Ecological trait differences are associated with gene expression in the primary visual cortex of primates

Ecological trait differences are associated with gene expression in the primary visual cortex of primates | 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 Research article Ecological trait differences are associated with gene expression in the primary visual cortex of primates Trisha Marie Zintel, John J. Ely, Mary Ann Raghanti, William D. Hopkins, and 5 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.2.20778/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Background : Primate species differ drastically from most other mammals in how they visually perceive their environments, which is important for foraging, predator avoidance, and detection of social cues. Although it is well established that primates display diversity in color vision and various ecological specializations, it is not understood how visual system characteristics and ecological adaptations may be associated with gene expression levels within the primary visual cortex (V1). Results : We performed RNA-Seq on V1 tissue samples from 28 individuals, representing 13 species of anthropoid primates, including hominoids, cercopithecoids, and platyrrhines. We explored trait-dependent differential expression (DE) by contrasting species with different visual system phenotypes and ecological traits. Between 4-25% of genes were determined to be differentially expressed in primates that varied in type of color vision (trichromatic or polymorphic di/trichromatic), habitat use (arboreal or terrestrial), group size (large or small), and primary diet (frugivorous, folivorous, or omnivorous). DE analyses revealed that humans and chimpanzees showed the most marked differences between any two species, despite the fact that they are only separated by 6-8 million years of independent evolution. Pathway enrichment analyses of DE genes demonstrated that changes in cellular metabolic pathways (e.g. glycolysis) contribute to altered gene expression in primate V1 more than neuron-specific processes (e.g. synaptic signaling). The exception to this trend is between human and chimpanzee, which exhibited DE for a number of processes related to cholinergic and GABAergic synaptic signaling. Conclusions : Our data significantly expand the number of primate species for which V1 expression data exists. These results show a combination of species-specific and trait-dependent differences in the evolution of gene expression in primate V1. We also show that human-specific changes in brain gene expression extend to the primary visual cortex in a manner similar to that reported of other brain regions. Evolutionary Biology Evolutionary Developmental Biology Brain evolution metabolic phenotype genomics visual cortex gene expression Figures Figure 1 Figure 2 Figure 3 Full Text Supplementary Files ZintelV1SITables.xlsx Cite Share Download PDF Status: Posted 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-11379","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research article","associatedPublications":[],"authors":[{"id":291154,"identity":"ba2c55db-023e-43d8-83a8-135c663c0243","order_by":1,"name":"Trisha Marie Zintel","email":"","orcid":"https://orcid.org/0000-0001-7356-0867","institution":"University of Massachusetts Amherst","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Trisha","middleName":"Marie","lastName":"Zintel","suffix":""},{"id":291155,"identity":"782dc880-0fab-4aa0-bfda-63ed2d0c8de4","order_by":2,"name":"John J. 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Babbitt","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA5ElEQVRIiWNgGAWjYDACCQY2ZgYDBgZ+CcYGhCgPYS0GEpIzSNPCYCBhcANZFJ8W/tnNzx4XFPypM77d3PiAsW2bvHz/AcYHb9vwWHLnmLnxDKDDzO4cbDZgbLttuOFGArPhXDxaDCQSzKR5QFpuJLZJALUwbgA6VZoXr5b0b2AtxjMgWuzn9x9g/41fSw7EFgMJiJbEhgMJbMz4tEjcOVMO9Iux5AyQXxLO3U7ecCOxWXLOOdxa+Ge3b3tc8EeOH8h4+OBD2W3b+f2HD354U4ZbCypIAJPIcToKRsEoGAWjgCwAAC7RTynxH5QaAAAAAElFTkSuQmCC","orcid":"","institution":"","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Courtney","middleName":"C.","lastName":"Babbitt","suffix":""}],"badges":[],"createdAt":"2020-01-10 16:34:48","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.2.20778/v1","doiUrl":"https://doi.org/10.21203/rs.2.20778/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":361880,"identity":"237462a0-f974-4e10-8d9c-9de9ad847a81","added_by":"auto","created_at":"2020-01-14 16:21:12","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":130476,"visible":true,"origin":"","legend":"Phenotypic traits of species for which V1 gene expression was investigated. Phenotypic traits\nfor color vision, habitat use, and group size are mapped on the phylogeny and diet is depicted to the right of species names. Species without a diet indicator were coded 887 as omnivorous. The tree was generated\nusing 10k Trees Version 3 [79] and Mesquite [90].","description":"","filename":"Figure1V1TMZ.png","url":"https://assets-eu.researchsquare.com/files/ec8413f0-49ea-46dd-8c2a-9b8c7a3db1c0/v1/Figure1_V1_TMZ.png"},{"id":361882,"identity":"bee78184-9017-459e-b3e2-14b2506d43c3","added_by":"auto","created_at":"2020-01-14 16:21:13","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":64312,"visible":true,"origin":"","legend":"Humans and chimpanzees are the most divergent in V1 gene expression. A) principal\ncoordinate analyses (PCoA) of V1 transcriptomes color-coded by species. Shapes of points indicate clade:\ntriangles for hominoids, squares for cercopithecoids, and circles for platyrrhines. B) Hierarchical\n clustering of V1 transcriptomes of each sample with bootstrap values and the individual sample number\nin brackets.","description":"","filename":"Figure2V1TMZ.png","url":"https://assets-eu.researchsquare.com/files/ec8413f0-49ea-46dd-8c2a-9b8c7a3db1c0/v1/Figure2_V1_TMZ.png"},{"id":361883,"identity":"c5752049-926d-4a9d-8cb0-3297cab6409d","added_by":"auto","created_at":"2020-01-14 16:21:13","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":241337,"visible":true,"origin":"","legend":"Expression profiles of metabolic genes in primate V1 cluster by clade. Clustering of expression\nprofiles of 1,039 metabolic genes in primate V1. Highly correlated genes (columns) cluster together and\nsamples (rows) cluster based on Euclidean distance between expression values. Only species for which\nthere were greater than one sample per species were used. Averages of expression per gene were\n calculated across replicates per species. The bottom bar represents membership in the color-coded KEGG\n metabolic pathways for each gene in the heatmap.","description":"","filename":"Figure3V1TMZ.png","url":"https://assets-eu.researchsquare.com/files/ec8413f0-49ea-46dd-8c2a-9b8c7a3db1c0/v1/Figure3_V1_TMZ.png"},{"id":790636,"identity":"28685c85-aee6-4ba2-aae6-627c771b1615","added_by":"auto","created_at":"2020-03-31 00:49:31","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2015160,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-11379/v1/manuscript.pdf"},{"id":524284,"identity":"c98cc68a-55a3-4bcb-a648-f7e0e9f7ce9d","added_by":"auto","created_at":"2020-02-21 11:55:07","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":427067,"visible":true,"origin":"","legend":"","description":"","filename":"ZintelV1Manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/ec8413f0-49ea-46dd-8c2a-9b8c7a3db1c0/v1/Zintel_V1_Manuscript.pdf"},{"id":361886,"identity":"34ed89e3-dbfc-4a77-aeb6-508732711094","added_by":"auto","created_at":"2020-01-14 16:21:29","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":418667,"visible":true,"origin":"","legend":"","description":"","filename":"ZintelV1Manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/ec8413f0-49ea-46dd-8c2a-9b8c7a3db1c0/v1/Manuscript.pdf"},{"id":361881,"identity":"d5083085-a58f-46a0-8b4f-764575d0549b","added_by":"auto","created_at":"2020-01-14 16:21:13","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":427067,"visible":true,"origin":"","legend":"","description":"","filename":"ZintelV1Manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/ec8413f0-49ea-46dd-8c2a-9b8c7a3db1c0/v1/Zintel_V1_Manuscript.pdf"},{"id":13485326,"identity":"31ce81ad-736c-4f19-914e-68b11b890443","added_by":"auto","created_at":"2021-09-16 22:01:34","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":703808,"visible":true,"origin":"","legend":"","description":"","filename":"ZintelV1Manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-11379/v1_covered.pdf"},{"id":361879,"identity":"2286517b-be2a-4973-ab67-bec115a99a2a","added_by":"auto","created_at":"2020-01-14 16:21:12","extension":"xlsx","order_by":0,"title":"","display":"","copyAsset":false,"role":"supplement","size":2956352,"visible":true,"origin":"","legend":"","description":"","filename":"ZintelV1SITables.xlsx","url":"https://assets-eu.researchsquare.com/files/ec8413f0-49ea-46dd-8c2a-9b8c7a3db1c0/v1/Zintel_V1_SI_Tables.xlsx"}],"financialInterests":"","formattedTitle":"Ecological trait differences are associated with gene expression in the primary visual cortex of primates","fulltext":[{"header":"Full Text","content":"\u003cp\u003eThis preprint is available for \u003ca href='/article/rs-11379/latest.pdf' target='_blank'\u003edownload as a PDF\u003c/a\u003e.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":true,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"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":"Brain, evolution, metabolic, phenotype, genomics, visual cortex, gene expression","lastPublishedDoi":"10.21203/rs.2.20778/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.2.20778/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eBackground : Primate species differ drastically from most other mammals in how they visually perceive their environments, which is important for foraging, predator avoidance, and detection of social cues. Although it is well established that primates display diversity in color vision and various ecological specializations, it is not understood how visual system characteristics and ecological adaptations may be associated with gene expression levels within the primary visual cortex (V1). \u003c/p\u003e\u003cp\u003eResults :\u0026nbsp;We performed RNA-Seq on V1 tissue samples from 28 individuals, representing 13 species of anthropoid primates, including hominoids, cercopithecoids, and platyrrhines. We explored trait-dependent differential expression (DE) by contrasting species with different visual system phenotypes and ecological traits. Between 4-25% of genes were determined to be differentially expressed in primates that varied in type of color vision (trichromatic or polymorphic di/trichromatic), habitat use (arboreal or terrestrial), group size (large or small), and primary diet (frugivorous, folivorous, or omnivorous). DE analyses revealed that humans and chimpanzees showed the most marked differences between any two species, despite the fact that they are only separated by 6-8 million years of independent evolution. Pathway enrichment analyses of DE genes demonstrated that changes in cellular metabolic pathways (e.g. glycolysis) contribute to altered gene expression in primate V1 more than neuron-specific processes (e.g. synaptic signaling). The exception to this trend is between human and chimpanzee, which exhibited DE for a number of processes related to cholinergic and GABAergic synaptic signaling. \u003c/p\u003e\u003cp\u003eConclusions : Our data significantly expand the number of primate species for which V1 expression data exists.\u0026nbsp;These results show a combination of species-specific and trait-dependent differences in the evolution of gene expression in primate V1. We also show that human-specific changes in brain gene expression extend to the primary visual cortex in a manner similar to that reported of other brain regions.\u003c/p\u003e","manuscriptTitle":"Ecological trait differences are associated with gene expression in the primary visual cortex of primates","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2020-01-14 16:21:12","doi":"10.21203/rs.2.20778/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":"7c52a27c-b592-4e91-8cc0-dd204baa25a2","owner":[],"postedDate":"January 14th, 2020","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":49388,"name":"Evolutionary Biology"},{"id":49389,"name":"Evolutionary Developmental Biology"}],"tags":[],"updatedAt":"","versionOfRecord":[],"versionCreatedAt":"2020-01-14 16:21:12","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-11379","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"identity":"rs-11379","version":["v1"]},"buildId":"WrCJVZZCHTDjtuVLN7oU0","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}