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The genetic model nematode <jats:italic>Caenorhabditis elegans<\/jats:italic> has well-defined mechanisms of stress response, aging, and sexual differentiation. <jats:italic>C<\/jats:italic>. <jats:italic>elegans<\/jats:italic> has males, but the vast majority of research only uses hermaphrodites. We found that males of the standard N2 laboratory strain were more resistant to hyperosmolarity, heat, and a natural pro-oxidant than hermaphrodites when in mixed-sex groups. Resistance to heat and pro-oxidant were also male-biased in three genetically and geographically diverse <jats:italic>C<\/jats:italic>. <jats:italic>elegans<\/jats:italic> strains consistent with a species-wide dimorphism that is not specific to domestication. N2 males were also more resistant to heat and pro-oxidant when keep individually indicating that differences in resistance do not require interactions between worms. We found that males induce canonical stress response genes by similar degrees and in similar tissues as hermaphrodites suggesting the importance of other mechanisms. We find that resistance to heat and pro-oxidant are influenced by the sex differentiation transcription factor TRA-1 suggesting that downstream organ differentiation pathways establish differences in stress resistance. Environmental stress influences survival in natural environments, degenerative disease, and aging. Understanding mechanisms of stress response dimorphism can therefore provide insights into sex-specific population dynamics, disease, and longevity.<\/jats:p>","DOI":"10.1371\/journal.pone.0272452","type":"journal-article","created":{"date-parts":[[2022,8,11]],"date-time":"2022-08-11T17:42:53Z","timestamp":1660239773000},"page":"e0272452","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":12,"title":["Sexual dimorphism in Caenorhabditis elegans stress resistance"],"prefix":"10.1371","volume":"17","author":[{"given":"Juan H.","family":"Piloto","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Rodriguez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1405-7492","authenticated-orcid":true,"given":"Keith 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Zucker","year":"2010","journal-title":"Nature"},{"key":"pone.0272452.ref004","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1124\/pr.115.011163","article-title":"Sex differences in animal models: Focus on addiction","volume":"68","author":"JB Becker","year":"2016","journal-title":"Pharmacological Reviews"},{"key":"pone.0272452.ref005","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1038\/s41582-018-0032-9","article-title":"Sex differences in Alzheimer disease\u2014The gateway to precision medicine","volume":"14","author":"MT Ferretti","year":"2018","journal-title":"Nature Reviews Neurology"},{"key":"pone.0272452.ref006","doi-asserted-by":"crossref","first-page":"18231","DOI":"10.1073\/pnas.0505172102","article-title":"Sex ratio bias, male aggression, and population collapse in lizards","volume":"102","author":"J-F Le Galliard","year":"2005","journal-title":"Proceedings of the National Academy of Sciences of the United States of 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Clutton-Brock","year":"2007","journal-title":"Proceedings Biological Sciences"},{"key":"pone.0272452.ref014","doi-asserted-by":"crossref","first-page":"8546","DOI":"10.1073\/pnas.1911999117","article-title":"Sex differences in adult lifespan and aging rates of mortality across wild mammals","volume":"117","author":"J-F Lema\u00eetre","year":"2020","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"pone.0272452.ref015","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1016\/j.cell.2005.02.002","article-title":"The plasticity of aging: insights from long-lived mutants","volume":"120","author":"C Kenyon","year":"2005","journal-title":"Cell"},{"key":"pone.0272452.ref016","doi-asserted-by":"crossref","first-page":"2707","DOI":"10.1016\/j.bbadis.2017.09.016","article-title":"Drosophila as a model for ageing","volume":"1864","author":"MDW Piper","year":"2018","journal-title":"Biochimica Et Biophysica Acta Molecular Basis of 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Gems","year":"1996","journal-title":"Nature"},{"key":"pone.0272452.ref020","doi-asserted-by":"crossref","first-page":"1597","DOI":"10.1093\/genetics\/154.4.1597","article-title":"Genetic, behavioral and environmental determinants of male longevity in Caenorhabditis elegans","volume":"154","author":"D Gems","year":"2000","journal-title":"Genetics"},{"key":"pone.0272452.ref021","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1093\/gerona\/59.1.B3","article-title":"Sex differences in the effect of dietary restriction on life span and mortality rates in female and male Drosophila melanogaster","volume":"59","author":"T Magwere","year":"2004","journal-title":"The Journals of Gerontology Series A, Biological Sciences and Medical Sciences"},{"key":"pone.0272452.ref022","doi-asserted-by":"crossref","first-page":"e71358","DOI":"10.1371\/journal.pone.0071358","article-title":"Climate influences fledgling sex ratio and sex-specific dispersal in a seabird","volume":"8","author":"A Barros","year":"2013","journal-title":"PloS One"},{"key":"pone.0272452.ref023","first-page":"1537","article-title":"Stochastic predation events and population persistence in bighorn sheep","volume":"273","author":"M Festa-Bianchet","year":"2006","journal-title":"Proceedings Biological Sciences"},{"key":"pone.0272452.ref024","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1016\/j.cmet.2018.05.021","article-title":"Short-term fasting reveals amino acid metabolism as a major sex-discriminating factor in the liver","volume":"28","author":"S Della Torre","year":"2018","journal-title":"Cell Metabolism"},{"key":"pone.0272452.ref025","doi-asserted-by":"crossref","first-page":"3646","DOI":"10.1016\/j.celrep.2017.11.108","article-title":"The sexual dimorphism of dietary restriction responsiveness in Caenorhabditis elegans","volume":"21","author":"S Honjoh","year":"2017","journal-title":"Cell Reports"},{"key":"pone.0272452.ref026","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1016\/j.cmet.2016.05.027","article-title":"Effects of sex, strain, and energy intake on hallmarks of aging in mice","volume":"23","author":"SJ Mitchell","year":"2016","journal-title":"Cell Metabolism"},{"key":"pone.0272452.ref027","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.freeradbiomed.2015.06.008","article-title":"SKN-1\/Nrf, stress responses, and aging in Caenorhabditis elegans","volume":"88","author":"TK Blackwell","year":"2015","journal-title":"Free Radical Biology & Medicine"},{"key":"pone.0272452.ref028","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1038\/88850","article-title":"Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin\/IGF-1 and germline signaling","volume":"28","author":"K Lin","year":"2001","journal-title":"Nature 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elegans","volume":"305","author":"KP Choe","year":"2013","journal-title":"American Journal of Physiology Regulatory, Integrative and Comparative Physiology"},{"key":"pone.0272452.ref035","doi-asserted-by":"crossref","first-page":"1014","DOI":"10.1016\/j.exger.2013.02.018","article-title":"Dietary restriction in C. elegans: Recent advances","volume":"48","author":"JR Cypser","year":"2013","journal-title":"Experimental Gerontology"},{"key":"pone.0272452.ref036","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1016\/j.mad.2018.08.001","article-title":"Emerging topics in C. elegans aging research: Transcriptional regulation, stress response and epigenetics","volume":"177","author":"MS Denzel","year":"2019","journal-title":"Mechanisms of Ageing and Development"},{"key":"pone.0272452.ref037","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1895\/wormbook.1.83.2","article-title":"Signaling in the innate immune response.","volume":"2018","author":"DH Kim","year":"2018","journal-title":"WormBook: The Online Review of C Elegans Biology"},{"key":"pone.0272452.ref038","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/j.tig.2013.01.010","article-title":"Worms under stress: C. elegans stress response and its relevance to complex human disease and aging.","volume":"29","author":"M Rodriguez","year":"2013","journal-title":"Trends in genetics: TIG"},{"key":"pone.0272452.ref039","doi-asserted-by":"crossref","first-page":"983","DOI":"10.1093\/genetics\/160.3.983","article-title":"Why are there males in the hermaphroditic species Caenorhabditis elegans?","volume":"160","author":"JR Chasnov","year":"2002","journal-title":"Genetics"},{"key":"pone.0272452.ref040","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1534\/genetics.119.300244","article-title":"Males, outcrossing, and sexual selection in Caenorhabditis elegans","volume":"213","author":"AD Cutter","year":"2019","journal-title":"Genetics"},{"key":"pone.0272452.ref041","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1093\/genetics\/77.1.71","article-title":"The genetics of Caenorhabditis elegans","volume":"77","author":"S Brenner","year":"1974","journal-title":"Genetics"},{"key":"pone.0272452.ref042","doi-asserted-by":"crossref","first-page":"C1488","DOI":"10.1152\/ajpcell.00450.2008","article-title":"Genome-wide RNAi screen and in vivo protein aggregation reporters identify degradation of damaged proteins as an essential hypertonic stress response","volume":"295","author":"KP Choe","year":"2008","journal-title":"American Journal of Physiology Cell Physiology"},{"key":"pone.0272452.ref043","doi-asserted-by":"crossref","first-page":"C915","DOI":"10.1152\/ajpcell.00126.2007","article-title":"Evolutionarily conserved WNK and Ste20 kinases are essential for acute volume recovery and survival after hypertonic shrinkage in Caenorhabditis elegans","volume":"293","author":"KP Choe","year":"2007","journal-title":"American Journal of Physiology Cell Physiology"},{"key":"pone.0272452.ref044","doi-asserted-by":"crossref","first-page":"3517","DOI":"10.1002\/jps.22573","article-title":"Evaluation of pharmacokinetic, biodistribution, pharmacodynamic, and toxicity profile of free juglone and its sterically stabilized liposomes","volume":"100","author":"BK Aithal","year":"2011","journal-title":"Journal of Pharmaceutical Sciences"},{"key":"pone.0272452.ref045","doi-asserted-by":"crossref","first-page":"91","DOI":"10.3390\/antiox8040091","article-title":"Juglone in oxidative stress and cell signaling","volume":"8","author":"T Ahmad","year":"2019","journal-title":"Antioxidants"},{"key":"pone.0272452.ref046","doi-asserted-by":"crossref","first-page":"2704","DOI":"10.1128\/MCB.01811-08","article-title":"The WD40 repeat protein WDR-23 functions with the CUL4\/DDB1 ubiquitin ligase to regulate nuclear abundance and activity of SKN-1 in Caenorhabditis elegans","volume":"29","author":"KP Choe","year":"2009","journal-title":"Molecular and Cellular Biology"},{"key":"pone.0272452.ref047","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1016\/j.ymeth.2014.04.015","article-title":"Methodological considerations for heat shock of the nematode Caenorhabditis elegans","volume":"68","author":"SC Zevian","year":"2014","journal-title":"Methods (San Diego, Calif)"},{"key":"pone.0272452.ref048","article-title":"Increased expression of pgph-1, T23F2.4, and cyp-14A5 in C. elegans dpy-7 mutants and by high salt. microPublication","author":"G Scolaro","year":"2019","journal-title":"Biology"},{"key":"pone.0272452.ref049","doi-asserted-by":"crossref","first-page":"e23525","DOI":"10.1371\/journal.pone.0023525","article-title":"OASIS: online application for the survival analysis of lifespan assays performed in aging research","volume":"6","author":"JS Yang","year":"2011","journal-title":"PLoS One"},{"key":"pone.0272452.ref050","doi-asserted-by":"crossref","first-page":"C566","DOI":"10.1152\/ajpcell.00030.2011","article-title":"Hypertonic stress induces rapid and widespread protein damage in C. elegans","volume":"301","author":"K Burkewitz","year":"2011","journal-title":"American Journal of Physiology Cell Physiology"},{"key":"pone.0272452.ref051","doi-asserted-by":"crossref","first-page":"e34153","DOI":"10.1371\/journal.pone.0034153","article-title":"Characterization of the proteostasis roles of glycerol accumulation, protein degradation and protein synthesis during osmotic stress in C. elegans","volume":"7","author":"K Burkewitz","year":"2012","journal-title":"PloS One"},{"key":"pone.0272452.ref052","doi-asserted-by":"crossref","first-page":"C785","DOI":"10.1152\/ajpcell.00381.2003","article-title":"Adaptation of the nematode Caenorhabditis elegans to extreme osmotic stress","volume":"286","author":"ST Lamitina","year":"2004","journal-title":"American Journal of Physiology Cell Physiology"},{"key":"pone.0272452.ref053","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1038\/s41438-018-0067-5","article-title":"The origin and biosynthesis of the naphthalenoid moiety of juglone in black walnut","volume":"5","author":"RM McCoy","year":"2018","journal-title":"Horticulture Research"},{"key":"pone.0272452.ref054","doi-asserted-by":"crossref","first-page":"1076","DOI":"10.1080\/15548627.2017.1299313","article-title":"Hormetic heat shock and HSF-1 overexpression improve C. elegans survival and proteostasis by inducing autophagy.","volume":"13","author":"C Kumsta","year":"2017","journal-title":"Autophagy"},{"key":"pone.0272452.ref055","first-page":"257","article-title":"On the geographical distribution of the Juglandaceae","volume":"20","author":"L An-Ming","year":"1982","journal-title":"J Syst Evol"},{"key":"pone.0272452.ref056","doi-asserted-by":"crossref","first-page":"975","DOI":"10.1534\/genetics.115.175950","article-title":"Remarkably divergent regions punctuate the genome assembly of the Caenorhabditis elegans Hawaiian strain CB4856","volume":"200","author":"OA Thompson","year":"2015","journal-title":"Genetics"},{"key":"pone.0272452.ref057","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1093\/genetics\/146.1.149","article-title":"Natural variation and copulatory plug formation in Caenorhabditis elegans","volume":"146","author":"J Hodgkin","year":"1997","journal-title":"Genetics"},{"key":"pone.0272452.ref058","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1046\/j.1474-9728.2003.00047.x","article-title":"Evolution of male longevity bias in nematodes","volume":"2","author":"D McCulloch","year":"2003","journal-title":"Aging Cell"},{"key":"pone.0272452.ref059","doi-asserted-by":"crossref","first-page":"12173","DOI":"10.1073\/pnas.0602987103","article-title":"Genome-wide RNAi screening identifies protein damage as a regulator of osmoprotective gene expression","volume":"103","author":"T Lamitina","year":"2006","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"pone.0272452.ref060","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.bbrc.2011.06.001","article-title":"H+\/myo-inositol transporter genes, hmit-1.1 and hmit-1.2, have roles in the osmoprotective response in Caenorhabditis elegans","volume":"410","author":"E Kage-Nakadai","year":"2011","journal-title":"Biochem Biophys Res Commun"},{"key":"pone.0272452.ref061","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.mad.2015.06.001","article-title":"Characterization of skn-1\/wdr-23 phenotypes in Caenorhabditis elegans; pleiotrophy, aging, glutathione, and interactions with other longevity pathways","volume":"149","author":"L Tang","year":"2015","journal-title":"Mechanisms of Ageing and Development"},{"key":"pone.0272452.ref062","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1016\/j.mad.2009.02.004","article-title":"Increased age reduces DAF-16 and SKN-1 signaling and the hormetic response of Caenorhabditis elegans to the xenobiotic juglone","volume":"130","author":"AJ Przybysz","year":"2009","journal-title":"Mechanisms of Ageing and Development"},{"key":"pone.0272452.ref063","doi-asserted-by":"crossref","first-page":"1142","DOI":"10.1126\/science.1083701","article-title":"Regulation of aging and age-related disease by DAF-16 and heat-shock factor","volume":"300","author":"A-L Hsu","year":"2003","journal-title":"Science (New York, NY)"},{"key":"pone.0272452.ref064","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1089\/dna.1.1989.8.481","article-title":"Differential regulation of closely related members of the hsp-16 gene family in Caenorhabditis elegans","volume":"8","author":"D Jones","year":"1989","journal-title":"DNA (Mary Ann Liebert, Inc)"},{"key":"pone.0272452.ref065","doi-asserted-by":"crossref","first-page":"e1000105","DOI":"10.1371\/journal.ppat.1000105","article-title":"Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides.","volume":"4","author":"N Pujol","year":"2008","journal-title":"PLoS pathogens"},{"key":"pone.0272452.ref066","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1186\/s12915-019-0675-z","article-title":"RNA processing errors triggered by cadmium and integrator complex disruption are signals for environmental stress","volume":"17","author":"C-W Wu","year":"2019","journal-title":"BMC biology"},{"key":"pone.0272452.ref067","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1016\/S0092-8674(01)00612-2","article-title":"Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development","volume":"107","author":"X Shen","year":"2001","journal-title":"Cell"},{"key":"pone.0272452.ref068","doi-asserted-by":"crossref","first-page":"e1005520","DOI":"10.1371\/journal.pgen.1005520","article-title":"FLCN and AMPK confer resistance to hyperosmotic stress via remodeling of glycogen stores","volume":"11","author":"E Possik","year":"2015","journal-title":"PLoS genetics"},{"key":"pone.0272452.ref069","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.ydbio.2020.12.002","article-title":"Stressful development: integrating endoderm development, stress, and longevity","volume":"471","author":"CK Ewe","year":"2021","journal-title":"Developmental Biology"},{"key":"pone.0272452.ref070","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/bs.ctdb.2020.12.007","article-title":"Innate immunity in C. elegans","volume":"144","author":"CN Martineau","year":"2021","journal-title":"Current Topics in Developmental 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nematodes","volume":"197","author":"SE Albritton","year":"2014","journal-title":"Genetics"},{"key":"pone.0272452.ref085","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1042\/BST0340007","article-title":"Coping with stress: eIF2 kinases and translational control","volume":"34","author":"RC Wek","year":"2006","journal-title":"Biochem Soc Trans"},{"key":"pone.0272452.ref086","doi-asserted-by":"crossref","first-page":"C1269","DOI":"10.1152\/ajpcell.00294.2012","article-title":"GCN-2 dependent inhibition of protein synthesis activates osmosensitive gene transcription via WNK and STE20 kinase signaling","volume":"303","author":"EC-H Lee","year":"2012","journal-title":"American Journal of Physiology Cell Physiology"},{"key":"pone.0272452.ref087","doi-asserted-by":"crossref","first-page":"613S","DOI":"10.1080\/07315724.2007.10719667","article-title":"Mechanisms and significance of cell volume regulation","volume":"26","author":"F Lang","year":"2007","journal-title":"Journal of the 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Chen","year":"2000","journal-title":"Development"},{"key":"pone.0272452.ref094","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1006\/dbio.2000.9993","article-title":"Regulation of cell fate in Caenorhabditis elegans by a novel cytoplasmic polyadenylation element binding protein","volume":"229","author":"SW Jin","year":"2001","journal-title":"Dev Biol"},{"key":"pone.0272452.ref095","doi-asserted-by":"crossref","first-page":"4469","DOI":"10.1242\/dev.127.20.4469","article-title":"mab-3 is a direct tra-1 target gene regulating diverse aspects of C. elegans male sexual development and behavior","volume":"127","author":"W Yi","year":"2000","journal-title":"Development"},{"key":"pone.0272452.ref096","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1242\/dev.126.5.873","article-title":"Similarity of DNA binding and transcriptional regulation by Caenorhabditis elegans MAB-3 and Drosophila melanogaster DSX suggests conservation of sex determining 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