A key event in meiosis is the conversion of a small subset of double strand breaks into interhomolog crossovers. In this study, we demonstrate that Caenorhabditis elegans male spermatogenesis has less robust mechanisms than hermaphrodite oogenesis for ensuring and limiting the conversion of double strand breaks into crossovers. This is not a consequence of differences in meiotic prophase timing, sex chromosome genotype, or the presence or absence of germline apoptosis. Using the cyclin-like crossover marker COSA-1, we show that males have a linear response in converting increasing numbers of double strand breaks into crossovers, suggesting weakened crossover homeostasis. While the topoisomerase SPO-11, responsible for initiating meiotic double strand breaks, has an extended period of activity in males as in hermaphrodites, we discovered that COSA-1 foci form at the very end of meiotic prophase in the absence of SPO-11 during spermatogenesis. These COSA-1-marked sites are also independent of homologous recombination, and Topoisomerases I and II. We find that the synaptonemal complex, which holds homologs in proximity, differently modulates COSA-1 enrichment to chromosomes in the absence of SPO-11 in males and hermaphrodites. Together, these findings suggest that males have less robust crossover control and that there are previously unrecognized lesions or structures at the end of meiotic prophase in spermatocytes that can accumulate CO markers.

Biochemistry Molecular Cellular and Developmental Biology Graduate Group University of California Davis Davis California 95616

Department of Biology Faculty of Medicine Masaryk University Brno Czech Republic

Department of Molecular and Cellular Biology University of California Davis Davis California 95616

Molecular Biology Institute University of California Los Angeles Los Angeles California 90095

Molecular Cellular and Developmental Biology University of California Santa Barbara Santa Barbara California 93106

MRC Laboratory of Medical Sciences London United Kingdom

See more in PubMed

Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell. 1998;94(3):387–98. doi: 10.1016/s0092-8674(00)81481-6. PubMed DOI

Keeney S, Giroux CN, Kleckner N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell. 1997;88(3):375–84. doi: 10.1016/s0092-8674(00)81876-0. PubMed DOI

Gray S, Cohen PE. Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation. Annu Rev Genet. 2016;50:175–210. Epub 20160914. doi: 10.1146/annurev-genet-120215-035111. PubMed DOI PMC

Zickler D, Kleckner N. Meiosis: Dances Between Homologs. Annu Rev Genet. 2023;57:1–63. Epub 20231003. doi: 10.1146/annurev-genet-061323-044915. PubMed DOI

Hollis JA, Glover ML, Schlientz AJ, Cahoon CK, Bowerman B, Wignall SM, et al. Excess crossovers impede faithful meiotic chromosome segregation in C. elegans. PLoS Genet. 2020;16(9):e1009001. Epub 20200904. doi: 10.1371/journal.pgen.1009001. PubMed DOI PMC

Capilla-Perez L, Durand S, Hurel A, Lian Q, Chambon A, Taochy C, et al. The synaptonemal complex imposes crossover interference and heterochiasmy in Arabidopsis. Proc Natl Acad Sci U S A. 2021;118(12). doi: 10.1073/pnas.2023613118. PubMed DOI PMC

Libuda DE, Uzawa S, Meyer BJ, Villeneuve AM. Meiotic chromosome structures constrain and respond to designation of crossover sites. Nature. 2013;502(7473):703–6. Epub 20131009. doi: 10.1038/nature12577. PubMed DOI PMC

Voelkel-Meiman K, Cheng SY, Morehouse SJ, MacQueen AJ. Synaptonemal Complex Proteins of Budding Yeast Define Reciprocal Roles in MutSgamma-Mediated Crossover Formation. Genetics. 2016;203(3):1091–103. Epub 20160516. doi: 10.1534/genetics.115.182923. PubMed DOI PMC

Cahoon CK, Libuda DE. Leagues of their own: sexually dimorphic features of meiotic prophase I. Chromosoma. 2019;128(3):199–214. Epub 20190302. doi: 10.1007/s00412-019-00692-x. PubMed DOI PMC

Cahoon CK, Richter CM, Dayton AE, Libuda DE. Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans. Elife. 2023;12. Epub 20231005. doi: 10.7554/eLife.84538. PubMed DOI PMC

Morelli MA, Cohen PE. Not all germ cells are created equal: aspects of sexual dimorphism in mammalian meiosis. Reproduction. 2005;130(6):761–81. doi: 10.1530/rep.1.00865. PubMed DOI

Nagaoka SI, Hassold TJ, Hunt PA. Human aneuploidy: mechanisms and new insights into an age-old problem. Nat Rev Genet. 2012;13(7):493–504. Epub 20120618. doi: 10.1038/nrg3245. PubMed DOI PMC

Turner JM. Meiotic sex chromosome inactivation. Development. 2007;134(10):1823–31. Epub 20070228. doi: 10.1242/dev.000018. PubMed DOI

Gartner A, Engebrecht J. DNA repair, recombination, and damage signaling. Genetics. 2022;220(2). doi: 10.1093/genetics/iyab178. PubMed DOI PMC

Meyer BJ. Mechanisms of sex determination and X-chromosome dosage compensation. Genetics. 2022;220(2). doi: 10.1093/genetics/iyab197. PubMed DOI PMC

Checchi PM, Engebrecht J. Heteromorphic sex chromosomes: navigating meiosis without a homologous partner. Mol Reprod Dev. 2011;78(9):623–32. Epub 20110816. doi: 10.1002/mrd.21369. PubMed DOI PMC

Shakes DC, Wu JC, Sadler PL, Laprade K, Moore LL, Noritake A, et al. Spermatogenesis-specific features of the meiotic program in Caenorhabditis elegans. PLoS Genet. 2009;5(8):e1000611. Epub 20090821. doi: 10.1371/journal.pgen.1000611. PubMed DOI PMC

Jaramillo-Lambert A, Ellefson M, Villeneuve AM, Engebrecht J. Differential timing of S phases, X chromosome replication, and meiotic prophase in the C. elegans germ line. Dev Biol. 2007;308(1):206–21. Epub 20070525. doi: 10.1016/j.ydbio.2007.05.019. PubMed DOI

Morgan DE, Crittenden SL, Kimble J. The C. elegans adult male germline: stem cells and sexual dimorphism. Dev Biol. 2010;346(2):204–14. Epub 20100724. doi: 10.1016/j.ydbio.2010.07.022. PubMed DOI PMC

Gartner A, Milstein S, Ahmed S, Hodgkin J, Hengartner MO. A conserved checkpoint pathway mediates DNA damage--induced apoptosis and cell cycle arrest in C. elegans. Mol Cell. 2000;5(3):435–43. doi: 10.1016/s1097-2765(00)80438-4. PubMed DOI

Jaramillo-Lambert A, Harigaya Y, Vitt J, Villeneuve A, Engebrecht J. Meiotic errors activate checkpoints that improve gamete quality without triggering apoptosis in male germ cells. Curr Biol. 2010;20(23):2078–89. Epub 20101021. doi: 10.1016/j.cub.2010.10.008. PubMed DOI PMC

Checchi PM, Lawrence KS, Van MV, Larson BJ, Engebrecht J. Pseudosynapsis and decreased stringency of meiotic repair pathway choice on the hemizygous sex chromosome of Caenorhabditis elegans males. Genetics. 2014;197(2):543–60. doi: 10.1534/genetics.114.164152. PubMed DOI PMC

Jaramillo-Lambert A, Engebrecht J. A single unpaired and transcriptionally silenced X chromosome locally precludes checkpoint signaling in the Caenorhabditis elegans germ line. Genetics. 2010;184(3):613–28. Epub 20091214. doi: 10.1534/genetics.109.110338. PubMed DOI PMC

Li Q, Hariri S, Engebrecht J. Meiotic Double-Strand Break Processing and Crossover Patterning Are Regulated in a Sex-Specific Manner by BRCA1-BARD1 in Caenorhabditis elegans. Genetics. 2020;216(2):359–79. Epub 20200812. doi: 10.1534/genetics.120.303292. PubMed DOI PMC

Colaiacovo MP, MacQueen AJ, Martinez-Perez E, McDonald K, Adamo A, La Volpe A, et al. Synaptonemal complex assembly in C. elegans is dispensable for loading strandexchange proteins but critical for proper completion of recombination. Dev Cell. 2003;5(3):463–74. doi: 10.1016/s1534-5807(03)00232-6. PubMed DOI

Lim JG, Stine RR, Yanowitz JL. Domain-specific regulation of recombination in Caenorhabditis elegans in response to temperature, age and sex. Genetics. 2008;180(2):715–26. Epub 20080909. doi: 10.1534/genetics.108.090142. PubMed DOI PMC

Yokoo R, Zawadzki KA, Nabeshima K, Drake M, Arur S, Villeneuve AM. COSA-1 reveals robust homeostasis and separable licensing and reinforcement steps governing meiotic crossovers. Cell. 2012;149(1):75–87. doi: 10.1016/j.cell.2012.01.052. PubMed DOI PMC

Li Q, Kaur A, Mallory B, Hariri S, Engebrecht J. Inducible degradation of dosage compensation protein DPY-27 facilitates isolation of Caenorhabditis elegans males for molecular and biochemical analyses. G3 (Bethesda). 2022;12(5). doi: 10.1093/g3journal/jkac085. PubMed DOI PMC

Cahoon CK, Uebel CJ, Villeneuve AM, Libuda DE. Epitope tag-specific differences in the detection of COSA-1 marked crossover sites in C. elegans spermatocytes. MicroPubl Biol. 2023;2023. Epub 20230106. doi: 10.17912/micropub.biology.000724. PubMed DOI PMC

Haversat J, Woglar A, Klatt K, Akerib CC, Roberts V, Chen SY, et al. Robust designation of meiotic crossover sites by CDK-2 through phosphorylation of the MutSgamma complex. Proc Natl Acad Sci U S A. 2022;119(21):e2117865119. Epub 20220516. doi: 10.1073/pnas.2117865119. PubMed DOI PMC

Hicks T, Trivedi S, Eppert M, Bowman R, Tian H, Dafalla A, et al. Continuous double-strand break induction and their differential processing sustain chiasma formation during Caenorhabditis elegans meiosis. Cell Rep. 2022;40(13):111403. doi: 10.1016/j.celrep.2022.111403. PubMed DOI

Carlton PM, Farruggio AP, Dernburg AF. A link between meiotic prophase progression and crossover control. PLoS Genet. 2006;2(2):e12. Epub 20060203. doi: 10.1371/journal.pgen.0020012. PubMed DOI PMC

Li Q, Saito TT, Martinez-Garcia M, Deshong AJ, Nadarajan S, Lawrence KS, et al. The tumor suppressor BRCA1-BARD1 complex localizes to the synaptonemal complex and regulates recombination under meiotic dysfunction in Caenorhabditis elegans. PLoS Genet. 2018;14(11):e1007701. Epub 2018/11/02. doi: 10.1371/journal.pgen.1007701. PubMed DOI PMC

Lucchesi JCDTS. The interchromosomal control of recombination. Annual Review of Genetics. 1968;2:53–86

Hodgkin JA, Brenner S. Mutations causing transformation of sexual phenotype in the nematode Caenorhabditis elegans. Genetics. 1977;86(2 Pt. 1):275–87. PubMed PMC

Gumienny TL, Lambie E, Hartwieg E, Horvitz HR, Hengartner MO. Genetic control of programmed cell death in the Caenorhabditis elegans hermaphrodite germline. Development. 1999;126(5):1011–22. doi: 10.1242/dev.126.5.1011. PubMed DOI

Andux S, Ellis RE. Apoptosis maintains oocyte quality in aging Caenorhabditis elegans females. PLoS Genet. 2008;4(12):e1000295. Epub 20081205. doi: 10.1371/journal.pgen.1000295. PubMed DOI PMC

Ellis HM, Horvitz HR. Genetic control of programmed cell death in the nematode C. elegans. Cell. 1986;44(6):817–29. doi: 10.1016/0092-8674(86)90004-8. PubMed DOI

Zhang L, Ward JD, Cheng Z, Dernburg AF. The auxin-inducible degradation (AID) system enables versatile conditional protein depletion in C. elegans. Development. 2015;142(24):4374–84. Epub 20151109. doi: 10.1242/dev.129635. PubMed DOI PMC

Severson AF, Ling L, van Zuylen V, Meyer BJ. The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. Genes Dev. 2009;23(15):1763–78. Epub 20090702. doi: 10.1101/gad.1808809. PubMed DOI PMC

Wang H, Park H, Liu J, Sternberg PW. An Efficient Genome Editing Strategy To Generate Putative Null Mutants in Caenorhabditis elegans Using CRISPR/Cas9. G3 (Bethesda). 2018;8(11):3607–16. Epub 20181106. doi: 10.1534/g3.118.200662. PubMed DOI PMC

Jagut M, Hamminger P, Woglar A, Millonigg S, Paulin L, Mikl M, et al. Separable Roles for a Caenorhabditis elegans RMI1 Homolog in Promoting and Antagonizing Meiotic Crossovers Ensure Faithful Chromosome Inheritance. PLoS Biol. 2016;14(3):e1002412. Epub 20160324. doi: 10.1371/journal.pbio.1002412. PubMed DOI PMC

Brinkmeier J, Coelho S, de Massy B, Bourbon HM. Evolution and Diversity of the TopoVI and TopoVI-like Subunits With Extensive Divergence of the TOPOVIBL subunit. Mol Biol Evol. 2022;39(11). doi: 10.1093/molbev/msac227. PubMed DOI PMC

Claeys Bouuaert C, Tischfield SE, Pu S, Mimitou EP, Arias-Palomo E, Berger JM, et al. Structural and functional characterization of the Spo11 core complex. Nat Struct Mol Biol. 2021;28(1):92–102. Epub 20210104. doi: 10.1038/s41594-020-00534-w. PubMed DOI PMC

Kumar R, Bourbon HM, de Massy B. Functional conservation of Mei4 for meiotic DNA double-strand break formation from yeasts to mice. Genes Dev. 2010;24(12):1266–80. doi: 10.1101/gad.571710. PubMed DOI PMC

Tesse S, Bourbon HM, Debuchy R, Budin K, Dubois E, Liangran Z, et al. Asy2/Mer2: an evolutionarily conserved mediator of meiotic recombination, pairing, and global chromosome compaction. Genes Dev. 2017;31(18):1880–93. Epub 20171011. doi: 10.1101/gad.304543.117. PubMed DOI PMC

Chin GM, Villeneuve AM. C. elegans mre-11 is required for meiotic recombination and DNA repair but is dispensable for the meiotic G(2) DNA damage checkpoint. Genes Dev. 2001;15(5):522–34. doi: 10.1101/gad.864101. PubMed DOI PMC

Hayashi M, Chin GM, Villeneuve AM. C. elegans germ cells switch between distinct modes of double-strand break repair during meiotic prophase progression. PLoS Genet. 2007;3(11):e191. doi: 10.1371/journal.pgen.0030191. PubMed DOI PMC

Reddy KC, Villeneuve AM. C. elegans HIM-17 links chromatin modification and competence for initiation of meiotic recombination. Cell. 2004;118(4):439–52. doi: 10.1016/j.cell.2004.07.026. PubMed DOI

Meneely PM, McGovern OL, Heinis FI, Yanowitz JL. Crossover distribution and frequency are regulated by him-5 in Caenorhabditis elegans. Genetics. 2012;190(4):1251–66. Epub 20120120. doi: 10.1534/genetics.111.137463. PubMed DOI PMC

Hinman AW, Yeh HY, Roelens B, Yamaya K, Woglar A, Bourbon HG, et al. Caenorhabditis elegans DSB-3 reveals conservation and divergence among protein complexes promoting meiotic double-strand breaks. Proc Natl Acad Sci U S A. 2021;118(33). doi: 10.1073/pnas.2109306118. PubMed DOI PMC

Rosu S, Zawadzki KA, Stamper EL, Libuda DE, Reese AL, Dernburg AF, et al. The C. elegans DSB-2 protein reveals a regulatory network that controls competence for meiotic DSB formation and promotes crossover assurance. PLoS Genet. 2013;9(8):e1003674. Epub 20130808. doi: 10.1371/journal.pgen.1003674. PubMed DOI PMC

Stamper EL, Rodenbusch SE, Rosu S, Ahringer J, Villeneuve AM, Dernburg AF. Identification of DSB-1, a protein required for initiation of meiotic recombination in Caenorhabditis elegans, illuminates a crossover assurance checkpoint. PLoS Genet. 2013;9(8):e1003679. Epub 20130808. doi: 10.1371/journal.pgen.1003679. PubMed DOI PMC

Janisiw E, Raices M, Balmir F, Paulin LF, Baudrimont A, von Haeseler A, et al. Poly(ADP-ribose) glycohydrolase coordinates meiotic DNA double-strand break induction and repair independent of its catalytic activity. Nat Commun. 2020;11(1):4869. Epub 20200925. doi: 10.1038/s41467-020-18693-1. PubMed DOI PMC

Machovina TS, Mainpal R, Daryabeigi A, McGovern O, Paouneskou D, Labella S, et al. A Surveillance System Ensures Crossover Formation in C. elegans. Curr Biol. 2016;26(21):2873–84. Epub 20161006. doi: 10.1016/j.cub.2016.09.007. PubMed DOI PMC

Nitiss JL. Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim Biophys Acta. 1998;1400(1–3):63–81. doi: 10.1016/s0167-4781(98)00128-6. PubMed DOI

Chu DS, Liu H, Nix P, Wu TF, Ralston EJ, Yates JR 3rd, et al. Sperm chromatin proteomics identifies evolutionarily conserved fertility factors. Nature. 2006;443(7107):101–5. Epub 20060830. doi: 10.1038/nature05050. PubMed DOI PMC

Jaramillo-Lambert A, Fabritius AS, Hansen TJ, Smith HE, Golden A. The Identification of a Novel Mutant Allele of topoisomerase II in Caenorhabditis elegans Reveals a Unique Role in Chromosome Segregation During Spermatogenesis. Genetics. 2016;204(4):1407–22. Epub 20161005. doi: 10.1534/genetics.116.195099. PubMed DOI PMC

Goodyer W, Kaitna S, Couteau F, Ward JD, Boulton SJ, Zetka M. HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. Dev Cell. 2008;14(2):263–74. doi: 10.1016/j.devcel.2007.11.016. PubMed DOI

Zetka MC, Kawasaki I, Strome S, Muller F. Synapsis and chiasma formation in Caenorhabditis elegans require HIM-3, a meiotic chromosome core component that functions in chromosome segregation. Genes Dev. 1999;13(17):2258–70. doi: 10.1101/gad.13.17.2258. PubMed DOI PMC

Couteau F, Zetka M. HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans. Genes Dev. 2005;19(22):2744–56. doi: 10.1101/gad.1348205. PubMed DOI PMC

Martinez-Perez E, Villeneuve AM. HTP-1-dependent constraints coordinate homolog pairing and synapsis and promote chiasma formation during C. elegans meiosis. Genes Dev. 2005;19(22):2727–43. doi: 10.1101/gad.1338505. PubMed DOI PMC

Pasierbek P, Jantsch M, Melcher M, Schleiffer A, Schweizer D, Loidl J. A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. Genes Dev. 2001;15(11):1349–60. doi: 10.1101/gad.192701. PubMed DOI PMC

Severson AF, Meyer BJ. Divergent kleisin subunits of cohesin specify mechanisms to tether and release meiotic chromosomes. Elife. 2014;3:e03467. Epub 20140829. doi: 10.7554/eLife.03467. PubMed DOI PMC

Blundon JM, Cesar BI, Bae JW, Cavka I, Haversat J, Ries J, et al. Skp1 proteins are structural components of the synaptonemal complex in C. elegans. Sci Adv. 2024;10(7):eadl4876. Epub 20240214. doi: 10.1126/sciadv.adl4876. PubMed DOI PMC

Hurlock ME, Cavka I, Kursel LE, Haversat J, Wooten M, Nizami Z, et al. Identification of novel synaptonemal complex components in C. elegans. J Cell Biol. 2020;219(5). doi: 10.1083/jcb.201910043. PubMed DOI PMC

MacQueen AJ, Colaiacovo MP, McDonald K, Villeneuve AM. Synapsis-dependent and independent mechanisms stabilize homolog pairing during meiotic prophase in C. elegans. Genes Dev. 2002;16(18):2428–42. doi: 10.1101/gad.1011602. PubMed DOI PMC

Smolikov S, Eizinger A, Schild-Prufert K, Hurlburt A, McDonald K, Engebrecht J, et al. SYP-3 restricts synaptonemal complex assembly to bridge paired chromosome axes during meiosis in Caenorhabditis elegans. Genetics. 2007;176(4):2015–25. Epub 20070611. doi: 10.1534/genetics.107.072413. PubMed DOI PMC

Smolikov S, Schild-Prufert K, Colaiacovo MP. A yeast two-hybrid screen for SYP-3 interactors identifies SYP-4, a component required for synaptonemal complex assembly and chiasma formation in Caenorhabditis elegans meiosis. PLoS Genet. 2009;5(10):e1000669. Epub 20091002. doi: 10.1371/journal.pgen.1000669. PubMed DOI PMC

Zhang Z, Xie S, Wang R, Guo S, Zhao Q, Nie H, et al. Multivalent weak interactions between assembly units drive synaptonemal complex formation. J Cell Biol. 2020;219(5). doi: 10.1083/jcb.201910086. PubMed DOI PMC

Cahoon CK, Helm JM, Libuda DE. Synaptonemal Complex Central Region Proteins Promote Localization of Pro-crossover Factors to Recombination Events During Caenorhabditis elegans Meiosis. Genetics. 2019;213(2):395–409. Epub 20190820. doi: 10.1534/genetics.119.302625. PubMed DOI PMC

Gordon SG, Kursel LE, Xu K, Rog O. Synaptonemal Complex dimerization regulates chromosome alignment and crossover patterning in meiosis. PLoS Genet. 2021;17(3):e1009205. Epub 20210317. doi: 10.1371/journal.pgen.1009205. PubMed DOI PMC

Lascarez-Lagunas LI, Nadarajan S, Martinez-Garcia M, Quinn JN, Todisco E, Thakkar T, et al. ATM/ATR kinases link the synaptonemal complex and DNA double-strand break repair pathway choice. Curr Biol. 2022;32(21):4719–26 e4. Epub 20220921. doi: 10.1016/j.cub.2022.08.081. PubMed DOI PMC

Woglar A, Villeneuve AM. Dynamic Architecture of DNA Repair Complexes and the Synaptonemal Complex at Sites of Meiotic Recombination. Cell. 2018;173(7):1678–91 e16. Epub 20180510. doi: 10.1016/j.cell.2018.03.066. PubMed DOI PMC

Lukaszewicz A, Lange J, Keeney S, Jasin M. Control of meiotic double-strand-break formation by ATM: local and global views. Cell Cycle. 2018;17(10):1155–72. Epub 20180715. doi: 10.1080/15384101.2018.1464847. PubMed DOI PMC

Barber LJ, Youds JL, Ward JD, McIlwraith MJ, O’Neil NJ, Petalcorin MI, et al. RTEL1 maintains genomic stability by suppressing homologous recombination. Cell. 2008;135(2):261–71. doi: 10.1016/j.cell.2008.08.016. PubMed DOI PMC

Mets DG, Meyer BJ. Condensins regulate meiotic DNA break distribution, thus crossover frequency, by controlling chromosome structure. Cell. 2009;139(1):73–86. Epub 20090924. doi: 10.1016/j.cell.2009.07.035. PubMed DOI PMC

Patel B, Grobler M, Herrera A, Logari E, Ortiz V, Bhalla N. The conserved ATPase PCH-2 controls the number and distribution of crossovers by antagonizing their formation in Caenorhabditis elegans. Elife. 2025;13. Epub 20250218. doi: 10.7554/eLife.102409. PubMed DOI PMC

Reichman R, Shi Z, Malone R, Smolikove S. Mitotic and Meiotic Functions for the SUMOylation Pathway in the Caenorhabditis elegans Germline. Genetics. 2018;208(4):1421–41. Epub 20180222. doi: 10.1534/genetics.118.300787. PubMed DOI PMC

Tsai CJ, Mets DG, Albrecht MR, Nix P, Chan A, Meyer BJ. Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. Genes Dev. 2008;22(2):194–211. doi: 10.1101/gad.1618508. PubMed DOI PMC

Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, NJ ON, et al. RTEL-1 enforces meiotic crossover interference and homeostasis. Science. 2010;327(5970):1254–8. doi: 10.1126/science.1183112. PubMed DOI PMC

Gong T, McNally FJ. Caenorhabditis elegans spermatocytes can segregate achiasmate homologous chromosomes apart at higher than random frequency during meiosis I. Genetics. 2023;223(4). doi: 10.1093/genetics/iyad021. PubMed DOI PMC

Fabig G, Kiewisz R, Lindow N, Powers JA, Cota V, Quintanilla LJ, et al. Male meiotic spindle features that efficiently segregate paired and lagging chromosomes. Elife. 2020;9. Epub 20200310. doi: 10.7554/eLife.50988. PubMed DOI PMC

Mullen TJ, Davis-Roca AC, Wignall SM. Spindle assembly and chromosome dynamics during oocyte meiosis. Curr Opin Cell Biol. 2019;60:53–9. Epub 20190510. doi: 10.1016/j.ceb.2019.03.014. PubMed DOI PMC

Kurhanewicz NA, Dinwiddie D, Bush ZD, Libuda DE. Elevated Temperatures Cause Transposon-Associated DNA Damage in C. elegans Spermatocytes. Curr Biol. 2020;30(24):5007–17 e4. Epub 20201015. doi: 10.1016/j.cub.2020.09.050. PubMed DOI PMC

Oberlitner J, Tinman M, Das A, Koury E, Silva N, Smolikove S. Analysis of rad-51 separation of function allele suggests divergence of the SDSA and dHJ pathways prior to RAD-51 filament disassembly. Genetics. 2025. Epub 20250407. doi: 10.1093/genetics/iyaf063. PubMed DOI PMC

Paix A, Folkmann A, Rasoloson D, Seydoux G. High Efficiency, Homology-Directed Genome Editing in Caenorhabditis elegans Using CRISPR-Cas9 Ribonucleoprotein Complexes. Genetics. 2015;201(1):47–54. Epub 20150717. doi: 10.1534/genetics.115.179382. PubMed DOI PMC

Ellis R, Schedl T. Sex determination in the germ line. WormBook. 2007:1–13. Epub 20070305. doi: 10.1895/wormbook.1.82.2. PubMed DOI PMC