Formation and structure of the spermatozeugmata of Neoditram ransonneti (Perciformes: Embiotocidae).","volume":"5","author":"JS Lee","year":"2001","journal-title":"Dev Reprod."},{"key":"pone.0316519.ref004","doi-asserted-by":"crossref","first-page":"197","DOI":"10.7208\/chicago\/9780226222769.001.0001","volume-title":"Ecology and Evolution of Poeciliid fishes.","author":"JP Evans","year":"2011"},{"key":"pone.0316519.ref005","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1016\/S0065-2881(08)60131-5","article-title":"sperm transfer in marine crustaceans","volume":"29","author":"Subramoniam T. Spermatophores","year":"1993","journal-title":"Adv Mar Biol"},{"issue":"2","key":"pone.0316519.ref006","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1093\/biolinnean\/blab096","article-title":"A review of sperm storage methods and post-copulatory sexual selection in the Cephalopoda.","volume":"134","author":"N. Sato","year":"2021","journal-title":"Biol J Linnean Soc"},{"key":"pone.0316519.ref007","first-page":"13","volume-title":"Handbook of culture of abalone and other Gastropods.","author":"CRC Press","year":"1989"},{"key":"pone.0316519.ref008","unstructured":"Gurney LJ, Mundy CN. Reproductive biology: identifying spawning cycles in the genus Haliotis. Tasmania: Marine Research Laboratories, Tasmanian Aquaculture and Fisheries Institute; 2004. Report No.: 23."},{"issue":"1","key":"pone.0316519.ref009","doi-asserted-by":"crossref","first-page":"30","DOI":"10.1038\/s41597-022-01131-w","article-title":"SpermTree, a species-level database of sperm morphology spanning the animal tree of life","volume":"9","author":"JL Fitzpatrick","year":"2022","journal-title":"Sci Data"},{"issue":"2","key":"pone.0316519.ref010","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1002\/jmor.10787","article-title":"Sperm ultrastructure in Bathypolypus bairdii and B. sponsalis (Cephalopoda: Octopoda).","volume":"271","author":"\u00c1 Roura","year":"2010","journal-title":"J Morphol"},{"issue":"8","key":"pone.0316519.ref011","doi-asserted-by":"crossref","first-page":"932","DOI":"10.1002\/jmor.10842","article-title":"Sperm ultrastructure of the hydrothermal vent octopod Vulcanoctopus hydrothermalis","volume":"271","author":"\u00c1 Roura","year":"2010","journal-title":"J Morphol"},{"issue":"1","key":"pone.0316519.ref012","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1093\/mollus\/59.1.105","article-title":"Sperm and spermiogenesis in Opisthoteuthis persephone (Octopoda: Cirrata): ultrastructure, comparison with other cephalopods and evolutionary significance.","volume":"59","author":"JM Healy","year":"1993","journal-title":"J Molluscan Stud"},{"issue":"3","key":"pone.0316519.ref013","first-page":"223","article-title":"Fine Structure on the Spermiogenesis of Octopus minor on the Western Coast of Korea I","volume":"31","author":"NS Chang","year":"2001","journal-title":"Korean J Electron Microscopy"},{"issue":"4","key":"pone.0316519.ref014","first-page":"333","article-title":"Fine structure of mature sperms of cephalopods (Octopus minor, Octopus ocellatus and Todarodes pacificus) inhabiting the Korean waters II.","volume":"31","author":"SW Kim","year":"2001","journal-title":"Korean J Electron Microscopy"},{"issue":"31\u201332","key":"pone.0316519.ref015","doi-asserted-by":"crossref","first-page":"2037","DOI":"10.1080\/00222933.2016.1184343","article-title":"Ultrastructure of spermatozoa and spermatogenesis in Octopus minor (Sasaki, 1920)(Cephalopoda: Octopoda).","volume":"50","author":"YS Qian","year":"2016","journal-title":"J Nat Hist"},{"issue":"1","key":"pone.0316519.ref016","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1007\/s00343-010-9995-y","article-title":"The ultrastructure of the spermatozoon of Octopus ocellatus Gray, 1849 (Cephalopoda: Octopoda).","volume":"29","author":"J Yang","year":"2011","journal-title":"Chin J Oceanol Limnol"},{"issue":"4","key":"pone.0316519.ref017","doi-asserted-by":"crossref","first-page":"1203","DOI":"10.2983\/0730-8000(2005)24[1203:TUOTSO]2.0.CO;2","article-title":"The ultrastructure of the spermatozoon of Octopus tankahkeei","volume":"24","author":"JQ Zhu","year":"2005","journal-title":"J Shellfish Res"},{"key":"pone.0316519.ref018","doi-asserted-by":"crossref","first-page":"5589","DOI":"10.1007\/s11033-011-1363-4","article-title":"Molecular characterization of a KIF3B-like kinesin gene in the testis of Octopus tankahkeei (Cephalopoda, Octopus).","volume":"39","author":"R Dang","year":"2012","journal-title":"Mol Biol Rep"},{"issue":"2","key":"pone.0316519.ref019","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1002\/jez.1402430211","article-title":"Scanning electron microscope studies of sperm incorporation into the zebrafish (Brachydanio) egg.","volume":"243","author":"JS Wolenski","year":"1987","journal-title":"J Exp Zool"},{"issue":"13","key":"pone.0316519.ref020","doi-asserted-by":"crossref","first-page":"445","DOI":"10.2307\/20026019","article-title":"The salamanders of the family Hynobiidae","volume":"58","author":"ER Dunn","year":"1923","journal-title":"Proc Am Acad Arts Sci"},{"key":"pone.0316519.ref021","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1080\/00222933.2013.825026","article-title":"Evolution of spermatophore transfer mechanisms in cephalopods.","volume":"49","author":"JEAR Marian","year":"2015","journal-title":"J Nat Hist"},{"issue":"18","key":"pone.0316519.ref022","first-page":"1462","article-title":"The acrosome of Octopus vulgaris L. Observation with the electron microscope.","volume":"267","author":"V Galangau","year":"1968","journal-title":"C R Acad Hebd Seances Acad Sci D."},{"issue":"3","key":"pone.0316519.ref023","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1002\/mrd.10103","article-title":"Evolution of octopod sperm II: Comparison of acrosomal morphogenesis in Eledone and Octopus","volume":"62","author":"E Ribes","year":"2002","journal-title":"Mol Reprod Dev"},{"issue":"2","key":"pone.0316519.ref024","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1002\/mrd.20069","article-title":"Chromatin organization during spermiogenesis in Octopus vulgaris. I: Morphological structures.","volume":"68","author":"E Ribes","year":"2004","journal-title":"Mole Reprod Dev"},{"issue":"1","key":"pone.0316519.ref025","first-page":"41","article-title":"Sex change scale and pattern of Tegillarca granosa (Bivalvia: Arcidae).","volume":"9","author":"MA Jeon","year":"2024","journal-title":"J Mar Life Sci"},{"key":"pone.0316519.ref026","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/humrep\/13.suppl_1.1","article-title":"Spermatogenesis.","volume":"13","author":"DM de Kretser","year":"1998","journal-title":"Hum Reprod"},{"key":"pone.0316519.ref027","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/S0022-5320(80)90133-1","article-title":"Morphology of abalone spermatozoa before and after the acrosome reaction.","volume":"72","author":"CA Lewis","year":"1980","journal-title":"J Ultrastruct Res"},{"key":"pone.0316519.ref028","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1007\/BF00367642","article-title":"Structure of the sperm of some South African archaeogastropods (Mollusca) from the superfamilies Haliotoidea, Fissurelloidea and Trochoidea.","volume":"113","author":"AN Hodgson","year":"1992","journal-title":"Mar biol"},{"key":"pone.0316519.ref029","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1007\/BF00217139","article-title":"Ultrastructural changes in the spermatogonia and spermatocytes of Poecilia reticulata during spermatogenesis","volume":"237","author":"R. Billard","year":"1984","journal-title":"Cell Tissue Res"},{"issue":"2","key":"pone.0316519.ref030","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1002\/mrd.1120150204","article-title":"Ultrastructure of the sperm and spermatogenesis of three species of Mytilidae (Mollusca, Bivalvia).","volume":"15","author":"AN Hodgson","year":"1986","journal-title":"Gamete Res."},{"key":"pone.0316519.ref031","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/S0074-7696(08)61357-1","article-title":"Electron microscope studies on spermiogenesis in various animal species","volume":"37","author":"G. Yasuzumi","year":"1974","journal-title":"Int Rev Cytol"},{"issue":"2","key":"pone.0316519.ref032","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.tice.2007.01.005","article-title":"Sperm nucleomorphogenesis in the cephalopod Sepia officinalis","volume":"39","author":"F Mart\u00ednez-Soler","year":"2007","journal-title":"Tissue Cell"},{"key":"pone.0316519.ref033","first-page":"109","article-title":"Ultrastructure of spermatozoa and spermiogenesis in Spirula spirula (L.): systematic importance and comparison with other cephalopods.","volume":"44","author":"JM Healy","year":"1990","journal-title":"Helgoland Mar Res"},{"issue":"1083","key":"pone.0316519.ref034","first-page":"181","article-title":"Spermiogenesis of Eledone cirrhosa Lamarck (Cephalopoda, Octopoda).","volume":"186","author":"WL Maxwell","year":"1974","journal-title":"Proc R Soc Lond Ser B-Biol Sci"},{"key":"pone.0316519.ref035","doi-asserted-by":"crossref","first-page":"500","DOI":"10.1002\/jmor.21323","article-title":"Process of cytoplasm elimination during spermiogenesis in Octopus tankahkeei: Polarized development of the spermatid and discarding of the residual body","volume":"282","author":"X Gao","year":"2021","journal-title":"J Morphol"},{"issue":"1219","key":"pone.0316519.ref036","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1098\/rstb.1989.0038","article-title":"Spermatozoa of the deep-sea cephalopod Vampyroteuthis infernalis Chun: ultrastructure and possible phylogenetic significance","volume":"323","author":"JM Healy","year":"1989","journal-title":"Phil Trans R Soc Lond B"},{"issue":"3","key":"pone.0316519.ref037","doi-asserted-by":"crossref","first-page":"625","DOI":"10.1242\/jcs.107.3.625","article-title":"Association of cytoplasmic dynein with manchette microtubules and spermatid nuclear envelope during spermiogenesis in rats","volume":"107","author":"T Yoshida","year":"1994","journal-title":"J Cell Sci"},{"key":"pone.0316519.ref038","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.semcdb.2014.01.003","article-title":"Microtubules and spermatogenesis","volume":"30","author":"L O\u2019Donnell","year":"2014","journal-title":"Semin Cell Dev Biol"},{"issue":"1\u20132","key":"pone.0316519.ref039","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/S0022-5320(70)80039-9","article-title":"Structural and cytochemical features of the sperm of the cephalopod Octopus bimaculatus.","volume":"32","author":"FJ Longo","year":"1970","journal-title":"J Ultrastruct Res"},{"issue":"2","key":"pone.0316519.ref040","first-page":"161","article-title":"Ultrastructure of spermatogenesis of Octopus tankahkeei.","volume":"30","author":"JQ Zhu","year":"2006","journal-title":"J Fish China"},{"key":"pone.0316519.ref041","volume-title":"Fish evolution and systematics: evidence from spermatozoa.","author":"BGM Jamieson","year":"1991"},{"issue":"1","key":"pone.0316519.ref042","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1093\/biolre\/ioy045","article-title":"Sperm acrosome reaction: its site and role in fertilization","volume":"99","author":"N Hirohashi","year":"2018","journal-title":"Biol Reprod"},{"issue":"1","key":"pone.0316519.ref043","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1002\/aja.1001780109","article-title":"Comparative study of cytoplasmic elimination in spermatids of selected mammalian species","volume":"178","author":"RL Sprando","year":"1987","journal-title":"Am J Anat"},{"key":"pone.0316519.ref044","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1007\/BF00219830","article-title":"An ultrastructural analysis of the gametes and early fertilization in two bivalve molluscs, Chama macerophylla and Spisula solidissima with special reference to gamete binding","volume":"182","author":"BL Hylander","year":"1977","journal-title":"Cell Tissue Res"},{"issue":"4","key":"pone.0316519.ref045","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1111\/j.1469-7998.1992.tb04419.x","article-title":"Egg development in the octopus Eledone cirrhosa","volume":"227","author":"PR Boyle","year":"1992","journal-title":"J Zoo"},{"issue":"1090","key":"pone.0316519.ref046","first-page":"95","article-title":"The structure and function of the oviducal gland in octopods (Cephalopoda).","volume":"188","author":"D. Froesch","year":"1975","journal-title":"Pro Roy Soc Lond Ser B-Biol Sci."},{"issue":"4","key":"pone.0316519.ref047","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1080\/07924259.2019.1646674","article-title":"Morphological and histological description of the reproductive system of Octopus hubbsorum (Mollusca: Cephalopoda).","volume":"63","author":"M Garc\u00eda-Flores","year":"2019","journal-title":"Invertebr Reprod Dev"},{"key":"pone.0316519.ref048","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1515\/BC.2011.074","article-title":"Septins at the annulus of mammalian sperm","volume":"392","author":"A Toure","year":"2011","journal-title":"Biol Chem"},{"key":"pone.0316519.ref049","first-page":"527","article-title":"Spermiogenesis of Eusepia officinalis (L.), Loligo forbesi (Steenstrup) and Alloteuthis subulata (L.) (Cephalopda, Decapoda).","volume":"191","author":"WL Maxwell","year":"1975","journal-title":"Pro Roy Soc Lond Ser B-Biol Sci"},{"issue":"12","key":"pone.0316519.ref050","doi-asserted-by":"crossref","first-page":"10030","DOI":"10.3390\/ijms241210030","article-title":"The effect of prohibitins on mitochondrial function during Octopus tankahkeei spermiogenesis.","volume":"24","author":"J Wang","year":"2023","journal-title":"Int J Mol Sci"},{"issue":"6","key":"pone.0316519.ref051","doi-asserted-by":"crossref","first-page":"1296","DOI":"10.1093\/humrep\/dep020","article-title":"Absence of annulus in human asthenozoospermia: case report","volume":"24","author":"P Lhuillier","year":"2009","journal-title":"Hum Reprod"},{"issue":"1\u20132","key":"pone.0316519.ref052","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/0304-3975(95)00100-X","article-title":"Over testable languages","volume":"161","author":"C. Selmi","year":"1996","journal-title":"Theor Comput Sci"},{"issue":"4","key":"pone.0316519.ref053","doi-asserted-by":"crossref","first-page":"669","DOI":"10.1095\/biolreprod.109.079566","article-title":"The annulus of the mouse sperm tail is required to establish a membrane diffusion barrier that is engaged during the late steps of spermiogenesis","volume":"82","author":"S Kwitny","year":"2010","journal-title":"Biol Reprod"},{"issue":"2","key":"pone.0316519.ref054","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1016\/0012-1606(75)90411-X","article-title":"The mammalian spermatozoon","volume":"44","author":"DW Fawcett","year":"1975","journal-title":"Dev Biol"},{"key":"pone.0316519.ref055","doi-asserted-by":"crossref","first-page":"652","DOI":"10.1002\/cm.21338","article-title":"Functional anatomy of the mammalian sperm flagellum.","volume":"73","author":"CB Lindemann","year":"2016","journal-title":"Cytoskeleton"},{"issue":"152","key":"pone.0316519.ref056","doi-asserted-by":"crossref","first-page":"20180668","DOI":"10.1098\/rsif.2018.0668","article-title":"Flagellar ultrastructure suppresses buckling instabilities and enables mammalian sperm navigation in high-viscosity media.","volume":"16","author":"H Gad\u00ealha","year":"2019","journal-title":"J R Soc Interface"},{"issue":"13","key":"pone.0316519.ref057","doi-asserted-by":"crossref","first-page":"2880","DOI":"10.1016\/j.cell.2023.05.026","article-title":"Structural specializations of the sperm tail","volume":"186","author":"MR Leung","year":"2023","journal-title":"Cell"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0316519","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T18:37:42Z","timestamp":1737571062000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0316519"}},"subtitle":[],"editor":[{"given":"Wan-Xi","family":"Yang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,1,22]]},"references-count":57,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1,22]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0316519","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,22]]}}}