{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,10]],"date-time":"2026-04-10T23:10:28Z","timestamp":1775862628865,"version":"3.50.1"},"reference-count":63,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2024,4,20]],"date-time":"2024-04-20T00:00:00Z","timestamp":1713571200000},"content-version":"vor","delay-in-days":110,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004359","name":"Swedish Research Council","doi-asserted-by":"publisher","award":["2018-03695"],"award-info":[{"award-number":["2018-03695"]}],"id":[{"id":"10.13039\/501100004359","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000275","name":"Leverhulme Trust","doi-asserted-by":"publisher","award":["RPG-2021-141"],"award-info":[{"award-number":["RPG-2021-141"]}],"id":[{"id":"10.13039\/501100000275","id-type":"DOI","asserted-by":"publisher"}]},{"name":"FCT- Portuguese Science Foundation","award":["PTDC\/BIA-EVL\/1614\/2021"],"award-info":[{"award-number":["PTDC\/BIA-EVL\/1614\/2021"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2024,1,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>The speciation process often takes a long time. The speciation continuum framework has been useful to reconstruct the evolutionary processes that result in the formation of new species but defining when this continuum starts is far from trivial. Although a panmictic population is often considered the initial condition of speciation, this is unrealistic for almost all species. Local or divergent adaptation are viewed by many researchers as processes that shape intraspecific diversity and thus are not part of speciation. We propose that speciation starts when reproductive isolation becomes greater than zero, arguing in favour of the alternative view that local adaptation necessarily involves some reproductive isolation, independently of whether it results in the completion of speciation. Given that local adaptation is widespread, the consequence is that most species are constantly in the process of speciating. The process of speciation is best represented as the formation of separate subnetworks, defined by reproductive isolation, within extended and fluid spatial networks of populations.<\/jats:p>","DOI":"10.1093\/evolinnean\/kzae003","type":"journal-article","created":{"date-parts":[[2024,4,21]],"date-time":"2024-04-21T00:20:05Z","timestamp":1713658805000},"source":"Crossref","is-referenced-by-count":26,"title":["Local adaptation and reproductive isolation: when does speciation start?"],"prefix":"10.1093","volume":"3","author":[{"given":"Roger K","family":"Butlin","sequence":"first","affiliation":[{"name":"Ecology and Evolutionary Biology, School of Biosciences, The University of Sheffield , Sheffield S10 2TN ,","place":["United Kingdom"]},{"name":"Department of Marine Sciences, University of Gothenburg, Tj\u00e4rn\u00f6 Marine Laboratory , SE 45296 Str\u00f6mstad ,","place":["Sweden"]}]},{"given":"Rui","family":"Faria","sequence":"additional","affiliation":[{"name":"CIBIO, Centro de Investigac\u0327a\u0303o em Biodiversidade e Recursos Gene\u0301ticos, InBIO, Laborato\u0301rio Associado, Universidade do Porto , Vaira\u0303o ,","place":["Portugal"]},{"name":"BIOPOLIS Program in Genomics, Biodiversity and Land Planning, CIBIO , Campus de Vair\u00e3o, 4485-661 Vair\u00e3o ,","place":["Portugal"]}]}],"member":"286","published-online":{"date-parts":[[2024,4,20]]},"reference":[{"key":"2025030422463099500_CIT0001","doi-asserted-by":"crossref","first-page":"1214","DOI":"10.1126\/science.abo7719","article-title":"The role of divergent ecological adaptation during allopatric speciation in vertebrates","volume":"378","author":"Anderson","year":"2022","journal-title":"Science"},{"key":"2025030422463099500_CIT0002","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1038\/nature13301","article-title":"Genetics of ecological divergence during speciation","volume":"511","author":"Arnegard","year":"2014","journal-title":"Nature"},{"key":"2025030422463099500_CIT0003","first-page":"2257","article-title":"Multiple mechanisms contribute to isolation by environment in the redheaded pine sawfly, Neodiprion lecontei","volume":"77","author":"Bagley","year":"2023","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0004","article-title":"Does","author":"Barraclough","year":"2024","journal-title":"Journal of Evolutionary Biology"},{"key":"2025030422463099500_CIT0005","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/hdy.1986.135","article-title":"The barrier to genetic exchange between hybridising populations","volume":"57","author":"Barton","year":"1986","journal-title":"Heredity"},{"key":"2025030422463099500_CIT0007","doi-asserted-by":"crossref","first-page":"1641","DOI":"10.1111\/jeb.12683","article-title":"How mechanisms of habitat preference evolve and promote divergence with gene flow","volume":"28","author":"Berner","year":"2015","journal-title":"Journal of Evolutionary Biology"},{"key":"2025030422463099500_CIT0008","doi-asserted-by":"crossref","first-page":"318","DOI":"10.1093\/evolut\/qpac004","article-title":"A multivariate view of the speciation continuum","volume":"77","author":"Bolnick","year":"2023","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0009","doi-asserted-by":"crossref","first-page":"1195","DOI":"10.1111\/jeb.14029","article-title":"The language of isolation: a commentary on Westram et al., 2022","volume":"35","author":"Butlin","year":"2022","journal-title":"Journal of Evolutionary Biology"},{"key":"2025030422463099500_CIT0010","doi-asserted-by":"crossref","first-page":"978","DOI":"10.1111\/evo.14235","article-title":"Homage to Felsenstein 1981, or why are there so few\/many species","volume":"75","author":"Butlin","year":"2021","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0011","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1086\/695136","article-title":"Coupling, reinforcement, and speciation","volume":"191","author":"Butlin","year":"2018","journal-title":"The American Naturalist"},{"key":"2025030422463099500_CIT0012","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1111\/bij.12762","article-title":"Genetic characterization of flat periwinkles (Littorinidae) from the Iberian Peninsula reveals interspecific hybridization and different degrees of differentiation","volume":"118","author":"Carvalho","year":"2016","journal-title":"Biological Journal of the Linnean Society"},{"key":"2025030422463099500_CIT0013","doi-asserted-by":"crossref","first-page":"1244","DOI":"10.1111\/evo.12346","article-title":"Niche dimensionality and the genetics of ecological speciation","volume":"68","author":"Chevin","year":"2014","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0014","volume-title":"Speciation","author":"Coyne","year":"2004"},{"key":"2025030422463099500_CIT0015","doi-asserted-by":"crossref","first-page":"e6","DOI":"10.24072\/pcjournal.226","article-title":"How does the mode of evolutionary divergence affect reproductive isolation","volume":"3","author":"De Sanctis","year":"2023","journal-title":"Peer Community Journal"},{"key":"2025030422463099500_CIT0016","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1038\/22521","article-title":"On the origin of species by sympatric speciation","volume":"400","author":"Dieckmann","year":"1999","journal-title":"Nature"},{"key":"2025030422463099500_CIT0017","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1086\/725865","article-title":"Temporal variation in selection influences microgeographic local adaptation","volume":"202","author":"Dittmar","year":"2023","journal-title":"The American Naturalist"},{"key":"2025030422463099500_CIT0018","first-page":"a041432","article-title":"Coupling of barriers to gene exchange: Causes and consequences","author":"Dopman","year":"2023","journal-title":"Cold Spring Harbor Perspectives in Biology"},{"key":"2025030422463099500_CIT0019","doi-asserted-by":"crossref","first-page":"513","DOI":"10.1111\/mec.12616","article-title":"Advances in ecological speciation: an integrative approach","volume":"23","author":"Faria","year":"2014","journal-title":"Molecular Ecology"},{"key":"2025030422463099500_CIT0020","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1016\/j.tig.2012.03.009","article-title":"The genomics of speciation-with-gene-flow","volume":"28","author":"Feder","year":"2012","journal-title":"Trends in Genetics"},{"key":"2025030422463099500_CIT0021","doi-asserted-by":"crossref","first-page":"1729","DOI":"10.1111\/j.1558-5646.2009.00943.x","article-title":"The efficacy of divergence hitchhiking in generating genomic islands during ecological speciation","volume":"64","author":"Feder","year":"2010","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0022","doi-asserted-by":"crossref","first-page":"124","DOI":"10.2307\/2407946","article-title":"Skepticism towards Santa Rosalia, or why are there so few kinds of animals","volume":"35","author":"Felsenstein","year":"1981","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0064","doi-asserted-by":"crossref","first-page":"2287","DOI":"10.1111\/mec.16867","article-title":"Evidence for ecotone speciation across an African rainforest-savanna gradient","volume":"32","author":"Freedman","year":"2023","journal-title":"Molecular Ecology"},{"key":"2025030422463099500_CIT0023","doi-asserted-by":"crossref","first-page":"3643","DOI":"10.1111\/j.1558-5646.2012.01785.x","article-title":"The language of speciation","volume":"66","author":"Harrison","year":"2012","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0024","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1146\/annurev-ecolsys-110218-024701","article-title":"Beyond reproductive isolation: demographic controls on the speciation process","volume":"50","author":"Harvey","year":"2019","journal-title":"Annual Review of Ecology, Evolution, and Systematics"},{"key":"2025030422463099500_CIT0025","doi-asserted-by":"crossref","first-page":"1383","DOI":"10.1139\/F09-074","article-title":"Ecological speciation! Or the lack thereof","volume":"66","author":"Hendry","year":"2009","journal-title":"Canadian Journal of Fisheries and Aquatic Sciences"},{"key":"2025030422463099500_CIT0026","doi-asserted-by":"crossref","first-page":"579","DOI":"10.1086\/597611","article-title":"A quantitative survey of local adaptation and fitness trade-offs","volume":"173","author":"Hereford","year":"2009","journal-title":"The American Naturalist"},{"key":"2025030422463099500_CIT0027","doi-asserted-by":"crossref","first-page":"6890","DOI":"10.1002\/ece3.6524","article-title":"Is population subdivision different from speciation? From phylogeography to species delimitation","volume":"10","author":"Huang","year":"2020","journal-title":"Ecology and Evolution"},{"key":"2025030422463099500_CIT0028","doi-asserted-by":"crossref","first-page":"337","DOI":"10.1016\/j.tig.2024.01.002","article-title":"Diverse pathways to speciation revealed by marine snails","volume":"40","author":"Johannesson","year":"2024","journal-title":"Trends in Genetics"},{"key":"2025030422463099500_CIT0029","doi-asserted-by":"crossref","first-page":"1225","DOI":"10.1111\/j.1461-0248.2004.00684.x","article-title":"Conceptual issues in local adaptation","volume":"7","author":"Kawecki","year":"2004","journal-title":"Ecology Letters"},{"key":"2025030422463099500_CIT0030","doi-asserted-by":"crossref","first-page":"20190528","DOI":"10.1098\/rstb.2019.0528","article-title":"Towards the completion of speciation: The evolution of reproductive isolation beyond the first barriers","volume":"375","author":"Kulmuni","year":"2020","journal-title":"Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences"},{"key":"2025030422463099500_CIT0031","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1093\/evlett\/qrad002","article-title":"On the fast track: hybrids adapt more rapidly than parental populations in a novel environment","volume":"8","author":"Kulmuni","year":"2023","journal-title":"Evolution Letters"},{"key":"2025030422463099500_CIT0065","doi-asserted-by":"crossref","DOI":"10.1093\/evlett\/qrae014","article-title":"Coupling of twelve putative chromosomal inversions maintains a strong barrier to gene flow between snail ecotypes","author":"Le Moan","year":"2024","journal-title":"Evolution Letters"},{"key":"2025030422463099500_CIT0033","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/j.tree.2005.02.010","article-title":"Hybridization as an invasion of the genome","volume":"20","author":"Mallet","year":"2005","journal-title":"Trends in Ecology and Evolution"},{"key":"2025030422463099500_CIT0034","doi-asserted-by":"crossref","first-page":"1175","DOI":"10.1111\/jeb.14052","article-title":"Reproductive isolation is a heuristic, not a measure: a commentary on Westram et al., 2022","volume":"35","author":"Mallet","year":"2022","journal-title":"Journal of Evolutionary Biology"},{"key":"2025030422463099500_CIT0035","doi-asserted-by":"crossref","first-page":"637","DOI":"10.1086\/282457","article-title":"Sympatric speciation","volume":"100","author":"Maynard Smith","year":"1966","journal-title":"The American Naturalist"},{"key":"2025030422463099500_CIT0036","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.2307\/2408147","article-title":"Speciation and macroevolution","volume":"36","author":"Mayr","year":"1982","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0037","doi-asserted-by":"crossref","first-page":"1183","DOI":"10.1111\/jeb.14037","article-title":"Forty-two, and other precise answers to difficult questions: a commentary on Westram et al","volume":"35","author":"Moyle","year":"2022","journal-title":"Journal of Evolutionary Biology"},{"key":"2025030422463099500_CIT0038","doi-asserted-by":"crossref","first-page":"12084","DOI":"10.1073\/pnas.221274498","article-title":"Chromosomal inversions and the reproductive isolation of species","volume":"98","author":"Noor","year":"2001","journal-title":"Proceedings of the National Academy of Sciences of the United States of America"},{"key":"2025030422463099500_CIT0039","doi-asserted-by":"crossref","DOI":"10.1093\/acprof:osobl\/9780199587100.001.0001","volume-title":"Ecological Speciation","author":"Nosil","year":"2012"},{"key":"2025030422463099500_CIT0040","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1111\/j.1558-5646.2007.00299.x","article-title":"Heterogeneous genomic differentiation between walking-stick ecotypes: \u2018isolation by adaptation\u2019 and multiple roles for divergent selection","volume":"62","author":"Nosil","year":"2008","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0041","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1126\/science.abf6671","article-title":"How many genetic changes create new species","volume":"371","author":"Nosil","year":"2021","journal-title":"Science"},{"key":"2025030422463099500_CIT0042","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/j.tree.2008.10.011","article-title":"Ecological explanations for (incomplete) speciation","volume":"24","author":"Nosil","year":"2009","journal-title":"Trends in Ecology and Evolution"},{"key":"2025030422463099500_CIT0043","first-page":"705","article-title":"Reproductive isolation caused by natural selection against immigrants from divergent habitats","volume":"59","author":"Nosil","year":"2005","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0044","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1111\/bij.12703","article-title":"Reproductive isolation and the causes of speciation rate variation in nature","volume":"118","author":"Rabosky","year":"2016","journal-title":"Biological Journal of the Linnean Society"},{"key":"2025030422463099500_CIT0045","doi-asserted-by":"crossref","first-page":"1288","DOI":"10.1111\/evo.14223","article-title":"Inversions and genomic differentiation after secondary contact: when drift contributes to maintenance, not loss, of differentiation","volume":"75","author":"Rafajlovi\u0107","year":"2021","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0046","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/S0169-5347(01)02187-5","article-title":"Chromosomal rearrangements and speciation","volume":"16","author":"Rieseberg","year":"2001","journal-title":"Trends in Ecology and Evolution"},{"key":"2025030422463099500_CIT0047","doi-asserted-by":"crossref","first-page":"S4","DOI":"10.1086\/657060","article-title":"Adaptation and the origin of species","volume":"176","author":"Schemske","year":"2010","journal-title":"The American Naturalist"},{"key":"2025030422463099500_CIT0048","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1016\/S0169-5347(01)02198-X","article-title":"Ecology and the origin of species","volume":"16","author":"Schluter","year":"2001","journal-title":"Trends in Ecology and Evolution"},{"key":"2025030422463099500_CIT0049","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1126\/science.1160006","article-title":"Evidence for ecological speciation and its alternative","volume":"323","author":"Schluter","year":"2009","journal-title":"Science"},{"key":"2025030422463099500_CIT0050","doi-asserted-by":"crossref","first-page":"a041442","DOI":"10.1101\/cshperspect.a041442","article-title":"Fisher\u2019s geometric model as a tool to study speciation","author":"Schneemann","year":"2024","journal-title":"Cold Spring Harbor Perspectives in Biology"},{"key":"2025030422463099500_CIT0051","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1038\/nrg3644","article-title":"Genomics and the origin of species","volume":"15","author":"Seehausen","year":"2014","journal-title":"Nature Reviews Genetics"},{"key":"2025030422463099500_CIT0052","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1111\/evo.13880","article-title":"The evolution of partial reproductive isolation as an adaptive optimum","volume":"74","author":"Servedio","year":"2020","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0053","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1146\/annurev.ecolsys.34.011802.132412","article-title":"The role of reinforcement in speciation: theory and data","volume":"34","author":"Servedio","year":"2003","journal-title":"Annual Review of Ecology, Evolution, and Systematics"},{"key":"2025030422463099500_CIT0054","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1093\/genetics\/75.4.733","article-title":"Gene flow and selection in a cline","volume":"75","author":"Slatkin","year":"1973","journal-title":"Genetics"},{"key":"2025030422463099500_CIT0055","doi-asserted-by":"crossref","first-page":"1511","DOI":"10.1111\/evo.12362","article-title":"Unification of methods for estimating the strength of reproductive isolation","volume":"68","author":"Sobel","year":"2014","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0056","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1111\/j.1558-5646.2009.00877.x","article-title":"The biology of speciation","volume":"64","author":"Sobel","year":"2010","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0057","doi-asserted-by":"crossref","DOI":"10.1093\/evolinnean\/kzae001","article-title":"Toward the integration of speciation research","author":"Stankowski","year":"2024","journal-title":"Evolutionary Journal of the Linnean Society"},{"key":"2025030422463099500_CIT0058","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1111\/evo.14215","article-title":"Defining the speciation continuum","volume":"75","author":"Stankowski","year":"2021","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0059","doi-asserted-by":"crossref","first-page":"2510","DOI":"10.1111\/evo.13323","article-title":"Immigrant reproductive dysfunction facilitates ecological speciation","volume":"71","author":"Svensson","year":"2017","journal-title":"Evolution"},{"key":"2025030422463099500_CIT0060","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1002\/evl3.106","article-title":"Parallel genetic evolution and speciation from standing variation","volume":"3","author":"Thompson","year":"2019","journal-title":"Evolution Letters"},{"key":"2025030422463099500_CIT0066","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1111\/j.1365-294X.2009.04465.x","article-title":"Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison-dart frog","volume":"19","author":"Wang","year":"2009","journal-title":"Molecular Ecology"},{"key":"2025030422463099500_CIT0061","doi-asserted-by":"crossref","first-page":"1143","DOI":"10.1111\/jeb.14005","article-title":"What is reproductive isolation","volume":"35","author":"Westram","year":"2022","journal-title":"Journal of Evolutionary Biology"},{"key":"2025030422463099500_CIT0062","doi-asserted-by":"crossref","first-page":"1200","DOI":"10.1111\/jeb.14082","article-title":"Reproductive isolation, speciation, and the value of disagreement: a reply to the commentaries on \u2018What is reproductive isolation?\u2019","volume":"35","author":"Westram","year":"2022","journal-title":"Journal of Evolutionary Biology"}],"container-title":["Evolutionary Journal of the Linnean Society"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/evolinnean\/advance-article-pdf\/doi\/10.1093\/evolinnean\/kzae003\/57294323\/kzae003.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/evolinnean\/article-pdf\/3\/1\/kzae003\/59008799\/kzae003.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/evolinnean\/article-pdf\/3\/1\/kzae003\/59008799\/kzae003.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,4]],"date-time":"2025-03-04T22:46:55Z","timestamp":1741128415000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/evolinnean\/article\/doi\/10.1093\/evolinnean\/kzae003\/7655502"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,1,1]]},"references-count":63,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2024,1,1]]}},"URL":"https:\/\/doi.org\/10.1093\/evolinnean\/kzae003","relation":{},"ISSN":["2752-938X"],"issn-type":[{"value":"2752-938X","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2024,1,1]]},"published":{"date-parts":[[2024,1,1]]},"article-number":"kzae003"}}