The evolution of sex reconsidered: Resource limits offset the twofold cost of males

The evolution of sex reconsidered: Resource limits offset the twofold cost of males | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Biological Sciences - Article The evolution of sex reconsidered: Resource limits offset the twofold cost of males Yukio Yasui, Eisuke Hasegawa This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4360051/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 17 Mar, 2026 Read the published version in Journal of Ethology → Version 1 posted You are reading this latest preprint version Abstract In anisogamy (sexual reproduction by egg and sperm), the population growth rate is half that of thelytoky (all-female parthenogenesis) because half of the offspring are males, which do not lay eggs 1,2 . The present dominance of anisogamy in multicellular organisms despite this “twofold cost of male production” is the greatest enigma in evolutionary biology 3-8 . Various proposed benefits (e.g., Red Queen) of sex are insufficient to compete with thelytoky, which increases 2 10 = 1024-fold in 10 generations over anisogamy. Why is anisogamy protected from thelytoky invasion? However, the 1024-fold increase requires the 1024-fold resources and resources are finite in the real world. Here, using a very simple mathematical model and simulations, we show that the twofold cost disappears under resource limitations. Thelytoky can exhibit a twofold increase only at low densities with abundant resources, but anisogamy can coexist with thelytoky because competitive exclusion does not occur in such an unsaturated population. Once the population reaches the carrying capacity, thelytoky and anisogamy have the same realized fitness. If males offer slight advantages (e.g., lower resource requirements or greater resource competitiveness than thelytokous females), anisogamy has greater fitness than thelytoky and will displace thelytoky. Therefore, twofold benefits to compensate for the twofold cost are unnecessary. Biological sciences/Evolution/Evolutionary theory Biological sciences/Evolution/Sexual selection Full Text Additional Declarations There is NO Competing Interest. Supplementary Files 2022EvolutionaryBiologyForResearchersSpringerNature.jpg Award information Cite Share Download PDF Status: Published Journal Publication published 17 Mar, 2026 Read the published version in Journal of Ethology → Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4360051","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Biological Sciences - Article","associatedPublications":[],"authors":[{"id":300742330,"identity":"c984cf75-026d-4e5d-bae4-5eeb2daf7b9a","order_by":0,"name":"Yukio Yasui","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABG0lEQVRIiWNgGAWjYLCCBCCWYGZgfNiALMrYgE0tqhZmQ+K1gIAEAwObJCFFYGBw/PgziQcMhxNntjMfq5xRUytvcPwAmwRDjR0D82zsJhicyTGTSABqmc3MlnZzw7HjhhvOJAC1HEtmYJxzALuWAzlsYC3zmHnMbj5gO8a47UD+NwkGtgMMjDMSsGs5//wZXEvhg3/H7LedfwC05R8eLTcSYA7jMWPc2FaTuO0G0GGMbbi1SN54Y2yRYJBuPLOZLVlyZt+B5P03HjBbJPYl8+DyC9/59Ic3f1RYy844f/jgx55vdbYz+xMYb3z4ZidniCPEFMAmGTTD+IchFNBJPIYzsOpgkIeYVAfj1yFJSWDXMgpGwSgYBSMOAAA/kmOvZkiY/AAAAABJRU5ErkJggg==","orcid":"https://orcid.org/0000-0003-4875-9836","institution":"Kagawa University","correspondingAuthor":true,"prefix":"","firstName":"Yukio","middleName":"","lastName":"Yasui","suffix":""},{"id":300742334,"identity":"2a0a548e-2908-4983-80d4-d01ad41947b8","order_by":1,"name":"Eisuke Hasegawa","email":"","orcid":"","institution":"Hokkaido University","correspondingAuthor":false,"prefix":"","firstName":"Eisuke","middleName":"","lastName":"Hasegawa","suffix":""}],"badges":[],"createdAt":"2024-05-02 15:40:18","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4360051/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4360051/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1007/s10164-026-00885-9","type":"published","date":"2026-03-18T00:00:00+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":105953966,"identity":"23d46ebe-d879-43c1-bc07-14ed45b6452e","added_by":"auto","created_at":"2026-04-01 19:30:29","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":648213,"visible":true,"origin":"","legend":"Article File","description":"","filename":"Evolutionofsex20240501NatureAJE.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4360051/v1_covered_57976eff-8b62-427e-aaa3-a9adc176daad.pdf"},{"id":56215421,"identity":"6003d1c5-ef03-4267-b8f6-dbfe35d0c903","added_by":"auto","created_at":"2024-05-10 02:48:27","extension":"jpg","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":1464836,"visible":true,"origin":"","legend":"Award information","description":"","filename":"2022EvolutionaryBiologyForResearchersSpringerNature.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4360051/v1/43491d83ff93fe416ebf3d57.jpg"}],"financialInterests":"There is \u003cb\u003eNO\u003c/b\u003e Competing Interest.","formattedTitle":"The evolution of sex reconsidered: Resource limits offset the twofold cost of males","fulltext":[],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":true,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":true,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":true,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-4360051/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4360051/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eIn anisogamy (sexual reproduction by egg and sperm), the population growth rate is half that of thelytoky (all-female parthenogenesis) because half of the offspring are males, which do not lay eggs\u003csup\u003e1,2\u003c/sup\u003e. The present dominance of anisogamy in multicellular organisms despite this “twofold cost of male production” is the greatest enigma in evolutionary biology\u003csup\u003e3-8\u003c/sup\u003e. Various proposed benefits (e.g., Red Queen) of sex are insufficient to compete with thelytoky, which increases 2\u003csup\u003e10\u003c/sup\u003e = 1024-fold in 10 generations over anisogamy. Why is anisogamy protected from thelytoky invasion? However, the 1024-fold increase requires the 1024-fold resources and resources are finite in the real world. Here, using a very simple mathematical model and simulations, we show that the twofold cost disappears under resource limitations. Thelytoky can exhibit a twofold increase only at low densities with abundant resources, but anisogamy can coexist with thelytoky because competitive exclusion does not occur in such an unsaturated population. Once the population reaches the carrying capacity, thelytoky and anisogamy have the same realized fitness. If males offer slight advantages (e.g., lower resource requirements or greater resource competitiveness than thelytokous females), anisogamy has greater fitness than thelytoky and will displace thelytoky. Therefore, twofold benefits to compensate for the twofold cost are unnecessary.\u003c/p\u003e","manuscriptTitle":"The evolution of sex reconsidered: Resource limits offset the twofold cost of males","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-05-10 02:48:20","doi":"10.21203/rs.3.rs-4360051/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"77541e4d-b434-42c4-b672-7a23777594dc","owner":[],"postedDate":"May 10th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[{"id":31733856,"name":"Biological sciences/Evolution/Evolutionary theory"},{"id":31733858,"name":"Biological sciences/Evolution/Sexual selection"}],"tags":[],"updatedAt":"2026-04-01T19:30:24+00:00","versionOfRecord":{"articleIdentity":"rs-4360051","link":"https://doi.org/10.1007/s10164-026-00885-9","journal":{"identity":"journal-of-ethology","isVorOnly":true,"title":"Journal of Ethology"},"publishedOn":"2026-03-18 00:00:00","publishedOnDateReadable":"March 18th, 2026"},"versionCreatedAt":"2024-05-10 02:48:20","video":"","vorDoi":"10.1007/s10164-026-00885-9","vorDoiUrl":"https://doi.org/10.1007/s10164-026-00885-9","workflowStages":[]},"version":"v1","identity":"rs-4360051","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4360051","identity":"rs-4360051","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}