{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,5]],"date-time":"2026-07-05T04:05:09Z","timestamp":1783224309896,"version":"3.54.6"},"reference-count":87,"publisher":"Oxford University Press (OUP)","issue":"4","license":[{"start":{"date-parts":[[2024,12,12]],"date-time":"2024-12-12T00:00:00Z","timestamp":1733961600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01GM118836"],"award-info":[{"award-number":["R01GM118836"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"NIH","doi-asserted-by":"publisher","award":["R01GM121688"],"award-info":[{"award-number":["R01GM121688"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000048","name":"American Cancer Society","doi-asserted-by":"publisher","award":["126627-PF-15-228-01-DDC"],"award-info":[{"award-number":["126627-PF-15-228-01-DDC"]}],"id":[{"id":"10.13039\/100000048","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,4,17]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Sexual characteristics and reproductive systems are dynamic traits in many taxa, but the developmental modifications that allow change and innovation are largely unknown. A leading model for this process is the evolution of self-fertile hermaphrodites from male\/female ancestors. However, these studies require direct analysis of sex determination in male\/female species, as well as in the hermaphroditic species that are related to them. In Caenorhabditis nematodes, this has only become possible recently, with the discovery of new species. Here, we use gene editing to characterize major sex determination genes in Caenorhabditis nigoni, a sister to the widely studied hermaphroditic species Caenorhabditis briggsae. These 2 species are close enough to mate and form partially fertile hybrids. First, we find that tra-1 functions as the master regulator of sex in C. nigoni, in both the soma and the germ line. Surprisingly, these mutants make only sperm, in contrast to tra-1 mutants in related hermaphroditic species. Moreover, the XX mutants display a unique defect in somatic gonad development that is not seen elsewhere in the genus. Second, the fem-3 gene acts upstream of tra-1 in C. nigoni, and the mutants are females, unlike in the sister species C. briggsae, where they develop as hermaphrodites. This result points to a divergence in the role of fem-3 in the germ line of these species. Third, tra-2 encodes a transmembrane receptor that acts upstream of fem-3 in C. nigoni. Outside of the germ line, tra-2 mutations in all species cause a similar pattern of partial masculinization. However, heterozygosity for tra-2 does not alter germ cell fates in C. nigoni, as it can in sensitized backgrounds of 2 hermaphroditic species of Caenorhabditis. Finally, the epistatic relationships point to a simple, linear germline pathway in which tra-2 regulates fem-3 which regulates tra-1, unlike the more complex relationships seen in hermaphrodite germ cell development. Taking these results together, the regulation of sex determination is more robust and streamlined in the male\/female species C. nigoni than in related species that make self-fertile hermaphrodites, a conclusion supported by studies of interspecies hybrids using sex determination mutations. Thus, we infer that the origin of self-fertility not only required mutations that activated the spermatogenesis program in XX germ lines, but prior to these there must have been mutations that decanalized the sex determination process, allowing for subsequent changes to germ cell fates.<\/jats:p>","DOI":"10.1093\/genetics\/iyae207","type":"journal-article","created":{"date-parts":[[2024,12,12]],"date-time":"2024-12-12T08:03:10Z","timestamp":1733990590000},"source":"Crossref","is-referenced-by-count":4,"title":["Robust sex determination in the <i>Caenorhabditis nigoni<\/i> germ line"],"prefix":"10.1093","volume":"229","author":[{"given":"Jonathan P","family":"Harbin","sequence":"first","affiliation":[{"name":"Department of Molecular Biology, Rowan-Virtua School of Translational Biomedical Engineering and Sciences , Stratford, NJ 08084 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yongquan","family":"Shen","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Rowan-Virtua School of Translational Biomedical Engineering and Sciences , Stratford, NJ 08084 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shin-Yi","family":"Lin","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Rowan-Virtua School of Osteopathic Medicine , Stratford, NJ 08084 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kevin","family":"Kemper","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Rowan-Virtua School of Translational Biomedical Engineering and Sciences , Stratford, NJ 08084 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eric S","family":"Haag","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Maryland , College Park, MD 20742 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3151-4381","authenticated-orcid":false,"given":"Erich M","family":"Schwarz","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology and Genetics, Cornell University , Ithaca, NY 14853 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ronald E","family":"Ellis","sequence":"additional","affiliation":[{"name":"Department of Molecular Biology, Rowan-Virtua School of Translational Biomedical Engineering and Sciences , Stratford, NJ 08084 ,","place":["USA"]},{"name":"Department of Molecular Biology, Rowan-Virtua School of Osteopathic Medicine , Stratford, NJ 08084 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2024,12,12]]},"reference":[{"issue":"6307","key":"2025042112364985900_iyae207-B1","doi-asserted-by":"publisher","first-page":"346","DOI":"10.1038\/349346a0","article-title":"Control of the sperm-oocyte switch in Caenorhabditis elegans hermaphrodites by the fem-3 3","volume":"349","author":"Ahringer","year":"1991","journal-title":"Nature"},{"issue":"1","key":"2025042112364985900_iyae207-B2","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1186\/s13059-022-02823-7","article-title":"Automated assembly scaffolding using RagTag elevates a new tomato system for high-throughput genome editing","volume":"23","author":"Alonge","year":"2022","journal-title":"Genome Biol"},{"issue":"5955","key":"2025042112364985900_iyae207-B3","doi-asserted-by":"publisher","first-page":"1002","DOI":"10.1126\/science.1176013","article-title":"Mutations in two independent pathways are sufficient to create hermaphroditic nematodes","volume":"326","author":"Baldi","year":"2009","journal-title":"Science"},{"issue":"1","key":"2025042112364985900_iyae207-B4","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1093\/genetics\/115.1.107","article-title":"Gain-of-function mutations of fem-3, a sex-determination gene in Caenorhabditis elegans","volume":"115","author":"Barton","year":"1987","journal-title":"Genetics"},{"issue":"40","key":"2025042112364985900_iyae207-B5","doi-asserted-by":"publisher","first-page":"16033","DOI":"10.1073\/pnas.1312087110","article-title":"TRA-1 ChIP-seq reveals regulators of sexual differentiation and multilevel feedback in nematode sex determination","volume":"110","author":"Berkseth","year":"2013","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"4","key":"2025042112364985900_iyae207-B6","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1261\/rna.7255805","article-title":"Binding specificity and mRNA targets of a C. elegans PUF protein, FBF-1","volume":"11","author":"Bernstein","year":"2005","journal-title":"RNA"},{"issue":"3","key":"2025042112364985900_iyae207-B7","doi-asserted-by":"publisher","first-page":"801","DOI":"10.1534\/genetics.119.302202","article-title":"Specific interactions between autosome and X chromosomes cause hybrid male sterility in Caenorhabditis species","volume":"212","author":"Bi","year":"2019","journal-title":"Genetics"},{"issue":"1","key":"2025042112364985900_iyae207-B8","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1093\/genetics\/77.1.71","article-title":"The genetics of Caenorhabditis elegans","volume":"77","author":"Brenner","year":"1974","journal-title":"Genetics"},{"issue":"Suppl 1","key":"2025042112364985900_iyae207-B9","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1093\/humrep\/13.suppl_1.45","article-title":"Chromosome anomalies and Y chromosome microdeletions as causal factors in male infertility","volume":"13","author":"Chandley","year":"1998","journal-title":"Hum Reprod"},{"issue":"6","key":"2025042112364985900_iyae207-B10","doi-asserted-by":"publisher","first-page":"1425","DOI":"10.1242\/dev.01012","article-title":"A forkhead protein controls sexual identity of the C. elegans male somatic gonad","volume":"131","author":"Chang","year":"2004","journal-title":"Development"},{"issue":"2","key":"2025042112364985900_iyae207-B11","doi-asserted-by":"publisher","first-page":"e107","DOI":"10.1002\/imt2.107","article-title":"Ultrafast one-pass FASTQ data preprocessing, quality control, and deduplication using fastp","volume":"2","author":"Chen","year":"2023","journal-title":"Imeta"},{"issue":"4","key":"2025042112364985900_iyae207-B12","doi-asserted-by":"publisher","first-page":"1513","DOI":"10.1093\/genetics\/158.4.1513","article-title":"Specification of germ cell fates by FOG-3 has been conserved during nematode evolution","volume":"158","author":"Chen","year":"2001","journal-title":"Genetics"},{"issue":"14","key":"2025042112364985900_iyae207-B13","doi-asserted-by":"publisher","first-page":"3119","DOI":"10.1242\/dev.127.14.3119","article-title":"TRA-1A regulates transcription of fog-3, which controls germ cell fate in C. elegans","volume":"127","author":"Chen","year":"2000","journal-title":"Development"},{"issue":"24","key":"2025042112364985900_iyae207-B14","doi-asserted-by":"publisher","first-page":"5265","DOI":"10.1242\/dev.127.24.5265","article-title":"FOG-2, a novel F-box containing protein, associates with the GLD-1 RNA binding protein and directs male sex determination in the C. elegans hermaphrodite germline","volume":"127","author":"Clifford","year":"2000","journal-title":"Development"},{"issue":"1","key":"2025042112364985900_iyae207-B15","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1534\/genetics.119.300244","article-title":"Males, outcrossing, and sexual selection in Caenorhabditis nematodes","volume":"213","author":"Cutter","year":"2019","journal-title":"Genetics"},{"issue":"27","key":"2025042112364985900_iyae207-B16","doi-asserted-by":"publisher","first-page":"11056","DOI":"10.1073\/pnas.1303057110","article-title":"Molecular hyperdiversity defines populations of the nematode Caenorhabditis brenneri","volume":"110","author":"Dey","year":"2013","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"6","key":"2025042112364985900_iyae207-B17","doi-asserted-by":"publisher","first-page":"1339","DOI":"10.1111\/j.1558-5646.2007.00118.x","article-title":"Inbreeding and outbreeding depression in Caenorhabditis nematodes","volume":"61","author":"Dolgin","year":"2007","journal-title":"Evolution"},{"issue":"1","key":"2025042112364985900_iyae207-B18","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1093\/genetics\/114.1.53","article-title":"Activity of the sex-determining gene tra-2 is modulated to allow spermatogenesis in the C. elegans hermaphrodite","volume":"114","author":"Doniach","year":"1986","journal-title":"Genetics"},{"issue":"2","key":"2025042112364985900_iyae207-B19","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1002\/mrd.22668","article-title":"The persistence of memory - hermaphroditism in nematodes","volume":"84","author":"Ellis","year":"2017","journal-title":"Mol Reprod Dev"},{"issue":"5-6","key":"2025042112364985900_iyae207-B20","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1159\/000520872","article-title":"Sex determination in nematode germ cells","volume":"16","author":"Ellis","year":"2022","journal-title":"Sex Dev"},{"key":"2025042112364985900_iyae207-B21","doi-asserted-by":"publisher","first-page":"62","DOI":"10.12703\/P6-62","article-title":"The evolutionary origins and consequences of self-fertility in nematodes","volume":"6","author":"Ellis","year":"2014","journal-title":"F1000Prime Rep"},{"key":"2025042112364985900_iyae207-B22","doi-asserted-by":"publisher","DOI":"10.1895\/wormbook.1.93.2","article-title":"SNPs: introduction and two-point mapping","author":"Fay","year":"2008","journal-title":"WormBook"},{"issue":"8","key":"2025042112364985900_iyae207-B23","doi-asserted-by":"publisher","first-page":"483","DOI":"10.1038\/nrg3949","article-title":"Pervasive robustness in biological systems","volume":"16","author":"F\u00e9lix","year":"2015","journal-title":"Nat Rev Genet"},{"issue":"4","key":"2025042112364985900_iyae207-B24","doi-asserted-by":"publisher","first-page":"e94723","DOI":"10.1371\/journal.pone.0094723","article-title":"A streamlined system for species diagnosis in Caenorhabditis (Nematoda: Rhabditidae) with name designations for 15 distinct biological species","volume":"9","author":"F\u00e9lix","year":"2014","journal-title":"PLoS One"},{"issue":"6","key":"2025042112364985900_iyae207-B25","doi-asserted-by":"publisher","first-page":"e1005323","DOI":"10.1371\/journal.pgen.1005323","article-title":"Reproductive mode and the evolution of genome size and structure in Caenorhabditis nematodes","volume":"11","author":"Fierst","year":"2015","journal-title":"PLoS Genet"},{"issue":"2","key":"2025042112364985900_iyae207-B26","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1163\/187529283X00456","article-title":"Comparison of a new wild-type Caenorhabditis briggsae with laboratory strains of C. briggsae and C. elegans","volume":"29","author":"Fodor","year":"1983","journal-title":"Nematologica"},{"issue":"11","key":"2025042112364985900_iyae207-B27","doi-asserted-by":"publisher","first-page":"3087","DOI":"10.1111\/evo.12203","article-title":"Outbreeding depression with low genetic variation in selfing Caenorhabditis nematodes","volume":"67","author":"Gimond","year":"2013","journal-title":"Evolution"},{"issue":"2","key":"2025042112364985900_iyae207-B28","doi-asserted-by":"publisher","first-page":"329","DOI":"10.1016\/0092-8674(93)80074-O","article-title":"Translational regulation of tra-2 by its 3'-untranslated region controls sexual identity in C. elegans","volume":"75","author":"Goodwin","year":"1993","journal-title":"Cell"},{"issue":"21","key":"2025042112364985900_iyae207-B29","doi-asserted-by":"publisher","first-page":"1853","DOI":"10.1016\/j.cub.2009.09.042","article-title":"Independent recruitment of F box genes to regulate hermaphrodite development during nematode evolution","volume":"19","author":"Guo","year":"2009","journal-title":"Curr Biol"},{"issue":"1","key":"2025042112364985900_iyae207-B30","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1007\/s10709-006-0032-3","article-title":"Compensatory vs. pseudocompensatory evolution in molecular and developmental interactions","volume":"129","author":"Haag","year":"2007","journal-title":"Genetica"},{"issue":"1","key":"2025042112364985900_iyae207-B31","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1093\/genetics\/155.1.105","article-title":"Regulatory elements required for development of Caenorhabditis elegans hermaphrodites are conserved in the tra-2 homologue of C. remanei, a male\/female sister species","volume":"155","author":"Haag","year":"2000","journal-title":"Genetics"},{"issue":"5","key":"2025042112364985900_iyae207-B32","doi-asserted-by":"publisher","first-page":"837","DOI":"10.1016\/0092-8674(91)90391-B","article-title":"Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans","volume":"65","author":"Hall","year":"1991","journal-title":"Cell"},{"key":"2025042112364985900_iyae207-B33","doi-asserted-by":"publisher","first-page":"10.17912\/micropub.biology.000968","DOI":"10.17912\/micropub.biology.000968","article-title":"Efficient production of CRISPR\/Cas9 gene knockouts in the male\/female nematode Caenorhabditis nigoni","volume":"2023","author":"Harbin","year":"2023","journal-title":"MicroPubl Biol"},{"issue":"2","key":"2025042112364985900_iyae207-B34","doi-asserted-by":"publisher","first-page":"561","DOI":"10.1139\/g89-105","article-title":"Y chromosomal fertility genes of Drosophila: a new type of eukaryotic genes","volume":"31","author":"Hennig","year":"1989","journal-title":"Genome"},{"issue":"4","key":"2025042112364985900_iyae207-B35","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1016\/j.devcel.2006.02.002","article-title":"Genetic flexibility in the convergent evolution of hermaphroditism in Caenorhabditis nematodes","volume":"10","author":"Hill","year":"2006","journal-title":"Dev Cell"},{"issue":"4","key":"2025042112364985900_iyae207-B36","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1111\/j.1525-142X.2009.00340.x","article-title":"A sensitized genetic background reveals evolution near the terminus of the Caenorhabditis germline sex determination pathway","volume":"11","author":"Hill","year":"2009","journal-title":"Evol Dev"},{"issue":"3","key":"2025042112364985900_iyae207-B37","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1093\/genetics\/96.3.649","article-title":"More sex-determination mutants of Caenorhabditis elegans","volume":"96","author":"Hodgkin","year":"1980","journal-title":"Genetics"},{"issue":"1","key":"2025042112364985900_iyae207-B38","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1093\/genetics\/114.1.15","article-title":"Sex determination in the nematode C. elegans: analysis of tra-3 suppressors and characterization of fem genes","volume":"114","author":"Hodgkin","year":"1986","journal-title":"Genetics"},{"issue":"7","key":"2025042112364985900_iyae207-B39","doi-asserted-by":"publisher","first-page":"731","DOI":"10.1101\/gad.1.7.731","article-title":"A genetic analysis of the sex-determining gene, tra-1, in the nematode Caenorhabditis elegans","volume":"1","author":"Hodgkin","year":"1987","journal-title":"Genes Dev"},{"issue":"2","key":"2025042112364985900_iyae207-B40","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1093\/genetics\/86.2.275","article-title":"Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans","volume":"86","author":"Hodgkin","year":"1977","journal-title":"Genetics"},{"issue":"1","key":"2025042112364985900_iyae207-B41","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.devcel.2016.06.016","article-title":"Variable cell growth yields reproducible OrganDevelopment through spatiotemporal averaging","volume":"38","author":"Hong","year":"2016","journal-title":"Dev Cell"},{"issue":"2","key":"2025042112364985900_iyae207-B42","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/j.ydbio.2018.11.024","article-title":"Multi-modal regulation of C. elegans hermaphrodite spermatogenesis by the GLD-1-FOG-2 complex","volume":"446","author":"Hu","year":"2019","journal-title":"Dev Biol"},{"issue":"6360","key":"2025042112364985900_iyae207-B43","doi-asserted-by":"publisher","first-page":"551","DOI":"10.1038\/355551a0","article-title":"Evidence from mosaic analysis of the masculinizing gene her-1 for cell interactions in C. elegans sex determination","volume":"355","author":"Hunter","year":"1992","journal-title":"Nature"},{"issue":"4","key":"2025042112364985900_iyae207-B44","doi-asserted-by":"publisher","first-page":"e18638","DOI":"10.1371\/journal.pone.0018638","article-title":"A novel signaling pathway mediated by the nuclear targeting of C-terminal fragments of mammalian patched 1","volume":"6","author":"Kagawa","year":"2011","journal-title":"PLoS One"},{"issue":"11","key":"2025042112364985900_iyae207-B45","doi-asserted-by":"publisher","first-page":"e2002429","DOI":"10.1371\/journal.pbio.2002429","article-title":"Stochastic loss and gain of symmetric divisions in the C. elegans epidermis perturbs robustness of stem cell number","volume":"15","author":"Katsanos","year":"2017","journal-title":"PLoS Biol"},{"issue":"3","key":"2025042112364985900_iyae207-B46","doi-asserted-by":"publisher","first-page":"1415","DOI":"10.1534\/genetics.107.073668","article-title":"Comparative genetics of sex determination: masculinizing mutations in Caenorhabditis briggsae","volume":"178","author":"Kelleher","year":"2008","journal-title":"Genetics"},{"issue":"1","key":"2025042112364985900_iyae207-B47","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1186\/1471-2148-11-339","article-title":"A phylogeny and molecular barcodes for Caenorhabditis, with numerous new species from rotting fruits","volume":"11","author":"Kiontke","year":"2011","journal-title":"BMC Evol Biol"},{"issue":"11","key":"2025042112364985900_iyae207-B48","doi-asserted-by":"publisher","first-page":"826","DOI":"10.1038\/nrg1471","article-title":"Biological robustness","volume":"5","author":"Kitano","year":"2004","journal-title":"Nat Rev Genet"},{"issue":"4","key":"2025042112364985900_iyae207-B49","doi-asserted-by":"publisher","first-page":"461","DOI":"10.1091\/mbc.3.4.461","article-title":"tra-2 encodes a membrane protein and may mediate cell communication in the Caenorhabditis elegans sex determination pathway","volume":"3","author":"Kuwabara","year":"1992","journal-title":"Mol Biol Cell"},{"issue":"24","key":"2025042112364985900_iyae207-B50","doi-asserted-by":"publisher","first-page":"3153","DOI":"10.1101\/gad.853700","article-title":"Direct protein-protein interaction between the intracellular domain of TRA-2 and the transcription factor TRA-1A modulates feminizing activity in C. elegans","volume":"14","author":"Lum","year":"2000","journal-title":"Genes Dev"},{"key":"2025042112364985900_iyae207-B51","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1016\/j.mex.2015.02.002","article-title":"Rapid RNA analysis of individual Caenorhabditis elegans","volume":"2","author":"Ly","year":"2015","journal-title":"MethodsX"},{"issue":"17","key":"2025042112364985900_iyae207-B52","doi-asserted-by":"publisher","first-page":"4333","DOI":"10.1242\/dev.01288","article-title":"TRA-1\/GLI controls development of somatic gonadal precursors in C. elegans","volume":"131","author":"Mathies","year":"2004","journal-title":"Development"},{"key":"2025042112364985900_iyae207-B53","doi-asserted-by":"publisher","first-page":"101912","DOI":"10.1016\/j.gde.2022.101912","article-title":"The X chromosome in C. elegans sex determination and dosage compensation","volume":"74","author":"Meyer","year":"2022","journal-title":"Curr Opin Genet Dev"},{"issue":"1","key":"2025042112364985900_iyae207-B54","doi-asserted-by":"publisher","first-page":"167","DOI":"10.1016\/0092-8674(88)90019-0","article-title":"xol-1: a gene that controls the male modes of both sex determination and X chromosome dosage compensation in C. elegans","volume":"55","author":"Miller","year":"1988","journal-title":"Cell"},{"issue":"1","key":"2025042112364985900_iyae207-B55","doi-asserted-by":"publisher","first-page":"e6","DOI":"10.1371\/journal.pbio.0030006","article-title":"fog-2 and the evolution of self-fertile hermaphroditism in Caenorhabditis","volume":"3","author":"Nayak","year":"2005","journal-title":"PLoS Biol"},{"issue":"5","key":"2025042112364985900_iyae207-B56","doi-asserted-by":"publisher","first-page":"261","DOI":"10.1016\/j.tree.2015.03.006","article-title":"Sperm storage: distinguishing selective processes and evaluating criteria","volume":"30","author":"Orr","year":"2015","journal-title":"Trends Ecol Evol"},{"issue":"9","key":"2025042112364985900_iyae207-B57","doi-asserted-by":"publisher","first-page":"2018","DOI":"10.1111\/mec.13087","article-title":"Evolution of the mating system in colonizing plants","volume":"24","author":"Pannell","year":"2015","journal-title":"Mol Ecol"},{"issue":"2","key":"2025042112364985900_iyae207-B58","doi-asserted-by":"publisher","first-page":"216","DOI":"10.1101\/gad.7.2.216","article-title":"Molecular characterization of the her-1 gene suggests a direct role in cell signaling during Caenorhabditis elegans sex determination","volume":"7","author":"Perry","year":"1993","journal-title":"Genes Dev"},{"key":"2025042112364985900_iyae207-B59","doi-asserted-by":"publisher","first-page":"ISCB Comm J-304","DOI":"10.12688\/f1000research.23297.1","article-title":"GFF utilities: GffRead and GffCompare","volume":"9","author":"Pertea","year":"2020","journal-title":"F1000Res"},{"key":"2025042112364985900_iyae207-B60","doi-asserted-by":"publisher","first-page":"669045","DOI":"10.3389\/fgene.2021.669045","article-title":"Hybrid sterility, genetic conflict and complex speciation: lessons from the Drosophila simulans clade species","volume":"12","author":"Presgraves","year":"2021","journal-title":"Front Genet"},{"issue":"1","key":"2025042112364985900_iyae207-B61","doi-asserted-by":"publisher","first-page":"e102","DOI":"10.1002\/cpbi.102","article-title":"Using SPAdes de novo assembler","volume":"70","author":"Prjibelski","year":"2020","journal-title":"Curr Protoc Bioinformatics"},{"issue":"3","key":"2025042112364985900_iyae207-B62","doi-asserted-by":"publisher","first-page":"e1009409","DOI":"10.1371\/journal.pgen.1009409","article-title":"Widespread misregulation of inter-species hybrid transcriptomes due to sex-specific and sex-chromosome regulatory evolution","volume":"17","author":"S\u00e1nchez-Ram\u00edrez","year":"2021","journal-title":"PLoS Genet"},{"issue":"4","key":"2025042112364985900_iyae207-B63","doi-asserted-by":"publisher","first-page":"755","DOI":"10.1093\/genetics\/123.4.755","article-title":"Analysis of the role of tra-1 in germline sex determination in the nematode Caenorhabditis elegans","volume":"123","author":"Schedl","year":"1989","journal-title":"Genetics"},{"issue":"1","key":"2025042112364985900_iyae207-B64","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1093\/genetics\/119.1.43","article-title":"fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans","volume":"119","author":"Schedl","year":"1988","journal-title":"Genetics"},{"issue":"5","key":"2025042112364985900_iyae207-B65","doi-asserted-by":"publisher","first-page":"733","DOI":"10.1016\/j.devcel.2006.09.017","article-title":"The C. elegans sex-determining GLI protein TRA-1A is regulated by sex-specific proteolysis","volume":"11","author":"Schvarzstein","year":"2006","journal-title":"Dev Cell"},{"issue":"7","key":"2025042112364985900_iyae207-B66","doi-asserted-by":"publisher","first-page":"1287","DOI":"10.1111\/jeb.12424","article-title":"Sex uncovered: the evolutionary biology of reproductive systems","volume":"27","author":"Schwander","year":"2014","journal-title":"J Evol Biol"},{"issue":"6","key":"2025042112364985900_iyae207-B67","doi-asserted-by":"publisher","first-page":"msae101","DOI":"10.1093\/molbev\/msae101","article-title":"Rewiring the sex-determination pathway during the evolution of self-fertility","volume":"41","author":"Shen","year":"2024","journal-title":"Mol Biol Evol"},{"key":"2025042112364985900_iyae207-B501","article-title":"The Caenorhabditis Gli protein TRA-1 makes a transcriptional activator that promotes spermatogenesis","author":"Shen","year":"2024"},{"issue":"12","key":"2025042112364985900_iyae207-B68","doi-asserted-by":"publisher","first-page":"1639","DOI":"10.1093\/bioinformatics\/btaa1016","article-title":"Liftoff: accurate mapping of gene annotations","volume":"37","author":"Shumate","year":"2021","journal-title":"Bioinformatics"},{"issue":"1","key":"2025042112364985900_iyae207-B69","doi-asserted-by":"publisher","first-page":"127","DOI":"10.1016\/j.devcel.2007.05.008","article-title":"A CUL-2 ubiquitin ligase containing three FEM proteins degrades TRA-1 to regulate C. elegans sex determination","volume":"13","author":"Starostina","year":"2007","journal-title":"Dev Cell"},{"issue":"3","key":"2025042112364985900_iyae207-B70","doi-asserted-by":"publisher","first-page":"a018366","DOI":"10.1101\/cshperspect.a018366","article-title":"Regulation of the X chromosomes in Caenorhabditis elegans","volume":"6","author":"Strome","year":"2014","journal-title":"Cold Spring Harb Perspect Biol"},{"issue":"1","key":"2025042112364985900_iyae207-B71","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/0925-4773(91)90090-S","article-title":"Sex-specific transcriptional regulation of the C. elegans sex-determining gene her-1","volume":"34","author":"Trent","year":"1991","journal-title":"Mech Dev"},{"issue":"3","key":"2025042112364985900_iyae207-B72","doi-asserted-by":"publisher","first-page":"297","DOI":"10.1086\/688097","article-title":"Evolution of sex-biased dispersal","volume":"91","author":"Trochet","year":"2016","journal-title":"Q Rev Biol"},{"issue":"2","key":"2025042112364985900_iyae207-B73","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1046\/j.1525-142x.2001.003002109.x","article-title":"Developmental system drift and flexibility in evolutionary trajectories","volume":"3","author":"True","year":"2001","journal-title":"Evol Dev"},{"issue":"7","key":"2025042112364985900_iyae207-B74","doi-asserted-by":"publisher","first-page":"1793","DOI":"10.3390\/cells10071793","article-title":"Fisher vs. the worms: extraordinary sex ratios in nematodes and the mechanisms that produce them","volume":"10","author":"Van Goor","year":"2021","journal-title":"Cells"},{"issue":"7","key":"2025042112364985900_iyae207-B75","doi-asserted-by":"publisher","first-page":"1372","DOI":"10.1111\/jeb.12372","article-title":"The evolution of selfing from outcrossing ancestors in Brassicaceae: what have we learned from variation at the S-locus","volume":"27","author":"Vekemans","year":"2014","journal-title":"J Evol Biol"},{"issue":"6","key":"2025042112364985900_iyae207-B76","doi-asserted-by":"publisher","first-page":"1363","DOI":"10.1093\/emboj\/20.6.1363","article-title":"The TRA-1 transcription factor binds TRA-2 to regulate sexual fates in Caenorhabditis elegans","volume":"20","author":"Wang","year":"2001","journal-title":"EMBO J"},{"issue":"12","key":"2025042112364985900_iyae207-B77","doi-asserted-by":"publisher","first-page":"3670","DOI":"10.1111\/j.1558-5646.2012.01714.x","article-title":"The role of androdioecy and gynodioecy in mediating evolutionary transitions between dioecy and hermaphroditism in the animalia","volume":"66","author":"Weeks","year":"2012","journal-title":"Evolution"},{"issue":"2","key":"2025042112364985900_iyae207-B78","doi-asserted-by":"publisher","first-page":"468","DOI":"10.1093\/molbev\/mst213","article-title":"Rapid creation of forward-genetics tools for C. briggsae using TALENs: lessons for nonmodel organisms","volume":"31","author":"Wei","year":"2014","journal-title":"Mol Biol Evol"},{"issue":"1","key":"2025042112364985900_iyae207-B79","doi-asserted-by":"publisher","first-page":"5888","DOI":"10.1038\/ncomms6888","article-title":"Co-option of alternate sperm activation programs in the evolution of self-fertile nematodes","volume":"5","author":"Wei","year":"2014","journal-title":"Nat Commun"},{"key":"2025042112364985900_iyae207-B503","author":"Wood","year":"1988"},{"issue":"3","key":"2025042112364985900_iyae207-B80","doi-asserted-by":"publisher","first-page":"997","DOI":"10.1534\/genetics.110.120550","article-title":"Insights into species divergence and the evolution of hermaphroditism from fertile interspecies hybrids of Caenorhabditis nematodes","volume":"186","author":"Woodruff","year":"2010","journal-title":"Genetics"},{"issue":"11\u201312","key":"2025042112364985900_iyae207-B81","doi-asserted-by":"publisher","first-page":"2015","DOI":"10.1101\/gr.277205.122","article-title":"Genetic exchange with an outcrossing sister species causes severe genome-wide dysregulation in a selfing Caenorhabditis nematode","volume":"32","author":"Xie","year":"2022","journal-title":"Genome Res"},{"issue":"6371","key":"2025042112364985900_iyae207-B82","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1126\/science.aao0827","article-title":"Rapid genome shrinkage in a self-fertile nematode reveals sperm competition proteins","volume":"359","author":"Yin","year":"2018","journal-title":"Science"},{"key":"2025042112364985900_iyae207-B83","doi-asserted-by":"publisher","DOI":"10.1895\/wormbook.1.84.1","article-title":"Somatic sex determination","author":"Zarkower","year":"2006","journal-title":"WormBook"},{"issue":"2","key":"2025042112364985900_iyae207-B84","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1016\/0092-8674(92)90099-X","article-title":"Molecular analysis of the C. elegans sex-determining gene tra-1: a gene encoding two zinc finger proteins","volume":"70","author":"Zarkower","year":"1992","journal-title":"Cell"},{"issue":"6659","key":"2025042112364985900_iyae207-B85","doi-asserted-by":"publisher","first-page":"477","DOI":"10.1038\/37297","article-title":"A conserved RNA-binding protein that regulates sexual fates in the C. elegans hermaphrodite germ line","volume":"390","author":"Zhang","year":"1997","journal-title":"Nature"}],"container-title":["GENETICS"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/genetics\/advance-article-pdf\/doi\/10.1093\/genetics\/iyae207\/61080156\/iyae207.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/229\/4\/iyae207\/61080156\/iyae207.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/genetics\/article-pdf\/229\/4\/iyae207\/61080156\/iyae207.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,4,21]],"date-time":"2025-04-21T16:37:01Z","timestamp":1745253421000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/genetics\/article\/doi\/10.1093\/genetics\/iyae207\/7921911"}},"subtitle":[],"editor":[{"given":"B","family":"Conradt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2024,12,12]]},"references-count":87,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2024,12,12]]},"published-print":{"date-parts":[[2025,4,17]]}},"URL":"https:\/\/doi.org\/10.1093\/genetics\/iyae207","relation":{},"ISSN":["1943-2631"],"issn-type":[{"value":"1943-2631","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,4]]},"published":{"date-parts":[[2024,12,12]]},"article-number":"iyae207"}}