{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,30]],"date-time":"2026-10-30T20:30:17Z","timestamp":1793392217538,"version":"4.5.0"},"reference-count":78,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,5,11]],"date-time":"2022-05-11T00:00:00Z","timestamp":1652227200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,5,11]],"date-time":"2022-05-11T00:00:00Z","timestamp":1652227200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/100000011","name":"Howard Hughes Medical Institute","doi-asserted-by":"publisher","award":["047-101"],"award-info":[{"award-number":["047-101"]}],"id":[{"id":"10.13039\/100000011","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Commun"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Sex determination mechanisms evolve surprisingly rapidly, yet little is known in the large nematode phylum other than for <jats:italic>Caenorhabditis elegans<\/jats:italic>, which relies on chromosomal XX-XO sex determination and a dosage compensation mechanism. Here we analyze by sex-specific genome sequencing and genetic analysis sex determination in two fungal feeding\/plant-parasitic <jats:italic>Bursaphelenchus<\/jats:italic> nematodes and find that their sex differentiation is more likely triggered by random, epigenetic regulation than by more well-known mechanisms of chromosomal or environmental sex determination. There is no detectable difference in male and female chromosomes, nor any linkage to sexual phenotype. Moreover, the protein sets of these nematodes lack genes involved in X chromosome dosage counting or compensation. By contrast, our genetic screen for sex differentiation mutants identifies a <jats:italic>Bursaphelenchus<\/jats:italic> ortholog of <jats:italic>tra-1<\/jats:italic>, the major output of the <jats:italic>C. elegans<\/jats:italic> sex determination cascade. Nematode sex determination pathways might have evolved by \u201cbottom-up\u201d accretion from the most downstream regulator, <jats:italic>tra-1<\/jats:italic>.<\/jats:p>","DOI":"10.1038\/s41467-022-30173-2","type":"journal-article","created":{"date-parts":[[2022,5,11]],"date-time":"2022-05-11T10:07:53Z","timestamp":1652263673000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":22,"title":["Possible stochastic sex determination in Bursaphelenchus nematodes"],"prefix":"10.1038","volume":"13","author":[{"given":"Ryoji","family":"Shinya","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simo","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5367-918X","authenticated-orcid":false,"given":"Mehmet","family":"Dayi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2123-5058","authenticated-orcid":false,"given":"Isheng Jason","family":"Tsai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Atsushi","family":"Miyama","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anthony Fu","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9968-8129","authenticated-orcid":false,"given":"Koichi","family":"Hasegawa","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9934-3040","authenticated-orcid":false,"given":"Igor","family":"Antoshechkin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2759-9167","authenticated-orcid":false,"given":"Taisei","family":"Kikuchi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7699-0173","authenticated-orcid":false,"given":"Paul W.","family":"Sternberg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,5,11]]},"reference":[{"key":"30173_CR1","doi-asserted-by":"publisher","first-page":"e21","DOI":"10.1371\/journal.pbio.0030021","volume":"3","author":"ES Haag","year":"2005","unstructured":"Haag, E. S. & Doty, A. V. Sex determination across evolution: connecting the dots. PLoS Biol. 3, e21 (2005).","journal-title":"PLoS Biol."},{"key":"30173_CR2","first-page":"75","volume":"46","author":"A D\u00fcbendorfer","year":"2002","unstructured":"D\u00fcbendorfer, A., Hediger, M., Burghardt, G. & Bopp, D. Musca domestica, a window on the evolution of sex-determining mechanisms in insects. Int. J. Dev. Biol. 46, 75\u201379 (2002).","journal-title":"Int. J. Dev. Biol."},{"key":"30173_CR3","doi-asserted-by":"publisher","first-page":"e1001899","DOI":"10.1371\/journal.pbio.1001899","volume":"12","author":"D Bachtrog","year":"2014","unstructured":"Bachtrog, D. et al. Sex determination: why so many ways of doing it? PLoS Biol. 12, e1001899 (2014).","journal-title":"PLoS Biol."},{"key":"30173_CR4","doi-asserted-by":"publisher","first-page":"448","DOI":"10.1038\/348448a0","volume":"348","author":"P Berta","year":"1990","unstructured":"Berta, P. et al. Genetic evidence equating SRY and the testis-determining factor. Nature 348, 448\u2013450 (1990).","journal-title":"Nature"},{"key":"30173_CR5","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1086\/280023","volume":"59","author":"CB Bridges","year":"1925","unstructured":"Bridges, C. B. Sex in relation to chromosomes and genes. Am. Nat. 59, 127 (1925).","journal-title":"Am. Nat."},{"key":"30173_CR6","first-page":"1","volume":"11","author":"V Nigon","year":"1949","unstructured":"Nigon, V. Les modalit\u00e9s de la reproduction et le d\u00e9terminisme du sexe chez quelques N\u00e9matodes libres. Ann. Sci. Nat. Zool. Biol. Anim. 11, 1\u2013132 (1949).","journal-title":"Ann. Sci. Nat. Zool. Biol. Anim."},{"key":"30173_CR7","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1093\/genetics\/93.2.393","volume":"93","author":"JE Madl","year":"1979","unstructured":"Madl, J. E. & Herman, R. K. Polyploids and sex determination in Caenorhabditis elegans. Genetics 93, 393\u2013402 (1979).","journal-title":"Genetics"},{"key":"30173_CR8","doi-asserted-by":"publisher","first-page":"1049","DOI":"10.1534\/genetics.107.072140","volume":"176","author":"M Vandeputte","year":"2007","unstructured":"Vandeputte, M., Dupont-Nivet, M., Chavanne, H. & Chatain, B. A polygenic hypothesis for sex determination in the European sea bass Dicentrarchus labrax. Genetics 176, 1049\u20131057 (2007).","journal-title":"Genetics"},{"key":"30173_CR9","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1017\/S0016672300019157","volume":"40","author":"M Franco","year":"1982","unstructured":"Franco, M., Rubini, P. & Vecchi, M. Sex-determinants and their distribution in various populations of Musca domestica L. of Western Europe. Genet. Res. 40, 279\u2013293 (1982).","journal-title":"Genet. Res."},{"key":"30173_CR10","first-page":"620","volume":"160","author":"M Charnier","year":"1966","unstructured":"Charnier, M. Action of temperature on the sex ratio in the Agama agama (Agamidae, Lacertilia) embryo. C. R. Seances Soc. Biol. Fil. 160, 620\u2013622 (1966).","journal-title":"C. R. Seances Soc. Biol. Fil."},{"key":"30173_CR11","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1016\/S0044-8486(02)00057-1","volume":"208","author":"RH Devlin","year":"2002","unstructured":"Devlin, R. H. & Nagahama, Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 208, 191\u2013364 (2002).","journal-title":"Aquaculture"},{"key":"30173_CR12","doi-asserted-by":"publisher","first-page":"e1001518","DOI":"10.1371\/journal.pbio.1001518","volume":"11","author":"MD Cervantes","year":"2013","unstructured":"Cervantes, M. D. et al. Selecting one of several mating types through gene segment joining and deletion in tetrahymena thermophila. PLoS Biol. 11, e1001518 (2013).","journal-title":"PLoS Biol."},{"key":"30173_CR13","doi-asserted-by":"publisher","first-page":"667","DOI":"10.1242\/dev.127.4.667","volume":"127","author":"C Schutt","year":"2000","unstructured":"Schutt, C. & Nothiger, R. Structure, function and evolution of sex-determining systems in Dipteran insects. Development 127, 667\u2013677 (2000).","journal-title":"Development"},{"key":"30173_CR14","doi-asserted-by":"publisher","first-page":"3921","DOI":"10.1242\/dev.048983","volume":"137","author":"K Kashimada","year":"2010","unstructured":"Kashimada, K. & Koopman, P. Sry: the master switch in mammalian sex determination. Development 137, 3921\u20133930 (2010).","journal-title":"Development"},{"key":"30173_CR15","doi-asserted-by":"publisher","unstructured":"Hubbard, E. J. & Greenstein, D. Introduction to the germ line. WormBook, https:\/\/doi.org\/10.1895\/wormbook.1.18.1 (2005).","DOI":"10.1895\/wormbook.1.18.1"},{"key":"30173_CR16","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1093\/genetics\/91.1.67","volume":"91","author":"J Hodgkin","year":"1979","unstructured":"Hodgkin, J., Horvitz, H. R. & Brenner, S. Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91, 67\u201394 (1979).","journal-title":"Genetics"},{"key":"30173_CR17","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1002\/bies.10239","volume":"25","author":"P Stothard","year":"2003","unstructured":"Stothard, P. & Pilgrim, D. Sex-determination gene and pathway evolution in nematodes. Bioessays 25, 221\u2013231 (2003).","journal-title":"Bioessays"},{"key":"30173_CR18","doi-asserted-by":"publisher","unstructured":"Haag, E. S. The evolution of nematode sex determination: C. elegans as a reference point for comparative biology. WormBook, https:\/\/doi.org\/10.1895\/wormbook.1.120.1 (2005).","DOI":"10.1895\/wormbook.1.120.1"},{"key":"30173_CR19","doi-asserted-by":"publisher","first-page":"362","DOI":"10.1016\/j.semcdb.2006.11.014","volume":"18","author":"A Pires-daSilva","year":"2007","unstructured":"Pires-daSilva, A. Evolution of the control of sexual identity in nematodes. Semin. Cell Dev. Biol. 18, 362\u2013370 (2007).","journal-title":"Semin. Cell Dev. Biol."},{"key":"30173_CR20","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1017\/S003118200006354X","volume":"92","author":"CJ Delves","year":"1986","unstructured":"Delves, C. J., Howells, R. E. & Post, R. J. Gametogenesis and fertilization in Dirofilaria immitis (Nematoda: Filarioidea). Parasitology 92, 181\u2013197 (1986).","journal-title":"Parasitology"},{"key":"30173_CR21","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S0166-6851(98)00180-7","volume":"99","author":"AP Underwood","year":"1999","unstructured":"Underwood, A. P. & Bianco, A. E. Identification of a molecular marker for the Y chromosome of Brugia malayi. Mol. Biochem. Parasitol. 99, 1\u201310 (1999).","journal-title":"Mol. Biochem. Parasitol."},{"key":"30173_CR22","first-page":"549","volume":"14","author":"J Papadopoulou","year":"1982","unstructured":"Papadopoulou, J. & Traintaphyllou, A. C. Sex differentiation in Meloidogyne incognita and anatomical evidence of sex reversal. J. Nematol. 14, 549\u2013566 (1982).","journal-title":"J. Nematol."},{"key":"30173_CR23","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1017\/S0031182000064192","volume":"92","author":"GA Tingley","year":"1986","unstructured":"Tingley, G. A. & Anderson, R. M. Environmental sex determination and density-dependent population regulation in the entomogenous nematode Romanomermis culicivorax. Parasitology 92, 431\u2013449 (1986).","journal-title":"Parasitology"},{"key":"30173_CR24","doi-asserted-by":"publisher","first-page":"1907","DOI":"10.1534\/g3.114.012385","volume":"4","author":"R Shinya","year":"2014","unstructured":"Shinya, R., Hasegawa, K., Chen, A., Kanzaki, N. & Sternberg, P. W. Evidence of hermaphroditism and sex ratio distortion in the fungal feeding nematode Bursaphelenchus okinawaensis. G3 (Bethesda) 4, 1907\u20131917 (2014).","journal-title":"G3 (Bethesda)"},{"key":"30173_CR25","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1163\/156854106778493475","volume":"8","author":"K Hasegawa","year":"2006","unstructured":"Hasegawa, K., Mota, M. M., Futai, K. & Miwa, J. Chromosome structure and behaviour in Bursaphelenchus xylophilus (Nematoda: Parasitaphelenchidae) germ cells and early embryo. Nematology 8, 425\u2013434 (2006).","journal-title":"Nematology"},{"key":"30173_CR26","first-page":"241","volume":"30","author":"T Kiyohara","year":"1977","unstructured":"Kiyohara, T. Variation in virulence and reproduction rate among isolates of pine wilt nematode. Proc. Kyushu Jpn. Soc. 30, 241\u2013242 (1977).","journal-title":"Proc. Kyushu Jpn. Soc."},{"key":"30173_CR27","doi-asserted-by":"publisher","first-page":"e1002219","DOI":"10.1371\/journal.ppat.1002219","volume":"7","author":"T Kikuchi","year":"2011","unstructured":"Kikuchi, T. et al. Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathog. 7, e1002219 (2011).","journal-title":"PLoS Pathog."},{"key":"30173_CR28","doi-asserted-by":"publisher","first-page":"e01000","DOI":"10.1128\/MRA.01000-20","volume":"9","author":"S Sun","year":"2020","unstructured":"Sun, S. et al. Telomere-to-telomere genome assembly of Bursaphelenchus okinawaensis strain SH1. Microbiol. Resour. Announc. 9, e01000\u2013e01020 (2020).","journal-title":"Microbiol. Resour. Announc."},{"key":"30173_CR29","doi-asserted-by":"publisher","first-page":"e01002","DOI":"10.1128\/MRA.01002-20","volume":"9","author":"M Dayi","year":"2020","unstructured":"Dayi, M. et al. Nearly complete genome assembly of the pinewood nematode Bursaphelenchus xylophilus strain Ka4C1. Microbiol. Resour. Announc. 9, e01002\u2013e01020 (2020).","journal-title":"Microbiol. Resour. Announc."},{"key":"30173_CR30","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-14998-3","volume":"18","author":"TR Ranallo-Benavidez","year":"2020","unstructured":"Ranallo-Benavidez, T. R., Jaron, K. S. & Schatz, M. C. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat. Commun. 18, 1432 (2020).","journal-title":"Nat. Commun."},{"key":"30173_CR31","doi-asserted-by":"publisher","DOI":"10.1186\/s12864-019-5996-3","volume":"20","author":"S Rangavittal","year":"2019","unstructured":"Rangavittal, S. et al. DiscoverY: a classifier for identifying Y chromosome sequences in male assemblies. BMC Genomics 20, 641 (2019).","journal-title":"BMC Genomics"},{"key":"30173_CR32","doi-asserted-by":"publisher","first-page":"161","DOI":"10.3390\/insects3010161","volume":"3","author":"D Kageyama","year":"2012","unstructured":"Kageyama, D., Narita, S. & Watanabe, M. Insect sex determination manipulated by their endosymbionts: incidences, mechanisms and implications. Insects 3, 161\u2013199 (2012).","journal-title":"Insects"},{"key":"30173_CR33","doi-asserted-by":"publisher","first-page":"2935","DOI":"10.1242\/dev.01154","volume":"131","author":"M Belfiore","year":"2004","unstructured":"Belfiore, M., Pugnale, P., Saudan, Z. & Puoti, A. Roles of the C. elegans cyclophilin-like protein MOG-6 in MEP-1 binding and germline fates. Development 131, 2935\u20132945 (2004).","journal-title":"Development"},{"key":"30173_CR34","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/S0960-9822(02)00675-9","volume":"12","author":"EB Goodwin","year":"2002","unstructured":"Goodwin, E. B. & Ellis, R. E. Turning clustering loops: sex determination in Caenorhabditis elegans. Curr. Biol. 12, 111\u2013120 (2002).","journal-title":"Curr. Biol."},{"key":"30173_CR35","doi-asserted-by":"publisher","first-page":"16033","DOI":"10.1073\/pnas.1312087110","volume":"110","author":"M Berkseth","year":"2013","unstructured":"Berkseth, M., Ikegami, K., Arur, S., Lieb, J. D. & Zarkower, D. TRA-1 ChIP-seq reveals regulators of sexual differentiation and multilevel feedback in nematode sex determination. Proc. Natl Acad. Sci. USA 110, 16033\u201316038 (2013).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"30173_CR36","doi-asserted-by":"crossref","unstructured":"Chailakhyan, M. K. & Khrianin, V. N. Influence of environmental factors and nutrition on sex determination in plants. In sexuality in plants and its hormonal regulation. pp. 16\u201332 (Springer, New York, 1987).","DOI":"10.1007\/978-1-4612-4734-0_2"},{"key":"30173_CR37","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/j.jembe.2014.07.009","volume":"461","author":"EE Brown","year":"2014","unstructured":"Brown, E. E., Baumann, H. & Conover, D. O. Temperature and photoperiod effects on sex determination in a fish. J. Exp. Mar. Biol. Ecol. 461, 39\u201343 (2014).","journal-title":"J. Exp. Mar. Biol. Ecol."},{"key":"30173_CR38","doi-asserted-by":"publisher","first-page":"1548","DOI":"10.1016\/j.cub.2011.08.009","volume":"21","author":"J Chaudhuri","year":"2011","unstructured":"Chaudhuri, J., Kache, V. & Pires-daSilva, A. Regulation of sexual plasticity in a nematode that produces males, females, and hermaphrodites. Curr. Biol. 21, 1548\u20131551 (2011).","journal-title":"Curr. Biol."},{"key":"30173_CR39","doi-asserted-by":"publisher","first-page":"1218","DOI":"10.1002\/bies.201600093","volume":"38","author":"N Perrin","year":"2016","unstructured":"Perrin, N. Random sex determination: When developmental noise tips the sex balance. BioEssays 38, 1218\u20131226 (2016).","journal-title":"BioEssays"},{"key":"30173_CR40","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1146\/annurev.micro.112408.134306","volume":"64","author":"K Lewis","year":"2010","unstructured":"Lewis, K. Persister cells. Annu. Rev. Microbiol. 64, 357\u2013372 (2010).","journal-title":"Annu. Rev. Microbiol."},{"key":"30173_CR41","doi-asserted-by":"publisher","first-page":"4393","DOI":"10.1073\/pnas.0700463105","volume":"105","author":"JW Veening","year":"2008","unstructured":"Veening, J. W. et al. Bet-hedging and epigenetic inheritance in bacterial cell development. Proc. Natl Acad. Sci. USA 105, 4393\u20134398 (2008).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"30173_CR42","doi-asserted-by":"publisher","first-page":"861","DOI":"10.2108\/zsj.25.861","volume":"25","author":"N Kanzaki","year":"2008","unstructured":"Kanzaki, N., Maehara, N., Aikawa, T. & Togashi, K. First report of parthenogenesis in the genus Bursaphelenchus Fuchs, 1937: a description of Bursaphelenchus okinawaensis sp. nov. Isolated from Monochamus maruokai (Coleoptera: Cerambycidae). Zool. Sci. 25, 861\u2013873 (2008).","journal-title":"Zool. Sci."},{"key":"30173_CR43","doi-asserted-by":"publisher","first-page":"1260","DOI":"10.15252\/embr.201540667","volume":"16","author":"A Herpin","year":"2015","unstructured":"Herpin, A. & Schartl, M. Plasticity of gene-regulatory networks controlling sex determination: of masters, slaves, usual suspects, newcomers, and usurpators. EMBO Rep. 16, 1260\u20131274 (2015).","journal-title":"EMBO Rep."},{"key":"30173_CR44","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1093\/genetics\/86.2.275","volume":"86","author":"JA Hodgkin","year":"1977","unstructured":"Hodgkin, J. A. & Brenner, S. Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans. Genetics 86, 275\u2013287 (1977).","journal-title":"Genetics"},{"key":"30173_CR45","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1038\/304267a0","volume":"304","author":"J Hodgkin","year":"1983","unstructured":"Hodgkin, J. Two types of sex determination in a nematode. Nature 304, 267\u2013268 (1983).","journal-title":"Nature"},{"key":"30173_CR46","doi-asserted-by":"publisher","first-page":"1415","DOI":"10.1534\/genetics.107.073668","volume":"178","author":"DF Kelleher","year":"2008","unstructured":"Kelleher, D. F. et al. Comparative genetics of sex determination: masculinizing mutations in Caenorhabditis briggsae. Genetics 178, 1415\u20131429 (2008).","journal-title":"Genetics"},{"key":"30173_CR47","doi-asserted-by":"publisher","first-page":"1198","DOI":"10.1101\/gad.293504","volume":"18","author":"A Pires-daSilva","year":"2004","unstructured":"Pires-daSilva, A. & Sommer, R. J. Conservation of the global sex determination gene tra-1 in distantly related nematodes. Genes Dev. 18, 1198\u20131208 (2004).","journal-title":"Genes Dev."},{"key":"30173_CR48","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1038\/32160","volume":"392","author":"ML Blaxter","year":"1998","unstructured":"Blaxter, M. L. et al. A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71\u201375 (1998).","journal-title":"Nature"},{"key":"30173_CR49","doi-asserted-by":"publisher","first-page":"1016","DOI":"10.1038\/1741016b0","volume":"174","author":"C Ellenby","year":"1954","unstructured":"Ellenby, C. Environmental determination of the sex ratio of a plant parasitic nematode. Nature 174, 1016\u20131017 (1954).","journal-title":"Nature"},{"key":"30173_CR50","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1146\/annurev.py.11.090173.002301","volume":"11","author":"AC Triantaphyllou","year":"1973","unstructured":"Triantaphyllou, A. C. Environmental sex differentiation of nematodes in relation to pest management. Annu. Rev. Phytopathol. 11, 441\u2013462 (1973).","journal-title":"Annu. Rev. Phytopathol."},{"key":"30173_CR51","doi-asserted-by":"publisher","first-page":"1160","DOI":"10.1111\/pce.13728","volume":"43","author":"MS Anjam","year":"2020","unstructured":"Anjam, M. S. et al. Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana. Plant Cell Environ. 43, 1160\u20131174 (2020).","journal-title":"Plant Cell Environ."},{"key":"30173_CR52","doi-asserted-by":"publisher","first-page":"3604","DOI":"10.1016\/j.cub.2020.06.060","volume":"30","author":"EA Bayer","year":"2020","unstructured":"Bayer, E. A., Sun, H., Rafi, I. & Hobert, O. Temporal, spatial, sexual and environmental regulation of the master regulator of sexual differentiation in C. elegans. Curr. Biol. 30, 3604\u20133616 (2020).","journal-title":"Curr. Biol."},{"key":"30173_CR53","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1002\/bies.950170113","volume":"17","author":"AS Wilkins","year":"1995","unstructured":"Wilkins, A. S. Moving up the hierarchy: a hypothesis on the evolution of a genetic sex determination pathway. Bioessays 17, 71\u201377 (1995).","journal-title":"Bioessays"},{"key":"30173_CR54","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1073\/pnas.31.6.153","volume":"31","author":"NH Horowitz","year":"1945","unstructured":"Horowitz, N. H. On the evolution of biochemical syntheses. Proc. Natl Acad. Sci. USA 31, 153\u2013157 (1945).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"30173_CR55","doi-asserted-by":"publisher","first-page":"849","DOI":"10.2307\/3277110","volume":"54","author":"RI Bolla","year":"1968","unstructured":"Bolla, R. I. & Roberts, L. S. Gametogenesis and chromosomal complement in Strongyloides ratti (Nematode: Rhabdiasoidea). J. Parasitol. 54, 849\u2013855 (1968).","journal-title":"J. Parasitol."},{"key":"30173_CR56","first-page":"355","volume":"2","author":"HC Hechler","year":"1970","unstructured":"Hechler, H. C. Reproduction, chromosome number, and postembryonic development of Panagrellus redivivus (Nematoda: Cephalobidae). J. Nematol. 2, 355\u2013361 (1970).","journal-title":"J. Nematol."},{"key":"30173_CR57","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1007\/BF00330626","volume":"75","author":"DG Albertson","year":"1979","unstructured":"Albertson, D. G., Nwaorgu, O. C. & Sulston, J. E. Chromatin diminution and a chromosomal mechanism of sexual differentiation in Strongyloides papillosus. Chromosoma 75, 75\u201387 (1979).","journal-title":"Chromosoma"},{"key":"30173_CR58","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1007\/s13355-012-0124-8","volume":"47","author":"R Shinya","year":"2012","unstructured":"Shinya, R., Takeuchi, Y., Ichimura, K., Takemoto, S. & Futai, K. Establishment of a set of inbred strains of the pine wood nematode, Bursaphelenchus xylophilus (Aphelenchida: Aphelenchoididae), and evidence of their varying levels of virulence. Appl. Entmol. Zool. 47, 341\u2013350 (2012).","journal-title":"Appl. Entmol. Zool."},{"key":"30173_CR59","doi-asserted-by":"publisher","first-page":"2759","DOI":"10.1093\/bioinformatics\/btx304","volume":"33","author":"M Kokot","year":"2017","unstructured":"Kokot, M., D\u0142ugosz, M. & Deorowicz, S. KMC 3: counting and manipulating k-mer statistics. Bioinformatics 33, 2759\u20132761 (2017).","journal-title":"Bioinformatics"},{"key":"30173_CR60","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-14998-3","volume":"11","author":"TR Ranallo-Benavidez","year":"2020","unstructured":"Ranallo-Benavidez, T. R., Jaron, K. S. & Schatz, M. C. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat. Commun. 11, 1432 (2020).","journal-title":"Nat. Commun."},{"key":"30173_CR61","doi-asserted-by":"publisher","first-page":"2669","DOI":"10.1093\/bioinformatics\/btt476","volume":"29","author":"AV Zimin","year":"2013","unstructured":"Zimin, A. V. et al. The MaSuRCA genome assembler. Bioinformatics 29, 2669\u20132677 (2013).","journal-title":"Bioinformatics"},{"key":"30173_CR62","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-13-S14-S8","volume":"13","author":"F Nadalin","year":"2012","unstructured":"Nadalin, F., Vezzi, F. & Policriti, A. GapFiller: a de novo assembly approach to fill the gap within paired reads. BMC Bioinformatics 13, S8 (2012).","journal-title":"BMC Bioinformatics"},{"key":"30173_CR63","doi-asserted-by":"publisher","DOI":"10.1186\/gb-2010-11-4-r41","volume":"11","author":"IJ Tsai","year":"2010","unstructured":"Tsai, I. J., Otto, T. D. & Berriman, M. Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biol. 11, R41 (2010).","journal-title":"Genome Biol."},{"key":"30173_CR64","doi-asserted-by":"publisher","first-page":"1704","DOI":"10.1093\/bioinformatics\/btq269","volume":"26","author":"TD Otto","year":"2010","unstructured":"Otto, T. D., Sanders, M., Berriman, M. & Newbold, C. Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 26, 1704\u20131707 (2010).","journal-title":"Bioinformatics"},{"key":"30173_CR65","doi-asserted-by":"publisher","first-page":"540","DOI":"10.1038\/s41587-019-0072-8","volume":"37","author":"M Kolmogorov","year":"2019","unstructured":"Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P. A. Assembly of long, error-prone reads using repeat graphs. Nat. Biotechnol. 37, 540\u2013546 (2019).","journal-title":"Nat. Biotechnol."},{"key":"30173_CR66","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1126\/science.aal3327","volume":"356","author":"O Dudchenko","year":"2017","unstructured":"Dudchenko, O. et al. De novo assembly of the Aedes aegypti genome using Hi-C yields chromosome-length scaffolds. Science 356, 92\u201395 (2017).","journal-title":"Science"},{"key":"30173_CR67","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-42570-7","volume":"9","author":"SE Tanaka","year":"2019","unstructured":"Tanaka, S. E. et al. Stage-specific transcriptome of Bursaphelenchus xylophilus reveals temporal regulation of effector genes and roles of the dauer-like stages in the lifecycle. Sci. Rep. 9, 6080 (2019).","journal-title":"Sci. Rep."},{"key":"30173_CR68","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-019-1832-y","volume":"20","author":"DM Emms","year":"2019","unstructured":"Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238 (2019).","journal-title":"Genome Biol."},{"key":"30173_CR69","doi-asserted-by":"publisher","first-page":"867","DOI":"10.1093\/bioinformatics\/btx699","volume":"34","author":"BS Pedersen","year":"2018","unstructured":"Pedersen, B. S. & Quinlan, A. R. Mosdepth: quick coverage calculation for genomes and exomes. Bioinformatics 34, 867\u2013868 (2018).","journal-title":"Bioinformatics"},{"key":"30173_CR70","doi-asserted-by":"publisher","first-page":"e1004873","DOI":"10.1371\/journal.pcbi.1004873","volume":"12","author":"E Talevich","year":"2016","unstructured":"Talevich, E., Shain, A. H., Botton, T. & Bastian, B. C. CNVkit: genome-wide copy number detection and visualization from targeted DNA sequencing. PLoS Comput. Biol. 12, e1004873 (2016).","journal-title":"PLoS Comput. Biol."},{"key":"30173_CR71","doi-asserted-by":"publisher","first-page":"1297","DOI":"10.1101\/gr.107524.110","volume":"20","author":"A McKenna","year":"2010","unstructured":"McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297\u20131303 (2010).","journal-title":"Genome Res."},{"key":"30173_CR72","doi-asserted-by":"publisher","first-page":"2156","DOI":"10.1093\/bioinformatics\/btr330","volume":"27","author":"P Danecek","year":"2011","unstructured":"Danecek, P. et al. 1000 Genomes project analysis group. the variant call format and VCFtools. Bioinformatics 27, 2156\u20132158 (2011).","journal-title":"Bioinformatics"},{"key":"30173_CR73","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-13-637","volume":"13","author":"S Baldwin","year":"2012","unstructured":"Baldwin, S. et al. A toolkit for bulk PCR-based marker design from next-generation sequence data: application for development of a framework linkage map in bulb onion (Allium cepa L.). BMC Genomics 13, 637 (2012).","journal-title":"BMC Genomics"},{"key":"30173_CR74","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.3317","volume":"12","author":"D Kim","year":"2015","unstructured":"Kim, D., Langmead, B. & Salzberg, S. HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12, 357\u2013360 (2015).","journal-title":"Nat. Methods"},{"key":"30173_CR75","doi-asserted-by":"publisher","first-page":"166","DOI":"10.1093\/bioinformatics\/btu638","volume":"31","author":"S Anders","year":"2015","unstructured":"Anders, S., Pyl, P. T. & Huber, W. HTSeq\u2013a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166\u2013169 (2015).","journal-title":"Bioinformatics"},{"key":"30173_CR76","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","volume":"26","author":"MD Robinson","year":"2010","unstructured":"Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139\u2013140 (2010).","journal-title":"Bioinformatics"},{"key":"30173_CR77","doi-asserted-by":"publisher","first-page":"562","DOI":"10.1038\/nprot.2012.016","volume":"7","author":"C Trapnell","year":"2012","unstructured":"Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562\u2013578 (2012).","journal-title":"Nat. Protoc."},{"key":"30173_CR78","first-page":"176","volume":"47","author":"R Shinya","year":"2015","unstructured":"Shinya, R., Chen, A. & Sternberg, P. W. Sex attraction and mating in Bursaphelenchus okinawaensis and B. xylophilus. J. Nematol. 47, 176\u2013183 (2015).","journal-title":"J. Nematol."}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41467-022-30173-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-022-30173-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-022-30173-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,24]],"date-time":"2022-11-24T17:05:05Z","timestamp":1669309505000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41467-022-30173-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,11]]},"references-count":78,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["30173"],"URL":"https:\/\/doi.org\/10.1038\/s41467-022-30173-2","relation":{},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,11]]},"assertion":[{"value":"24 August 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 April 2022","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"11 May 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"2574"}}