{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T16:51:13Z","timestamp":1791996673641,"version":"4.4.0"},"reference-count":62,"publisher":"Wiley","issue":"19","license":[{"start":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T00:00:00Z","timestamp":1790553600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,9,28]],"date-time":"2026-09-28T00:00:00Z","timestamp":1790553600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["1R01AI123659\u201001A1"],"award-info":[{"award-number":["1R01AI123659\u201001A1"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000936","name":"Gordon and Betty Moore Foundation","doi-asserted-by":"publisher","award":["GBMF9323"],"award-info":[{"award-number":["GBMF9323"]}],"id":[{"id":"10.13039\/100000936","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["P30 CA034196"],"award-info":[{"award-number":["P30 CA034196"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Molecular Ecology"],"published-print":{"date-parts":[[2026,10]]},"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>\n                    Rates of evolutionary change vary by gene. While some broad gene categories are highly conserved with little divergence over time, others undergo continuous selection pressure and are highly divergent among populations or species. But such comparative evolutionary studies rely on gene ontology categories that are rarely validated in the study's focal species. An alternative is to determine species\u2010specific gene functions using single\u2010cell RNA sequencing (scRNAseq) that identifies cell types and the characteristic genes that each expresses. Here, we combine scRNAseq with evolutionary genomics to understand whether certain cell types exhibit faster evolutionary divergence (using their characteristic genes) than other types of cells (using intestine, head kidney, liver and gill tissues from an emerging model organism, the threespine stickleback). Merging scRNAseq with population genomic data, we show that cell types differ in the rate at which their characteristic genes evolve, as measured by allele frequency divergence among many populations (\n                    <jats:italic>F<\/jats:italic>\n                    <jats:sub>ST<\/jats:sub>\n                    ) and the longer\u2010term effect of selection driving sequence differences between species (\n                    <jats:italic>dN<\/jats:italic>\n                    \/\n                    <jats:italic>dS<\/jats:italic>\n                    ratios). Neutrophils, B cells and fibroblasts exhibit elevated\n                    <jats:italic>F<\/jats:italic>\n                    <jats:sub>ST<\/jats:sub>\n                    at characteristic genes, while eosinophils in the intestine and thrombocytes in the head kidney exhibit lower\n                    <jats:italic>F<\/jats:italic>\n                    <jats:sub>ST<\/jats:sub>\n                    than the average for 1000 random genes (\n                    <jats:italic>dN<\/jats:italic>\n                    \/\n                    <jats:italic>dS<\/jats:italic>\n                    showed similar results). Genes' positions within the scRNAseq coexpression network (measured by graph theory metrics of centrality) also differed between cell types and there was a weak tendency for genes with higher closeness centrality to have higher\n                    <jats:italic>F<\/jats:italic>\n                    <jats:sub>ST<\/jats:sub>\n                    . These results highlight the value of merging scRNAseq technology with evolutionary population genomic data and reveal that genes which define immune cell types exhibit especially rapid evolution.\n                  <\/jats:p>","DOI":"10.1111\/mec.70565","type":"journal-article","created":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T03:07:03Z","timestamp":1790651223000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Rates of Evolution Differ Between Cell Types Identified by Single\u2010Cell\n                    <scp>RNAseq<\/scp>\n                    in Threespine Stickleback"],"prefix":"10.1111","volume":"35","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0271-1303","authenticated-orcid":false,"given":"Maria L.","family":"Rodgers","sequence":"first","affiliation":[{"name":"Department of Ecology and Evolutionary Biology University of Connecticut  Storrs Connecticut USA"},{"name":"Department of Biological Sciences, Center for Marine Sciences and Technology North Carolina State University  Morehead City North Carolina USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Swapna","family":"Subramanian","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology University of Connecticut  Storrs Connecticut USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0197-7326","authenticated-orcid":false,"given":"Lauren E.","family":"Fuess","sequence":"additional","affiliation":[{"name":"Department of Biology Texas State University  San Marcos Texas USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0002-6004-4462","authenticated-orcid":false,"given":"Wan","family":"He","sequence":"additional","affiliation":[{"name":"Northeastern University, Institute of Experiential Artificial Intelligence  Boston Massachusetts USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5716-2770","authenticated-orcid":false,"given":"Samuel V.","family":"Scarpino","sequence":"additional","affiliation":[{"name":"Northeastern University, Institute of Experiential Artificial Intelligence  Boston Massachusetts USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4633-0702","authenticated-orcid":false,"given":"Andrea J.","family":"Roth\u2010Monz\u00f3n","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology University of Connecticut  Storrs Connecticut USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1701-3978","authenticated-orcid":false,"given":"Daniel L.","family":"Jeffries","sequence":"additional","affiliation":[{"name":"Division of Evolutionary Ecology, Institute of Ecology and Evolution University of Bern  Bern Switzerland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martine","family":"Seignon","sequence":"additional","affiliation":[{"name":"The Jackson Laboratory for Genomic Medicine  Farmington Connecticut USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8479-0809","authenticated-orcid":false,"given":"Kathryn","family":"Milligan\u2010McClellan","sequence":"additional","affiliation":[{"name":"Department of Molecular and Cell Biology University of Connecticut  Storrs Connecticut USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3002-7098","authenticated-orcid":false,"given":"Rebecca","family":"Carrier","sequence":"additional","affiliation":[{"name":"Department of Chemical Engineering Northeastern University  Boston Massachusetts USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7585-8402","authenticated-orcid":false,"given":"Natalie C.","family":"Steinel","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences University of Massachusetts Lowell  Lowell Massachusetts USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3148-6296","authenticated-orcid":false,"given":"Daniel I.","family":"Bolnick","sequence":"additional","affiliation":[{"name":"Department of Ecology and Evolutionary Biology University of Connecticut  Storrs Connecticut 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A.Nouri S.Keller et\u00a0al.2026.\u201cAn Intestinal Cell Atlas and Organoid Model for the Threespine Stickleback.\u201dPreprint bioRxiv.https:\/\/www.biorxiv.org\/content\/10.64898\/2026.06.25.734627v1.","DOI":"10.64898\/2026.06.25.734627"},{"key":"e_1_2_11_47_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41569-020-0359-y"},{"key":"e_1_2_11_48_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41581-018-0021-7"},{"key":"e_1_2_11_49_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-0716-1036-7_4"},{"key":"e_1_2_11_50_1","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-genom-111720-081402"},{"key":"e_1_2_11_51_1","doi-asserted-by":"publisher","DOI":"10.1038\/nbt.3192"},{"key":"e_1_2_11_52_1","doi-asserted-by":"publisher","DOI":"10.1093\/evlett\/qraf016"},{"key":"e_1_2_11_53_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.tig.2021.04.008"},{"key":"e_1_2_11_54_1","doi-asserted-by":"publisher","DOI":"10.1016\/0888-7543(91)90328-C"},{"key":"e_1_2_11_55_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-41695-z"},{"key":"e_1_2_11_56_1","first-page":"1","article-title":"A New Evolutionary Law","volume":"1","author":"Van Valen L.","year":"1973","journal-title":"Evolutionary Theory"},{"key":"e_1_2_11_57_1","doi-asserted-by":"publisher","DOI":"10.1111\/jeb.14181"},{"key":"e_1_2_11_58_1","doi-asserted-by":"publisher","DOI":"10.1093\/bioinformatics\/btag148"},{"key":"e_1_2_11_59_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.abo3411"},{"key":"e_1_2_11_60_1","volume-title":"dplyr: A Grammar of Data Manipulation","author":"Wickham H.","year":"2021"},{"key":"e_1_2_11_61_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-017-1382-0"},{"key":"e_1_2_11_62_1","doi-asserted-by":"publisher","DOI":"10.1093\/molbev\/msm088"},{"key":"e_1_2_11_63_1","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms14049"}],"container-title":["Molecular Ecology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/mec.70565","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1111\/mec.70565","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/mec.70565","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T16:26:53Z","timestamp":1791995213000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/mec.70565"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,9,28]]},"references-count":62,"journal-issue":{"issue":"19","published-print":{"date-parts":[[2026,10]]}},"alternative-id":["10.1111\/mec.70565"],"URL":"https:\/\/doi.org\/10.1111\/mec.70565","archive":["Portico"],"relation":{},"ISSN":["0962-1083","1365-294X"],"issn-type":[{"value":"0962-1083","type":"print"},{"value":"1365-294X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,9,28]]},"assertion":[{"value":"2026-02-12","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-10","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-09-28","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e70565"}}