MHC diversity confers transgenerational fitness advantage in wild dolphins

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Abstract

Abstract Darwin ascribed fitness to individuals with a “better chance of surviving and propagating their kind”1. Subsequently, the search for the genetic basis of fitness focused on traits of the generation that had been genotyped. However, there is only scant, indirect evidence for genetic variation conferring transgenerational fitness effects to subsequent generations2-5. Specifically, there is no direct evidence for a link between parental genetic variation and offspring fitness in long-lived, natural populations. Here we show transgenerational fitness effects mediated by adaptive genetic variation of the major histocompatibility complex (MHC) in a natural population of bottlenose dolphins. Our study, spanning nearly four decades of research (1984­2022), revealed that offspring of MHC-heterozygous mothers were twice as likely to survive. The mother’s age and MHC-heterozygosity were strong predictors of offspring viability. In contrast, we found no association between neutral genetic diversity and fitness. Interestingly, MHC-heterozygous females were less sociable, perhaps an indirect effect of them being more successful mothers that prioritize offspring investment over social bonds—in contrast to other social mammals that rely on female relationships to mediate fitness6. To our knowledge, this is the first study that offers empirical evidence for MHC diversity conferring a fitness advantage across generations. This is in line with theorized, but rarely tested expectations for MHC-dependent mate choice4. Our study also underscores the crucial role of long-term studies7 in revealing the genetic basis of fitness in long-lived, natural populations.
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MHC diversity confers transgenerational fitness advantage in wild dolphins | 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 MHC diversity confers transgenerational fitness advantage in wild dolphins Oliver Manlik, Janet Mann, Michael Krützen, Vivienne Foroughirad, and 7 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-7279666/v1 This work is licensed under a CC BY 4.0 License Status: Under Review Version 1 posted You are reading this latest preprint version Abstract Darwin ascribed fitness to individuals with a “better chance of surviving and propagating their kind” 1 . Subsequently, the search for the genetic basis of fitness focused on traits of the generation that had been genotyped. However, there is only scant, indirect evidence for genetic variation conferring transgenerational fitness effects to subsequent generations 2-5 . Specifically, there is no direct evidence for a link between parental genetic variation and offspring fitness in long-lived, natural populations. Here we show transgenerational fitness effects mediated by adaptive genetic variation of the major histocompatibility complex (MHC) in a natural population of bottlenose dolphins. Our study, spanning nearly four decades of research (1984­2022), revealed that offspring of MHC-heterozygous mothers were twice as likely to survive. The mother’s age and MHC-heterozygosity were strong predictors of offspring viability. In contrast, we found no association between neutral genetic diversity and fitness. Interestingly, MHC-heterozygous females were less sociable, perhaps an indirect effect of them being more successful mothers that prioritize offspring investment over social bonds—in contrast to other social mammals that rely on female relationships to mediate fitness 6 . To our knowledge, this is the first study that offers empirical evidence for MHC diversity conferring a fitness advantage across generations. This is in line with theorized, but rarely tested expectations for MHC-dependent mate choice 4 . Our study also underscores the crucial role of long-term studies 7 in revealing the genetic basis of fitness in long-lived, natural populations. Biological sciences/Evolution Biological sciences/Evolution/Evolutionary genetics Biological sciences/Ecology/Ecological genetics Full Text Additional Declarations There is NO Competing Interest. Supplementary Files SupplementManliketal2025MHCFitnessFINAL.pdf Supplementary Data File for: MHC genetic diversity confers transgenerational fitness advantage in dolphins Cite Share Download PDF Status: Under Review 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. 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