[{"author":[{"first_name":"Aurélien","last_name":"De Jode","full_name":"De Jode, Aurélien"},{"full_name":"Le Moan, Alan","last_name":"Le Moan","first_name":"Alan"},{"first_name":"Kerstin","last_name":"Johannesson","full_name":"Johannesson, Kerstin"},{"full_name":"Faria, Rui","first_name":"Rui","last_name":"Faria"},{"full_name":"Stankowski, Sean","last_name":"Stankowski","first_name":"Sean","id":"43161670-5719-11EA-8025-FABC3DDC885E"},{"id":"3C147470-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-1050-4969","last_name":"Westram","first_name":"Anja M","full_name":"Westram, Anja M"},{"last_name":"Butlin","first_name":"Roger K.","full_name":"Butlin, Roger K."},{"full_name":"Rafajlović, Marina","first_name":"Marina","last_name":"Rafajlović"},{"id":"32DF5794-F248-11E8-B48F-1D18A9856A87","first_name":"Christelle","orcid":"0000-0001-8441-5075","last_name":"Fraisse","full_name":"Fraisse, Christelle"}],"abstract":[{"lang":"eng","text":"Understanding population divergence that eventually leads to speciation is essential for evolutionary biology. High species diversity in the sea was regarded as a paradox when strict allopatry was considered necessary for most speciation events because geographical barriers seemed largely absent in the sea, and many marine species have high dispersal capacities. Combining genome-wide data with demographic modelling to infer the demographic history of divergence has introduced new ways to address this classical issue. These models assume an ancestral population that splits into two subpopulations diverging according to different scenarios that allow tests for periods of gene flow. Models can also test for heterogeneities in population sizes and migration rates along the genome to account, respectively, for background selection and selection against introgressed ancestry. To investigate how barriers to gene flow arise in the sea, we compiled studies modelling the demographic history of divergence in marine organisms and extracted preferred demographic scenarios together with estimates of demographic parameters. These studies show that geographical barriers to gene flow do exist in the sea but that divergence can also occur without strict isolation. Heterogeneity of gene flow was detected in most population pairs suggesting the predominance of semipermeable barriers during divergence. We found a weak positive relationship between the fraction of the genome experiencing reduced gene flow and levels of genome-wide differentiation. Furthermore, we found that the upper bound of the ‘grey zone of speciation’ for our dataset extended beyond that found before, implying that gene flow between diverging taxa is possible at higher levels of divergence than previously thought. Finally, we list recommendations for further strengthening the use of demographic modelling in speciation research. These include a more balanced representation of taxa, more consistent and comprehensive modelling, clear reporting of results and simulation studies to rule out nonbiological explanations for general results."}],"issue":"2","date_created":"2022-07-03T22:01:33Z","_id":"11479","date_published":"2023-02-01T00:00:00Z","scopus_import":"1","license":"https://creativecommons.org/licenses/by/4.0/","month":"02","language":[{"iso":"eng"}],"doi":"10.1111/eva.13428","year":"2023","ddc":["576"],"type":"journal_article","date_updated":"2023-08-01T12:25:44Z","publication_status":"published","intvolume":"        16","day":"01","oa":1,"citation":{"apa":"De Jode, A., Le Moan, A., Johannesson, K., Faria, R., Stankowski, S., Westram, A. M., … Fraisse, C. (2023). Ten years of demographic modelling of divergence and speciation in the sea. <i>Evolutionary Applications</i>. Wiley. <a href=\"https://doi.org/10.1111/eva.13428\">https://doi.org/10.1111/eva.13428</a>","mla":"De Jode, Aurélien, et al. “Ten Years of Demographic Modelling of Divergence and Speciation in the Sea.” <i>Evolutionary Applications</i>, vol. 16, no. 2, Wiley, 2023, pp. 542–59, doi:<a href=\"https://doi.org/10.1111/eva.13428\">10.1111/eva.13428</a>.","ama":"De Jode A, Le Moan A, Johannesson K, et al. Ten years of demographic modelling of divergence and speciation in the sea. <i>Evolutionary Applications</i>. 2023;16(2):542-559. doi:<a href=\"https://doi.org/10.1111/eva.13428\">10.1111/eva.13428</a>","ista":"De Jode A, Le Moan A, Johannesson K, Faria R, Stankowski S, Westram AM, Butlin RK, Rafajlović M, Fraisse C. 2023. Ten years of demographic modelling of divergence and speciation in the sea. Evolutionary Applications. 16(2), 542–559.","short":"A. De Jode, A. Le Moan, K. Johannesson, R. Faria, S. Stankowski, A.M. Westram, R.K. Butlin, M. Rafajlović, C. Fraisse, Evolutionary Applications 16 (2023) 542–559.","chicago":"De Jode, Aurélien, Alan Le Moan, Kerstin Johannesson, Rui Faria, Sean Stankowski, Anja M Westram, Roger K. Butlin, Marina Rafajlović, and Christelle Fraisse. “Ten Years of Demographic Modelling of Divergence and Speciation in the Sea.” <i>Evolutionary Applications</i>. Wiley, 2023. <a href=\"https://doi.org/10.1111/eva.13428\">https://doi.org/10.1111/eva.13428</a>.","ieee":"A. De Jode <i>et al.</i>, “Ten years of demographic modelling of divergence and speciation in the sea,” <i>Evolutionary Applications</i>, vol. 16, no. 2. Wiley, pp. 542–559, 2023."},"isi":1,"quality_controlled":"1","publication_identifier":{"eissn":["1752-4571"]},"file":[{"file_size":2269822,"success":1,"file_id":"12685","creator":"dernst","relation":"main_file","content_type":"application/pdf","file_name":"2023_EvolutionaryApplications_DeJode.pdf","date_updated":"2023-02-27T07:10:17Z","date_created":"2023-02-27T07:10:17Z","checksum":"d4d6fa9ddf36643af994a6a757919afb","access_level":"open_access"}],"volume":16,"oa_version":"Published Version","page":"542-559","article_type":"original","tmp":{"image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)"},"publication":"Evolutionary Applications","article_processing_charge":"No","external_id":{"isi":["000815663700001"]},"acknowledgement":"We greatly thank all the corresponding authors of the studies that were included in our synthesis for the sharing of additional data: Thomas Broquet, Dmitry Filatov, Quentin Rougemont, Paolo Momigliano, Pierre-Alexandre Gagnaire, Carlos Prada, Ahmed Souissi, Michael Møller Hansen, Sylvie Lapègue, Joseph Di Battista, Michael Hellberg and Carlos Prada. RKB and ADJ were supported by the European Research Council. MR was supported by the Swedish Research Council Vetenskapsrådet (grant number 2021-05243; to MR) and Formas (grant number 2019-00882; to KJ and MR), and by additional grants from the European Research Council (to RKB) and Vetenskapsrådet (to KJ) through the Centre for Marine Evolutionary Biology (https://www.gu.se/en/cemeb-marine-evolutionary-biology).","publisher":"Wiley","status":"public","has_accepted_license":"1","title":"Ten years of demographic modelling of divergence and speciation in the sea","department":[{"_id":"NiBa"},{"_id":"BeVi"}],"file_date_updated":"2023-02-27T07:10:17Z","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8"},{"article_type":"review","oa_version":"Published Version","tmp":{"short":"CC BY-NC (4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode","name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","image":"/images/cc_by_nc.png"},"main_file_link":[{"url":"https://doi.org/10.1111/jeb.14242","open_access":"1"}],"day":"08","article_number":"14242","citation":{"apa":"Berdan, E. L., Barton, N. H., Butlin, R., Charlesworth, B., Faria, R., Fragata, I., … Flatt, T. (2023). How chromosomal inversions reorient the evolutionary process. <i>Journal of Evolutionary Biology</i>. Wiley. <a href=\"https://doi.org/10.1111/jeb.14242\">https://doi.org/10.1111/jeb.14242</a>","ama":"Berdan EL, Barton NH, Butlin R, et al. How chromosomal inversions reorient the evolutionary process. <i>Journal of Evolutionary Biology</i>. 2023. doi:<a href=\"https://doi.org/10.1111/jeb.14242\">10.1111/jeb.14242</a>","mla":"Berdan, Emma L., et al. “How Chromosomal Inversions Reorient the Evolutionary Process.” <i>Journal of Evolutionary Biology</i>, 14242, Wiley, 2023, doi:<a href=\"https://doi.org/10.1111/jeb.14242\">10.1111/jeb.14242</a>.","ista":"Berdan EL, Barton NH, Butlin R, Charlesworth B, Faria R, Fragata I, Gilbert KJ, Jay P, Kapun M, Lotterhos KE, Mérot C, Durmaz Mitchell E, Pascual M, Peichel CL, Rafajlović M, Westram AM, Schaeffer SW, Johannesson K, Flatt T. 2023. How chromosomal inversions reorient the evolutionary process. Journal of Evolutionary Biology., 14242.","short":"E.L. Berdan, N.H. Barton, R. Butlin, B. Charlesworth, R. Faria, I. Fragata, K.J. Gilbert, P. Jay, M. Kapun, K.E. Lotterhos, C. Mérot, E. Durmaz Mitchell, M. Pascual, C.L. Peichel, M. Rafajlović, A.M. Westram, S.W. Schaeffer, K. Johannesson, T. Flatt, Journal of Evolutionary Biology (2023).","chicago":"Berdan, Emma L., Nicholas H Barton, Roger Butlin, Brian Charlesworth, Rui Faria, Inês Fragata, Kimberly J. Gilbert, et al. “How Chromosomal Inversions Reorient the Evolutionary Process.” <i>Journal of Evolutionary Biology</i>. Wiley, 2023. <a href=\"https://doi.org/10.1111/jeb.14242\">https://doi.org/10.1111/jeb.14242</a>.","ieee":"E. L. Berdan <i>et al.</i>, “How chromosomal inversions reorient the evolutionary process,” <i>Journal of Evolutionary Biology</i>. Wiley, 2023."},"oa":1,"quality_controlled":"1","publication_identifier":{"issn":["1010-061X"],"eissn":["1420-9101"]},"publisher":"Wiley","has_accepted_license":"1","status":"public","title":"How chromosomal inversions reorient the evolutionary process","department":[{"_id":"NiBa"}],"user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","publication":"Journal of Evolutionary Biology","article_processing_charge":"No","acknowledgement":"We are grateful to two referees and Luke Holman for valuable comments on a previous version of our manuscript. This paper was conceived at the ESEB Progress Meeting ‘Disentangling neutral versus adaptive evolution in chromosomal inversions’, organized by ELB, KJ and TF and held at Tjärnö Marine Laboratory (Sweden) between 28 February and 3 March 2022. We are indebted to ESEB for sponsoring our workshop and to the following funding bodies for supporting our research: ERC AdG 101055327 to NHB; Swedish Research Council (VR) 2018-03695 and Leverhulme Trust RPG-2021-141 to RKB; Fundação para a Ciência e a Tecnologia (FCT) contract 2020.00275.CEECIND and research project PTDC/BIA-1232 EVL/1614/2021 to RF; Fundação para a Ciência e a Tecnologia (FCT) junior researcher contract CEECIND/02616/2018 to IF; Swiss National Science Foundation (SNSF) Ambizione #PZ00P3_185952 to KJG; National Science Foundation NSF-OCE 2043905 and NSF-DEB 1655701 to KEL; Swiss National Science Foundation (SNSF) 310030_204681 to CLP; Swedish Research Council (VR) 2021-05243 to MR; Norwegian Research Council grant 315287 to AMW; Swiss National Science Foundation (SNSF) 31003A-182262 and FZEB-0-214654 to TF. We also thank Luca Ferretti for the discussion and Eliane Zinn (Flatt lab) for help with reference formatting.","date_created":"2023-11-19T23:00:55Z","_id":"14556","scopus_import":"1","date_published":"2023-11-08T00:00:00Z","license":"https://creativecommons.org/licenses/by-nc/4.0/","author":[{"last_name":"Berdan","first_name":"Emma L.","full_name":"Berdan, Emma L."},{"id":"4880FE40-F248-11E8-B48F-1D18A9856A87","full_name":"Barton, Nicholas H","first_name":"Nicholas H","orcid":"0000-0002-8548-5240","last_name":"Barton"},{"full_name":"Butlin, Roger","first_name":"Roger","last_name":"Butlin"},{"last_name":"Charlesworth","first_name":"Brian","full_name":"Charlesworth, Brian"},{"last_name":"Faria","first_name":"Rui","full_name":"Faria, Rui"},{"full_name":"Fragata, Inês","last_name":"Fragata","first_name":"Inês"},{"full_name":"Gilbert, Kimberly J.","last_name":"Gilbert","first_name":"Kimberly J."},{"full_name":"Jay, Paul","first_name":"Paul","last_name":"Jay"},{"last_name":"Kapun","first_name":"Martin","full_name":"Kapun, Martin"},{"first_name":"Katie E.","last_name":"Lotterhos","full_name":"Lotterhos, Katie E."},{"first_name":"Claire","last_name":"Mérot","full_name":"Mérot, Claire"},{"first_name":"Esra","last_name":"Durmaz Mitchell","full_name":"Durmaz Mitchell, Esra"},{"full_name":"Pascual, Marta","first_name":"Marta","last_name":"Pascual"},{"last_name":"Peichel","first_name":"Catherine L.","full_name":"Peichel, Catherine L."},{"full_name":"Rafajlović, Marina","last_name":"Rafajlović","first_name":"Marina"},{"first_name":"Anja M","orcid":"0000-0003-1050-4969","last_name":"Westram","full_name":"Westram, Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Schaeffer, Stephen W.","first_name":"Stephen W.","last_name":"Schaeffer"},{"full_name":"Johannesson, Kerstin","first_name":"Kerstin","last_name":"Johannesson"},{"full_name":"Flatt, Thomas","first_name":"Thomas","last_name":"Flatt"}],"abstract":[{"text":"Inversions are structural mutations that reverse the sequence of a chromosome segment and reduce the effective rate of recombination in the heterozygous state. They play a major role in adaptation, as well as in other evolutionary processes such as speciation. Although inversions have been studied since the 1920s, they remain difficult to investigate because the reduced recombination conferred by them strengthens the effects of drift and hitchhiking, which in turn can obscure signatures of selection. Nonetheless, numerous inversions have been found to be under selection. Given recent advances in population genetic theory and empirical study, here we review how different mechanisms of selection affect the evolution of inversions. A key difference between inversions and other mutations, such as single nucleotide variants, is that the fitness of an inversion may be affected by a larger number of frequently interacting processes. This considerably complicates the analysis of the causes underlying the evolution of inversions. We discuss the extent to which these mechanisms can be disentangled, and by which approach.","lang":"eng"}],"date_updated":"2023-11-20T08:51:09Z","type":"journal_article","publication_status":"epub_ahead","month":"11","language":[{"iso":"eng"}],"year":"2023","doi":"10.1111/jeb.14242","ddc":["570"]},{"language":[{"iso":"eng"}],"month":"11","year":"2023","doi":"10.1101/cshperspect.a041447","date_updated":"2024-01-08T12:52:29Z","type":"journal_article","intvolume":"        15","keyword":["General Biochemistry","Genetics and Molecular Biology"],"publication_status":"published","issue":"11","abstract":[{"text":"Chromosomal rearrangements (CRs) have been known since almost the beginning of genetics.\r\nWhile an important role for CRs in speciation has been suggested, evidence primarily stems\r\nfrom theoretical and empirical studies focusing on the microevolutionary level (i.e., on taxon\r\npairs where speciation is often incomplete). Although the role of CRs in eukaryotic speciation at\r\na macroevolutionary level has been supported by associations between species diversity and\r\nrates of evolution of CRs across phylogenies, these findings are limited to a restricted range of\r\nCRs and taxa. Now that more broadly applicable and precise CR detection approaches have\r\nbecome available, we address the challenges in filling some of the conceptual and empirical\r\ngaps between micro- and macroevolutionary studies on the role of CRs in speciation. We\r\nsynthesize what is known about the macroevolutionary impact of CRs and suggest new research avenues to overcome the pitfalls of previous studies to gain a more comprehensive understanding of the evolutionary significance of CRs in speciation across the tree of life.","lang":"eng"}],"author":[{"full_name":"Lucek, Kay","last_name":"Lucek","first_name":"Kay"},{"last_name":"Giménez","first_name":"Mabel D.","full_name":"Giménez, Mabel D."},{"full_name":"Joron, Mathieu","last_name":"Joron","first_name":"Mathieu"},{"first_name":"Marina","last_name":"Rafajlović","full_name":"Rafajlović, Marina"},{"full_name":"Searle, Jeremy B.","last_name":"Searle","first_name":"Jeremy B."},{"last_name":"Walden","first_name":"Nora","full_name":"Walden, Nora"},{"id":"3C147470-F248-11E8-B48F-1D18A9856A87","full_name":"Westram, Anja M","last_name":"Westram","orcid":"0000-0003-1050-4969","first_name":"Anja M"},{"last_name":"Faria","first_name":"Rui","full_name":"Faria, Rui"}],"_id":"14742","date_created":"2024-01-08T12:43:48Z","pmid":1,"scopus_import":"1","date_published":"2023-11-01T00:00:00Z","article_processing_charge":"No","publication":"Cold Spring Harbor Perspectives in Biology","external_id":{"pmid":["37604585"]},"acknowledgement":"K.L. was funded by a Swiss National Science Foundation Eccellenza project: The evolution of strong reproductive barriers towards the completion of speciation (PCEFP3_202869). R.F.\r\nwas funded by an FCT CEEC (Fundação para a Ciênca e a Tecnologia, Concurso Estímulo ao\r\nEmprego Científico) contract (2020.00275. CEECIND) and by an FCT research project\r\n(PTDC/BIA-EVL/1614/2021). M.R. was funded by the Swedish Research Council Vetenskapsrådet (grant number 2021-05243). A.M.W. was partly funded by the Norwegian Research Council RCN. We thank Luis Silva for his help preparing Figure 1. We are grateful to Maren Wellenreuther, Daniel Bolnick, and two anonymous reviewers for their constructive feedback on an earlier version of this paper.","publisher":"Cold Spring Harbor Laboratory","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","title":"The impact of chromosomal rearrangements in speciation: From micro- to macroevolution","status":"public","department":[{"_id":"NiBa"},{"_id":"BeVi"}],"citation":{"ieee":"K. Lucek <i>et al.</i>, “The impact of chromosomal rearrangements in speciation: From micro- to macroevolution,” <i>Cold Spring Harbor Perspectives in Biology</i>, vol. 15, no. 11. Cold Spring Harbor Laboratory, 2023.","chicago":"Lucek, Kay, Mabel D. Giménez, Mathieu Joron, Marina Rafajlović, Jeremy B. Searle, Nora Walden, Anja M Westram, and Rui Faria. “The Impact of Chromosomal Rearrangements in Speciation: From Micro- to Macroevolution.” <i>Cold Spring Harbor Perspectives in Biology</i>. Cold Spring Harbor Laboratory, 2023. <a href=\"https://doi.org/10.1101/cshperspect.a041447\">https://doi.org/10.1101/cshperspect.a041447</a>.","short":"K. Lucek, M.D. Giménez, M. Joron, M. Rafajlović, J.B. Searle, N. Walden, A.M. Westram, R. Faria, Cold Spring Harbor Perspectives in Biology 15 (2023).","ista":"Lucek K, Giménez MD, Joron M, Rafajlović M, Searle JB, Walden N, Westram AM, Faria R. 2023. The impact of chromosomal rearrangements in speciation: From micro- to macroevolution. Cold Spring Harbor Perspectives in Biology. 15(11), a041447.","apa":"Lucek, K., Giménez, M. D., Joron, M., Rafajlović, M., Searle, J. B., Walden, N., … Faria, R. (2023). The impact of chromosomal rearrangements in speciation: From micro- to macroevolution. <i>Cold Spring Harbor Perspectives in Biology</i>. Cold Spring Harbor Laboratory. <a href=\"https://doi.org/10.1101/cshperspect.a041447\">https://doi.org/10.1101/cshperspect.a041447</a>","ama":"Lucek K, Giménez MD, Joron M, et al. The impact of chromosomal rearrangements in speciation: From micro- to macroevolution. <i>Cold Spring Harbor Perspectives in Biology</i>. 2023;15(11). doi:<a href=\"https://doi.org/10.1101/cshperspect.a041447\">10.1101/cshperspect.a041447</a>","mla":"Lucek, Kay, et al. “The Impact of Chromosomal Rearrangements in Speciation: From Micro- to Macroevolution.” <i>Cold Spring Harbor Perspectives in Biology</i>, vol. 15, no. 11, a041447, Cold Spring Harbor Laboratory, 2023, doi:<a href=\"https://doi.org/10.1101/cshperspect.a041447\">10.1101/cshperspect.a041447</a>."},"oa":1,"day":"01","article_number":"a041447","publication_identifier":{"issn":["1943-0264"]},"quality_controlled":"1","article_type":"original","volume":15,"oa_version":"Published Version","main_file_link":[{"open_access":"1","url":"https://doi.org/10.1101/cshperspect.a041447"}]},{"citation":{"ista":"Stankowski S, Zagrodzka ZB, Galindo J, Montaño-Rendón M, Faria R, Mikhailova N, Blakeslee AMH, Arnason E, Broquet T, Morales HE, Grahame JW, Westram AM, Johannesson K, Butlin RK. 2023. Whole-genome phylogeography of the intertidal snail Littorina saxatilis. Evolutionary Journal of the Linnean Society. 2(1), kzad002.","apa":"Stankowski, S., Zagrodzka, Z. B., Galindo, J., Montaño-Rendón, M., Faria, R., Mikhailova, N., … Butlin, R. K. (2023). Whole-genome phylogeography of the intertidal snail Littorina saxatilis. <i>Evolutionary Journal of the Linnean Society</i>. Oxford University Press. <a href=\"https://doi.org/10.1093/evolinnean/kzad002\">https://doi.org/10.1093/evolinnean/kzad002</a>","ama":"Stankowski S, Zagrodzka ZB, Galindo J, et al. Whole-genome phylogeography of the intertidal snail Littorina saxatilis. <i>Evolutionary Journal of the Linnean Society</i>. 2023;2(1). doi:<a href=\"https://doi.org/10.1093/evolinnean/kzad002\">10.1093/evolinnean/kzad002</a>","mla":"Stankowski, Sean, et al. “Whole-Genome Phylogeography of the Intertidal Snail Littorina Saxatilis.” <i>Evolutionary Journal of the Linnean Society</i>, vol. 2, no. 1, kzad002, Oxford University Press, 2023, doi:<a href=\"https://doi.org/10.1093/evolinnean/kzad002\">10.1093/evolinnean/kzad002</a>.","ieee":"S. Stankowski <i>et al.</i>, “Whole-genome phylogeography of the intertidal snail Littorina saxatilis,” <i>Evolutionary Journal of the Linnean Society</i>, vol. 2, no. 1. Oxford University Press, 2023.","chicago":"Stankowski, Sean, Zuzanna B Zagrodzka, Juan Galindo, Mauricio Montaño-Rendón, Rui Faria, Natalia Mikhailova, April M H Blakeslee, et al. “Whole-Genome Phylogeography of the Intertidal Snail Littorina Saxatilis.” <i>Evolutionary Journal of the Linnean Society</i>. Oxford University Press, 2023. <a href=\"https://doi.org/10.1093/evolinnean/kzad002\">https://doi.org/10.1093/evolinnean/kzad002</a>.","short":"S. Stankowski, Z.B. Zagrodzka, J. Galindo, M. Montaño-Rendón, R. Faria, N. Mikhailova, A.M.H. Blakeslee, E. Arnason, T. Broquet, H.E. Morales, J.W. Grahame, A.M. Westram, K. Johannesson, R.K. Butlin, Evolutionary Journal of the Linnean Society 2 (2023)."},"oa":1,"day":"17","article_number":"kzad002","publication_identifier":{"eissn":["2752-938X"]},"quality_controlled":"1","article_type":"original","oa_version":"Published Version","volume":2,"file":[{"file_size":3408944,"success":1,"file_id":"14875","creator":"dernst","content_type":"application/pdf","relation":"main_file","file_name":"2023_EvolJourLinneanSociety_Stankowski.pdf","date_updated":"2024-01-23T08:10:00Z","date_created":"2024-01-23T08:10:00Z","checksum":"ba6f9102d3a9fe6631c4fa398c5e4313","access_level":"open_access"}],"tmp":{"short":"CC BY-NC (4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode","name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","image":"/images/cc_by_nc.png"},"article_processing_charge":"Yes (via OA deal)","publication":"Evolutionary Journal of the Linnean Society","acknowledgement":"Isobel Eyres, Richard Turney, Graciela Sotelo, Jenny Larson, and Stéphane Loisel helped with the collection and processing of samples. Petri Kemppainen kindly provided samples from Trondheim Fjord. Mark Dunning helped with the development of bioinformatic pipelines. The analysis of genomic data was conducted on the University of Sheffield high-performance computing cluster, ShARC. Funding was provided by the Natural Environment Research Council (NERC) and the European Research Council (ERC). J.G. was funded by a Juntas Industriales y Navales (JIN) project (Ministerio de Ciencia, Innovación y Universidades, code RTI2018-101274-J-I00).","publisher":"Oxford University Press","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","file_date_updated":"2024-01-23T08:10:00Z","department":[{"_id":"NiBa"}],"has_accepted_license":"1","title":"Whole-genome phylogeography of the intertidal snail Littorina saxatilis","status":"public","issue":"1","author":[{"full_name":"Stankowski, Sean","first_name":"Sean","last_name":"Stankowski","id":"43161670-5719-11EA-8025-FABC3DDC885E"},{"last_name":"Zagrodzka","first_name":"Zuzanna B","full_name":"Zagrodzka, Zuzanna B"},{"full_name":"Galindo, Juan","first_name":"Juan","last_name":"Galindo"},{"last_name":"Montaño-Rendón","first_name":"Mauricio","full_name":"Montaño-Rendón, Mauricio"},{"full_name":"Faria, Rui","first_name":"Rui","last_name":"Faria"},{"first_name":"Natalia","last_name":"Mikhailova","full_name":"Mikhailova, Natalia"},{"full_name":"Blakeslee, April M H","first_name":"April M H","last_name":"Blakeslee"},{"full_name":"Arnason, Einar","first_name":"Einar","last_name":"Arnason"},{"full_name":"Broquet, Thomas","last_name":"Broquet","first_name":"Thomas"},{"first_name":"Hernán E","last_name":"Morales","full_name":"Morales, Hernán E"},{"full_name":"Grahame, John W","last_name":"Grahame","first_name":"John W"},{"id":"3C147470-F248-11E8-B48F-1D18A9856A87","full_name":"Westram, Anja M","first_name":"Anja M","orcid":"0000-0003-1050-4969","last_name":"Westram"},{"full_name":"Johannesson, Kerstin","last_name":"Johannesson","first_name":"Kerstin"},{"full_name":"Butlin, Roger K","last_name":"Butlin","first_name":"Roger K"}],"abstract":[{"text":"Understanding the factors that have shaped the current distributions and diversity of species is a central and longstanding aim of evolutionary biology. The recent inclusion of genomic data into phylogeographic studies has dramatically improved our understanding in organisms where evolutionary relationships have been challenging to infer. We used whole-genome sequences to study the phylogeography of the intertidal snail Littorina saxatilis, which has successfully colonized and diversified across a broad range of coastal environments in the Northern Hemisphere amid repeated cycles of glaciation. Building on past studies based on short DNA sequences, we used genome-wide data to provide a clearer picture of the relationships among samples spanning most of the species natural range. Our results confirm the trans-Atlantic colonization of North America from Europe, and have allowed us to identify rough locations of glacial refugia and to infer likely routes of colonization within Europe. We also investigated the signals in different datasets to account for the effects of genomic architecture and non-neutral evolution, which provides new insights about diversification of four ecotypes of L. saxatilis (the crab, wave, barnacle, and brackish ecotypes) at different spatial scales. Overall, we provide a much clearer picture of the biogeography of L. saxatilis, providing a foundation for more detailed phylogenomic and demographic studies.","lang":"eng"}],"_id":"14833","date_created":"2024-01-18T07:54:10Z","date_published":"2023-08-17T00:00:00Z","language":[{"iso":"eng"}],"month":"08","ddc":["570"],"year":"2023","doi":"10.1093/evolinnean/kzad002","date_updated":"2024-01-23T08:13:43Z","type":"journal_article","intvolume":"         2","publication_status":"published"},{"quality_controlled":"1","isi":1,"publication_identifier":{"eissn":["1464-3766"],"issn":["0260-1230"]},"day":"01","article_number":"eyab049","citation":{"ista":"Perini S, Butlin R, Westram AM, Johannesson K. 2022. Very short mountings are enough for sperm transfer in Littorina saxatilis. Journal of Molluscan Studies. 88(1), eyab049.","apa":"Perini, S., Butlin, R., Westram, A. M., &#38; Johannesson, K. (2022). Very short mountings are enough for sperm transfer in Littorina saxatilis. <i>Journal of Molluscan Studies</i>. Oxford Academic. <a href=\"https://doi.org/10.1093/mollus/eyab049\">https://doi.org/10.1093/mollus/eyab049</a>","mla":"Perini, Samuel, et al. “Very Short Mountings Are Enough for Sperm Transfer in Littorina Saxatilis.” <i>Journal of Molluscan Studies</i>, vol. 88, no. 1, eyab049, Oxford Academic, 2022, doi:<a href=\"https://doi.org/10.1093/mollus/eyab049\">10.1093/mollus/eyab049</a>.","ama":"Perini S, Butlin R, Westram AM, Johannesson K. Very short mountings are enough for sperm transfer in Littorina saxatilis. <i>Journal of Molluscan Studies</i>. 2022;88(1). doi:<a href=\"https://doi.org/10.1093/mollus/eyab049\">10.1093/mollus/eyab049</a>","chicago":"Perini, Samuel, Rogerk Butlin, Anja M Westram, and Kerstin Johannesson. “Very Short Mountings Are Enough for Sperm Transfer in Littorina Saxatilis.” <i>Journal of Molluscan Studies</i>. Oxford Academic, 2022. <a href=\"https://doi.org/10.1093/mollus/eyab049\">https://doi.org/10.1093/mollus/eyab049</a>.","ieee":"S. Perini, R. Butlin, A. M. Westram, and K. Johannesson, “Very short mountings are enough for sperm transfer in Littorina saxatilis,” <i>Journal of Molluscan Studies</i>, vol. 88, no. 1. Oxford Academic, 2022.","short":"S. Perini, R. Butlin, A.M. Westram, K. Johannesson, Journal of Molluscan Studies 88 (2022)."},"oa":1,"main_file_link":[{"open_access":"1","url":"https://eprints.whiterose.ac.uk/187332/"}],"article_type":"original","oa_version":"Submitted Version","volume":88,"external_id":{"isi":["000759081600002"]},"publication":"Journal of Molluscan Studies","article_processing_charge":"No","department":[{"_id":"BeVi"}],"status":"public","title":"Very short mountings are enough for sperm transfer in Littorina saxatilis","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","publisher":"Oxford Academic","author":[{"first_name":"Samuel","last_name":"Perini","full_name":"Perini, Samuel"},{"full_name":"Butlin, Rogerk","first_name":"Rogerk","last_name":"Butlin"},{"id":"3C147470-F248-11E8-B48F-1D18A9856A87","full_name":"Westram, Anja M","first_name":"Anja M","orcid":"0000-0003-1050-4969","last_name":"Westram"},{"full_name":"Johannesson, Kerstin","first_name":"Kerstin","last_name":"Johannesson"}],"abstract":[{"lang":"eng","text":"Conflict over reproduction between females and males exists because of anisogamy and promiscuity. Together they generate differences in fitness optima between the sexes and result in antagonistic coevolution of female and male reproductive traits. Mounting duration is likely to be a compromise between male and female interests whose outcome depends on the intensity of sexual selection. The timing of sperm transfer during mounting is critical. For example, mountings may be interrupted before sperm is transferred as a consequence of female or male choice, or they may be prolonged to function as mate guarding. In the highly promiscuous intertidal snail Littorina saxatilis, mountings vary substantially in duration, from less than a minute to more than an hour, and it has been assumed that mountings of a few minutes do not result in any sperm being transferred. Here, we examined the timing of sperm transfer, a reproductive trait that is likely affected by sexual conflict. We performed time-controlled mounting trials using L. saxatilis males and virgin females, aiming to examine indirectly when the transfer of sperm starts. We observed the relationship between mounting duration and the proportion of developing embryos out of all eggs and embryos in the brood pouch. Developing embryos were observed in similar proportions in all treatments (i.e. 1, 5 and 10 or more minutes at which mountings were artificially interrupted), suggesting that sperm transfer begins rapidly (within 1 min) in L. saxatilis and very short matings do not result in sperm shortage in the females. We discuss how the observed pattern can be influenced by predation risk, population density, and female status and receptivity."}],"issue":"1","scopus_import":"1","date_published":"2022-03-01T00:00:00Z","date_created":"2022-03-27T22:01:46Z","_id":"10926","year":"2022","doi":"10.1093/mollus/eyab049","month":"03","language":[{"iso":"eng"}],"intvolume":"        88","publication_status":"published","date_updated":"2023-08-03T06:23:13Z","type":"journal_article"},{"_id":"11334","date_created":"2022-04-24T22:01:44Z","pmid":1,"date_published":"2022-05-01T00:00:00Z","scopus_import":"1","issue":"5","author":[{"first_name":"Susana","last_name":"Freitas","full_name":"Freitas, Susana"},{"last_name":"Westram","orcid":"0000-0003-1050-4969","first_name":"Anja M","full_name":"Westram, Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Schwander","first_name":"Tanja","full_name":"Schwander, Tanja"},{"last_name":"Arakelyan","first_name":"Marine","full_name":"Arakelyan, Marine"},{"full_name":"Ilgaz, Çetin","last_name":"Ilgaz","first_name":"Çetin"},{"full_name":"Kumlutas, Yusuf","last_name":"Kumlutas","first_name":"Yusuf"},{"full_name":"Harris, David James","last_name":"Harris","first_name":"David James"},{"last_name":"Carretero","first_name":"Miguel A.","full_name":"Carretero, Miguel A."},{"full_name":"Butlin, Roger K.","last_name":"Butlin","first_name":"Roger K."}],"abstract":[{"lang":"eng","text":"Hybridization is a common evolutionary process with multiple possible outcomes. In vertebrates, interspecific hybridization has repeatedly generated parthenogenetic hybrid species. However, it is unknown whether the generation of parthenogenetic hybrids is a rare outcome of frequent hybridization between sexual species within a genus or the typical outcome of rare hybridization events. Darevskia is a genus of rock lizards with both hybrid parthenogenetic and sexual species. Using capture sequencing, we estimate phylogenetic relationships and gene flow among the sexual species, to determine how introgressive hybridization relates to the origins of parthenogenetic hybrids. We find evidence for widespread hybridization with gene flow, both between recently diverged species and deep branches. Surprisingly, we find no signal of gene flow between parental species of the parthenogenetic hybrids, suggesting that the parental pairs were either reproductively or geographically isolated early in their divergence. The generation of parthenogenetic hybrids in Darevskia is, then, a rare outcome of the total occurrence of hybridization within the genus, but the typical outcome when specific species pairs hybridize. Our results question the conventional view that parthenogenetic lineages are generated by hybridization in a window of divergence. Instead, they suggest that some lineages possess specific properties that underpin successful parthenogenetic reproduction."}],"ec_funded":1,"type":"journal_article","date_updated":"2023-08-03T07:00:28Z","publication_status":"published","intvolume":"        76","language":[{"iso":"eng"}],"month":"05","ddc":["570"],"doi":"10.1111/evo.14462","year":"2022","oa_version":"Published Version","volume":76,"page":"899-914","article_type":"original","file":[{"file_size":2855214,"creator":"dernst","file_id":"11729","success":1,"file_name":"2022_Evolution_Freitas.pdf","content_type":"application/pdf","relation":"main_file","date_updated":"2022-08-05T06:19:28Z","date_created":"2022-08-05T06:19:28Z","checksum":"c27c025ae9afcf6c804d46a909775ee5","access_level":"open_access"}],"tmp":{"short":"CC BY-NC (4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode","name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","image":"/images/cc_by_nc.png"},"oa":1,"citation":{"chicago":"Freitas, Susana, Anja M Westram, Tanja Schwander, Marine Arakelyan, Çetin Ilgaz, Yusuf Kumlutas, David James Harris, Miguel A. Carretero, and Roger K. Butlin. “Parthenogenesis in Darevskia Lizards: A Rare Outcome of Common Hybridization, Not a Common Outcome of Rare Hybridization.” <i>Evolution</i>. Wiley, 2022. <a href=\"https://doi.org/10.1111/evo.14462\">https://doi.org/10.1111/evo.14462</a>.","ieee":"S. Freitas <i>et al.</i>, “Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization,” <i>Evolution</i>, vol. 76, no. 5. Wiley, pp. 899–914, 2022.","short":"S. Freitas, A.M. Westram, T. Schwander, M. Arakelyan, Ç. Ilgaz, Y. Kumlutas, D.J. Harris, M.A. Carretero, R.K. Butlin, Evolution 76 (2022) 899–914.","ista":"Freitas S, Westram AM, Schwander T, Arakelyan M, Ilgaz Ç, Kumlutas Y, Harris DJ, Carretero MA, Butlin RK. 2022. Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization. Evolution. 76(5), 899–914.","apa":"Freitas, S., Westram, A. M., Schwander, T., Arakelyan, M., Ilgaz, Ç., Kumlutas, Y., … Butlin, R. K. (2022). Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization. <i>Evolution</i>. Wiley. <a href=\"https://doi.org/10.1111/evo.14462\">https://doi.org/10.1111/evo.14462</a>","mla":"Freitas, Susana, et al. “Parthenogenesis in Darevskia Lizards: A Rare Outcome of Common Hybridization, Not a Common Outcome of Rare Hybridization.” <i>Evolution</i>, vol. 76, no. 5, Wiley, 2022, pp. 899–914, doi:<a href=\"https://doi.org/10.1111/evo.14462\">10.1111/evo.14462</a>.","ama":"Freitas S, Westram AM, Schwander T, et al. Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization. <i>Evolution</i>. 2022;76(5):899-914. doi:<a href=\"https://doi.org/10.1111/evo.14462\">10.1111/evo.14462</a>"},"day":"01","publication_identifier":{"eissn":["1558-5646"],"issn":["0014-3820"]},"isi":1,"quality_controlled":"1","publisher":"Wiley","file_date_updated":"2022-08-05T06:19:28Z","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","title":"Parthenogenesis in Darevskia lizards: A rare outcome of common hybridization, not a common outcome of rare hybridization","has_accepted_license":"1","status":"public","department":[{"_id":"NiBa"},{"_id":"BeVi"}],"article_processing_charge":"No","publication":"Evolution","project":[{"name":"Theoretical and empirical approaches to understanding Parallel Adaptation","_id":"265B41B8-B435-11E9-9278-68D0E5697425","call_identifier":"H2020","grant_number":"797747"}],"external_id":{"isi":["000781632500001"],"pmid":["35323995"]},"acknowledgement":"The authors thank A. van der Meijden and F. Ahmadzadeh for providing specimens and tissue samples, and A. Vardanyan, C. Corti, F. Jorge, and S. Drovetski for support during field work. The authors also thank S. Qiu for assistance with python scripting, S. Rocha for her support in BEAST analysis, and B. Wielstra for his comments on\r\na previous version of the manuscript. SF was funded by FCT grant SFRH/BD/81483/2011 (a PhD individual grant). AMW was funded by the European Union’s Horizon 2020 research and innovation programme under Marie Skłodowska-Curie grant agreement no. 797747. TS acknowledges funding from the Swiss National Science Foundation (grants\r\nPP00P3_170627 and 31003A_182495). The work was carried out under financial support of the projects “Preserving Armenian biodiversity: Joint Portuguese – Armenian program for training in modern conservation biology” of Gulbenkian Foundation (Portugal) and PTDC/BIABEC/101256/2008 of Fundação para a Ciência e a Tecnologia (FCT, Portugal)."},{"issue":"1856","abstract":[{"text":"Local adaptation leads to differences between populations within a species. In many systems, similar environmental contrasts occur repeatedly, sometimes driving parallel phenotypic evolution. Understanding the genomic basis of local adaptation and parallel evolution is a major goal of evolutionary genomics. It is now known that by preventing the break-up of favourable combinations of alleles across multiple loci, genetic architectures that reduce recombination, like chromosomal inversions, can make an important contribution to local adaptation. However, little is known about whether inversions also contribute disproportionately to parallel evolution. Our aim here is to highlight this knowledge gap, to showcase existing studies, and to illustrate the differences between genomic architectures with and without inversions using simple models. We predict that by generating stronger effective selection, inversions can sometimes speed up the parallel adaptive process or enable parallel adaptation where it would be impossible otherwise, but this is highly dependent on the spatial setting. We highlight that further empirical work is needed, in particular to cover a broader taxonomic range and to understand the relative importance of inversions compared to genomic regions without inversions.","lang":"eng"}],"author":[{"full_name":"Westram, Anja M","orcid":"0000-0003-1050-4969","last_name":"Westram","first_name":"Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Faria","first_name":"Rui","full_name":"Faria, Rui"},{"first_name":"Kerstin","last_name":"Johannesson","full_name":"Johannesson, Kerstin"},{"first_name":"Roger","last_name":"Butlin","full_name":"Butlin, Roger"},{"id":"4880FE40-F248-11E8-B48F-1D18A9856A87","first_name":"Nicholas H","orcid":"0000-0002-8548-5240","last_name":"Barton","full_name":"Barton, Nicholas H"}],"date_published":"2022-08-01T00:00:00Z","scopus_import":"1","_id":"11546","date_created":"2022-07-08T11:41:56Z","ddc":["570"],"doi":"10.1098/rstb.2021.0203","year":"2022","language":[{"iso":"eng"}],"month":"08","publication_status":"published","intvolume":"       377","keyword":["General Agricultural and Biological Sciences","General Biochemistry","Genetics and Molecular Biology"],"type":"journal_article","date_updated":"2023-08-03T11:55:42Z","publication_identifier":{"issn":["0962-8436"],"eissn":["1471-2970"]},"isi":1,"quality_controlled":"1","oa":1,"citation":{"mla":"Westram, Anja M., et al. “Inversions and Parallel Evolution.” <i>Philosophical Transactions of the Royal Society B: Biological Sciences</i>, vol. 377, no. 1856, 20210203, Royal Society of London, 2022, doi:<a href=\"https://doi.org/10.1098/rstb.2021.0203\">10.1098/rstb.2021.0203</a>.","ama":"Westram AM, Faria R, Johannesson K, Butlin R, Barton NH. Inversions and parallel evolution. <i>Philosophical Transactions of the Royal Society B: Biological Sciences</i>. 2022;377(1856). doi:<a href=\"https://doi.org/10.1098/rstb.2021.0203\">10.1098/rstb.2021.0203</a>","apa":"Westram, A. M., Faria, R., Johannesson, K., Butlin, R., &#38; Barton, N. H. (2022). Inversions and parallel evolution. <i>Philosophical Transactions of the Royal Society B: Biological Sciences</i>. Royal Society of London. <a href=\"https://doi.org/10.1098/rstb.2021.0203\">https://doi.org/10.1098/rstb.2021.0203</a>","ista":"Westram AM, Faria R, Johannesson K, Butlin R, Barton NH. 2022. Inversions and parallel evolution. Philosophical Transactions of the Royal Society B: Biological Sciences. 377(1856), 20210203.","short":"A.M. Westram, R. Faria, K. Johannesson, R. Butlin, N.H. Barton, Philosophical Transactions of the Royal Society B: Biological Sciences 377 (2022).","ieee":"A. M. Westram, R. Faria, K. Johannesson, R. Butlin, and N. H. Barton, “Inversions and parallel evolution,” <i>Philosophical Transactions of the Royal Society B: Biological Sciences</i>, vol. 377, no. 1856. Royal Society of London, 2022.","chicago":"Westram, Anja M, Rui Faria, Kerstin Johannesson, Roger Butlin, and Nicholas H Barton. “Inversions and Parallel Evolution.” <i>Philosophical Transactions of the Royal Society B: Biological Sciences</i>. Royal Society of London, 2022. <a href=\"https://doi.org/10.1098/rstb.2021.0203\">https://doi.org/10.1098/rstb.2021.0203</a>."},"article_number":"20210203","day":"01","tmp":{"image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)"},"oa_version":"Published Version","volume":377,"article_type":"original","file":[{"success":1,"creator":"dernst","file_id":"12479","relation":"main_file","content_type":"application/pdf","file_name":"2022_PhilosophicalTransactionsB_Westram.pdf","file_size":920304,"checksum":"49f69428f3dcf5ce3ff281f7d199e9df","access_level":"open_access","date_updated":"2023-02-02T08:20:29Z","date_created":"2023-02-02T08:20:29Z"}],"project":[{"grant_number":"P32166","_id":"05959E1C-7A3F-11EA-A408-12923DDC885E","name":"The maintenance of alternative adaptive peaks in snapdragons"}],"acknowledgement":"We thank the editor and two anonymous reviewers for their helpful and interesting comments on this manuscript.","external_id":{"isi":["000812317300005"]},"article_processing_charge":"Yes (via OA deal)","publication":"Philosophical Transactions of the Royal Society B: Biological Sciences","file_date_updated":"2023-02-02T08:20:29Z","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","has_accepted_license":"1","department":[{"_id":"BeVi"},{"_id":"NiBa"}],"title":"Inversions and parallel evolution","status":"public","publisher":"Royal Society of London"},{"ddc":["570"],"doi":"10.5061/DRYAD.M905QFV4B","year":"2022","article_processing_charge":"No","month":"07","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","department":[{"_id":"NiBa"}],"status":"public","title":"Data from: Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution","type":"research_data_reference","date_updated":"2023-08-04T09:42:10Z","publisher":"Dryad","author":[{"first_name":"Eva","last_name":"Koch","full_name":"Koch, Eva"},{"full_name":"Ravinet, Mark","first_name":"Mark","last_name":"Ravinet"},{"full_name":"Westram, Anja M","last_name":"Westram","orcid":"0000-0003-1050-4969","first_name":"Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Jonannesson, Kerstin","first_name":"Kerstin","last_name":"Jonannesson"},{"full_name":"Butlin, Roger","first_name":"Roger","last_name":"Butlin"}],"abstract":[{"text":"Chromosomal inversions have been shown to play a major role in local adaptation by suppressing recombination between alternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding the genetic architecture of adaptation requires better estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site-specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence.","lang":"eng"}],"related_material":{"record":[{"id":"12247","status":"public","relation":"used_in_publication"}]},"oa":1,"citation":{"chicago":"Koch, Eva, Mark Ravinet, Anja M Westram, Kerstin Jonannesson, and Roger Butlin. “Data from: Genetic Architecture of Repeated Phenotypic Divergence in Littorina Saxatilis Ecotype Evolution.” Dryad, 2022. <a href=\"https://doi.org/10.5061/DRYAD.M905QFV4B\">https://doi.org/10.5061/DRYAD.M905QFV4B</a>.","ieee":"E. Koch, M. Ravinet, A. M. Westram, K. Jonannesson, and R. Butlin, “Data from: Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution.” Dryad, 2022.","short":"E. Koch, M. Ravinet, A.M. Westram, K. Jonannesson, R. Butlin, (2022).","ista":"Koch E, Ravinet M, Westram AM, Jonannesson K, Butlin R. 2022. Data from: Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution, Dryad, <a href=\"https://doi.org/10.5061/DRYAD.M905QFV4B\">10.5061/DRYAD.M905QFV4B</a>.","apa":"Koch, E., Ravinet, M., Westram, A. M., Jonannesson, K., &#38; Butlin, R. (2022). Data from: Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution. Dryad. <a href=\"https://doi.org/10.5061/DRYAD.M905QFV4B\">https://doi.org/10.5061/DRYAD.M905QFV4B</a>","ama":"Koch E, Ravinet M, Westram AM, Jonannesson K, Butlin R. Data from: Genetic architecture of repeated phenotypic divergence in Littorina saxatilis ecotype evolution. 2022. doi:<a href=\"https://doi.org/10.5061/DRYAD.M905QFV4B\">10.5061/DRYAD.M905QFV4B</a>","mla":"Koch, Eva, et al. <i>Data from: Genetic Architecture of Repeated Phenotypic Divergence in Littorina Saxatilis Ecotype Evolution</i>. Dryad, 2022, doi:<a href=\"https://doi.org/10.5061/DRYAD.M905QFV4B\">10.5061/DRYAD.M905QFV4B</a>."},"day":"28","main_file_link":[{"open_access":"1","url":"https://doi.org/10.5061/dryad.m905qfv4b"}],"license":"https://creativecommons.org/publicdomain/zero/1.0/","date_published":"2022-07-28T00:00:00Z","tmp":{"short":"CC0 (1.0)","legal_code_url":"https://creativecommons.org/publicdomain/zero/1.0/legalcode","name":"Creative Commons Public Domain Dedication (CC0 1.0)","image":"/images/cc_0.png"},"oa_version":"Published Version","_id":"13066","date_created":"2023-05-23T16:33:12Z"},{"date_created":"2022-08-28T22:02:02Z","_id":"12001","date_published":"2022-10-01T00:00:00Z","scopus_import":"1","author":[{"full_name":"Hearn, Katherine E.","first_name":"Katherine E.","last_name":"Hearn"},{"full_name":"Koch, Eva L.","last_name":"Koch","first_name":"Eva L."},{"last_name":"Stankowski","first_name":"Sean","full_name":"Stankowski, Sean","id":"43161670-5719-11EA-8025-FABC3DDC885E"},{"last_name":"Butlin","first_name":"Roger K.","full_name":"Butlin, Roger K."},{"first_name":"Rui","last_name":"Faria","full_name":"Faria, Rui"},{"last_name":"Johannesson","first_name":"Kerstin","full_name":"Johannesson, Kerstin"},{"full_name":"Westram, Anja M","last_name":"Westram","orcid":"0000-0003-1050-4969","first_name":"Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"}],"abstract":[{"lang":"eng","text":"Sexual antagonism is a common hypothesis for driving the evolution of sex chromosomes, whereby recombination suppression is favored between sexually antagonistic loci and the sex-determining locus to maintain beneficial combinations of alleles. This results in the formation of a sex-determining region. Chromosomal inversions may contribute to recombination suppression but their precise role in sex chromosome evolution remains unclear. Because local adaptation is frequently facilitated through the suppression of recombination between adaptive loci by chromosomal inversions, there is potential for inversions that cover sex-determining regions to be involved in local adaptation as well, particularly if habitat variation creates environment-dependent sexual antagonism. With these processes in mind, we investigated sex determination in a well-studied example of local adaptation within a species: the intertidal snail, Littorina saxatilis. Using SNP data from a Swedish hybrid zone, we find novel evidence for a female-heterogametic sex determination system that is restricted to one ecotype. Our results suggest that four putative chromosomal inversions, two previously described and two newly discovered, span the putative sex chromosome pair. We determine their differing associations with sex, which suggest distinct strata of differing ages. The same inversions are found in the second ecotype but do not show any sex association. The striking disparity in inversion-sex associations between ecotypes that are connected by gene flow across a habitat transition that is just a few meters wide indicates a difference in selective regime that has produced a distinct barrier to the spread of the newly discovered sex-determining region between ecotypes. Such sex chromosome-environment interactions have not previously been uncovered in L. saxatilis and are known in few other organisms. A combination of both sex-specific selection and divergent natural selection is required to explain these highly unusual patterns."}],"issue":"5","type":"journal_article","date_updated":"2023-08-03T13:18:17Z","publication_status":"published","intvolume":"         6","month":"10","language":[{"iso":"eng"}],"doi":"10.1002/evl3.295","year":"2022","ddc":["570"],"file":[{"file_name":"2022_EvolutionLetters_Hearn.pdf","content_type":"application/pdf","relation":"main_file","file_id":"12686","creator":"dernst","success":1,"file_size":2368965,"access_level":"open_access","checksum":"2dcd06186a11b7d1be4cddc6b189f8fb","date_created":"2023-02-27T07:17:42Z","date_updated":"2023-02-27T07:17:42Z"}],"page":"358-374","volume":6,"oa_version":"Published Version","article_type":"original","tmp":{"image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)"},"day":"01","oa":1,"citation":{"short":"K.E. Hearn, E.L. Koch, S. Stankowski, R.K. Butlin, R. Faria, K. Johannesson, A.M. Westram, Evolution Letters 6 (2022) 358–374.","ieee":"K. E. Hearn <i>et al.</i>, “Differing associations between sex determination and sex-linked inversions in two ecotypes of Littorina saxatilis,” <i>Evolution Letters</i>, vol. 6, no. 5. Oxford Academic, pp. 358–374, 2022.","chicago":"Hearn, Katherine E., Eva L. Koch, Sean Stankowski, Roger K. Butlin, Rui Faria, Kerstin Johannesson, and Anja M Westram. “Differing Associations between Sex Determination and Sex-Linked Inversions in Two Ecotypes of Littorina Saxatilis.” <i>Evolution Letters</i>. Oxford Academic, 2022. <a href=\"https://doi.org/10.1002/evl3.295\">https://doi.org/10.1002/evl3.295</a>.","apa":"Hearn, K. E., Koch, E. L., Stankowski, S., Butlin, R. K., Faria, R., Johannesson, K., &#38; Westram, A. M. (2022). Differing associations between sex determination and sex-linked inversions in two ecotypes of Littorina saxatilis. <i>Evolution Letters</i>. Oxford Academic. <a href=\"https://doi.org/10.1002/evl3.295\">https://doi.org/10.1002/evl3.295</a>","ama":"Hearn KE, Koch EL, Stankowski S, et al. Differing associations between sex determination and sex-linked inversions in two ecotypes of Littorina saxatilis. <i>Evolution Letters</i>. 2022;6(5):358-374. doi:<a href=\"https://doi.org/10.1002/evl3.295\">10.1002/evl3.295</a>","mla":"Hearn, Katherine E., et al. “Differing Associations between Sex Determination and Sex-Linked Inversions in Two Ecotypes of Littorina Saxatilis.” <i>Evolution Letters</i>, vol. 6, no. 5, Oxford Academic, 2022, pp. 358–74, doi:<a href=\"https://doi.org/10.1002/evl3.295\">10.1002/evl3.295</a>.","ista":"Hearn KE, Koch EL, Stankowski S, Butlin RK, Faria R, Johannesson K, Westram AM. 2022. Differing associations between sex determination and sex-linked inversions in two ecotypes of Littorina saxatilis. Evolution Letters. 6(5), 358–374."},"isi":1,"quality_controlled":"1","publication_identifier":{"eissn":["2056-3744"]},"publisher":"Oxford Academic","title":"Differing associations between sex determination and sex-linked inversions in two ecotypes of Littorina saxatilis","status":"public","department":[{"_id":"NiBa"}],"has_accepted_license":"1","file_date_updated":"2023-02-27T07:17:42Z","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","publication":"Evolution Letters","article_processing_charge":"Yes","acknowledgement":"We thank A. Wright and four anonymous reviewers for valuable comments on an earlier draft of this manuscript and all members of the Littorina group for helpful discussions. This work was supported by a European Research Council grant to RKB and by a Natural Environment Research Council studentship to KEH through the ACCE doctoral training program. KJ acknowledges support from the Swedish Science Research Council VR (Vetenskaprådet) (2017-03798). RF was supported by an FCT CEEC (Fundação para a Ciênca e a Tecnologia, Concurso Estímulo ao Emprego Científico) contract (2020.00275.CEECIND).","external_id":{"isi":["000839621100001"]}},{"abstract":[{"text":"Kerstin Johannesson is a marine ecologist and evolutionary biologist based at the Tjärnö Marine Laboratory of the University of Gothenburg, which is situated in the beautiful Kosterhavet National Park on the Swedish west coast. Her work, using marine periwinkles (especially Littorina saxatilis and L. fabalis) as main model systems, has made a remarkable contribution to marine evolutionary biology and our understanding of local adaptation and its genetic underpinnings.","lang":"eng"}],"author":[{"full_name":"Westram, Anja M","first_name":"Anja M","orcid":"0000-0003-1050-4969","last_name":"Westram","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Butlin, Roger","last_name":"Butlin","first_name":"Roger"}],"issue":"1","date_created":"2023-01-12T12:10:28Z","_id":"12166","date_published":"2022-11-28T00:00:00Z","scopus_import":"1","month":"11","language":[{"iso":"eng"}],"doi":"10.1111/mec.16779","year":"2022","type":"journal_article","date_updated":"2023-08-04T09:09:15Z","publication_status":"published","intvolume":"        32","keyword":["Genetics","Ecology","Evolution","Behavior and Systematics"],"day":"28","oa":1,"citation":{"ista":"Westram AM, Butlin R. 2022. Professor Kerstin Johannesson–winner of the 2022 Molecular Ecology Prize. Molecular Ecology. 32(1), 26–29.","ama":"Westram AM, Butlin R. Professor Kerstin Johannesson–winner of the 2022 Molecular Ecology Prize. <i>Molecular Ecology</i>. 2022;32(1):26-29. doi:<a href=\"https://doi.org/10.1111/mec.16779\">10.1111/mec.16779</a>","mla":"Westram, Anja M., and Roger Butlin. “Professor Kerstin Johannesson–Winner of the 2022 Molecular Ecology Prize.” <i>Molecular Ecology</i>, vol. 32, no. 1, Wiley, 2022, pp. 26–29, doi:<a href=\"https://doi.org/10.1111/mec.16779\">10.1111/mec.16779</a>.","apa":"Westram, A. M., &#38; Butlin, R. (2022). Professor Kerstin Johannesson–winner of the 2022 Molecular Ecology Prize. <i>Molecular Ecology</i>. Wiley. <a href=\"https://doi.org/10.1111/mec.16779\">https://doi.org/10.1111/mec.16779</a>","chicago":"Westram, Anja M, and Roger Butlin. “Professor Kerstin Johannesson–Winner of the 2022 Molecular Ecology Prize.” <i>Molecular Ecology</i>. Wiley, 2022. <a href=\"https://doi.org/10.1111/mec.16779\">https://doi.org/10.1111/mec.16779</a>.","ieee":"A. M. Westram and R. Butlin, “Professor Kerstin Johannesson–winner of the 2022 Molecular Ecology Prize,” <i>Molecular Ecology</i>, vol. 32, no. 1. Wiley, pp. 26–29, 2022.","short":"A.M. Westram, R. Butlin, Molecular Ecology 32 (2022) 26–29."},"isi":1,"quality_controlled":"1","publication_identifier":{"eissn":["1365-294X"],"issn":["0962-1083"]},"oa_version":"Published Version","page":"26-29","volume":32,"article_type":"letter_note","main_file_link":[{"url":"https://doi.org/10.1111/mec.16779","open_access":"1"}],"publication":"Molecular Ecology","article_processing_charge":"No","external_id":{"isi":["000892168800001"]},"publisher":"Wiley","department":[{"_id":"NiBa"}],"status":"public","title":"Professor Kerstin Johannesson–winner of the 2022 Molecular Ecology Prize","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8"},{"article_processing_charge":"No","publication":"Evolution","external_id":{"pmid":["35994296"],"isi":["000848449100001"]},"acknowledgement":"We thank everyone who helped with fieldwork, snail processing, and DNA extractions, particularly Laura Brettell, Mårten Duvetorp, Juan Galindo, Anne-Lise Liabot, Irena Senčić, and Zuzanna Zagrodzka. We also thank Rui Faria and Jenny Larsson for their contributions, with inversions and shell shape respectively. KJ was funded by the Swedish research council Vetenskapsrådet, grant number 2017-03798. R.K.B. and E.K. were funded by the European Research Council (ERC-2015-AdG-693030-BARRIERS). R.K.B. was also funded by the Natural Environment Research Council and the Swedish Research Council Vetenskapsrådet.","publisher":"Wiley","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","file_date_updated":"2023-01-30T08:45:35Z","has_accepted_license":"1","department":[{"_id":"NiBa"}],"title":"Genetic architecture of repeated phenotypic divergence in Littorina saxatilis evolution","status":"public","citation":{"ista":"Koch EL, Ravinet M, Westram AM, Johannesson K, Butlin RK. 2022. Genetic architecture of repeated phenotypic divergence in Littorina saxatilis evolution. Evolution. 76(10), 2332–2346.","ama":"Koch EL, Ravinet M, Westram AM, Johannesson K, Butlin RK. Genetic architecture of repeated phenotypic divergence in Littorina saxatilis evolution. <i>Evolution</i>. 2022;76(10):2332-2346. doi:<a href=\"https://doi.org/10.1111/evo.14602\">10.1111/evo.14602</a>","mla":"Koch, Eva L., et al. “Genetic Architecture of Repeated Phenotypic Divergence in Littorina Saxatilis Evolution.” <i>Evolution</i>, vol. 76, no. 10, Wiley, 2022, pp. 2332–46, doi:<a href=\"https://doi.org/10.1111/evo.14602\">10.1111/evo.14602</a>.","apa":"Koch, E. L., Ravinet, M., Westram, A. M., Johannesson, K., &#38; Butlin, R. K. (2022). Genetic architecture of repeated phenotypic divergence in Littorina saxatilis evolution. <i>Evolution</i>. Wiley. <a href=\"https://doi.org/10.1111/evo.14602\">https://doi.org/10.1111/evo.14602</a>","chicago":"Koch, Eva L., Mark Ravinet, Anja M Westram, Kerstin Johannesson, and Roger K. Butlin. “Genetic Architecture of Repeated Phenotypic Divergence in Littorina Saxatilis Evolution.” <i>Evolution</i>. Wiley, 2022. <a href=\"https://doi.org/10.1111/evo.14602\">https://doi.org/10.1111/evo.14602</a>.","ieee":"E. L. Koch, M. Ravinet, A. M. Westram, K. Johannesson, and R. K. Butlin, “Genetic architecture of repeated phenotypic divergence in Littorina saxatilis evolution,” <i>Evolution</i>, vol. 76, no. 10. Wiley, pp. 2332–2346, 2022.","short":"E.L. Koch, M. Ravinet, A.M. Westram, K. Johannesson, R.K. Butlin, Evolution 76 (2022) 2332–2346."},"oa":1,"day":"01","publication_identifier":{"issn":["0014-3820"],"eissn":["1558-5646"]},"quality_controlled":"1","isi":1,"article_type":"original","volume":76,"page":"2332-2346","oa_version":"Published Version","file":[{"file_id":"12439","creator":"dernst","success":1,"file_name":"2022_Evolution_Koch.pdf","content_type":"application/pdf","relation":"main_file","file_size":2990581,"checksum":"defd8a4bea61cf00a3c88d4a30e2728c","access_level":"open_access","date_updated":"2023-01-30T08:45:35Z","date_created":"2023-01-30T08:45:35Z"}],"tmp":{"image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)"},"language":[{"iso":"eng"}],"month":"10","ddc":["570"],"year":"2022","doi":"10.1111/evo.14602","date_updated":"2023-08-04T09:42:11Z","type":"journal_article","intvolume":"        76","keyword":["General Agricultural and Biological Sciences","Genetics","Ecology","Evolution","Behavior and Systematics"],"publication_status":"published","related_material":{"record":[{"id":"13066","status":"public","relation":"research_data"}]},"issue":"10","abstract":[{"lang":"eng","text":"Chromosomal inversions have been shown to play a major role in a local adaptation by suppressing recombination between alternative arrangements and maintaining beneficial allele combinations. However, so far, their importance relative to the remaining genome remains largely unknown. Understanding the genetic architecture of adaptation requires better estimates of how loci of different effect sizes contribute to phenotypic variation. Here, we used three Swedish islands where the marine snail Littorina saxatilis has repeatedly evolved into two distinct ecotypes along a habitat transition. We estimated the contribution of inversion polymorphisms to phenotypic divergence while controlling for polygenic effects in the remaining genome using a quantitative genetics framework. We confirmed the importance of inversions but showed that contributions of loci outside inversions are of similar magnitude, with variable proportions dependent on the trait and the population. Some inversions showed consistent effects across all sites, whereas others exhibited site-specific effects, indicating that the genomic basis for replicated phenotypic divergence is only partly shared. The contributions of sexual dimorphism as well as environmental factors to phenotypic variation were significant but minor compared to inversions and polygenic background. Overall, this integrated approach provides insight into the multiple mechanisms contributing to parallel phenotypic divergence."}],"author":[{"full_name":"Koch, Eva L.","last_name":"Koch","first_name":"Eva L."},{"full_name":"Ravinet, Mark","last_name":"Ravinet","first_name":"Mark"},{"orcid":"0000-0003-1050-4969","last_name":"Westram","first_name":"Anja M","full_name":"Westram, Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Johannesson, Kerstin","first_name":"Kerstin","last_name":"Johannesson"},{"full_name":"Butlin, Roger K.","first_name":"Roger K.","last_name":"Butlin"}],"_id":"12247","date_created":"2023-01-16T09:54:15Z","pmid":1,"scopus_import":"1","date_published":"2022-10-01T00:00:00Z"},{"type":"journal_article","date_updated":"2023-08-04T09:53:40Z","publication_status":"published","intvolume":"        35","keyword":["Ecology","Evolution","Behavior and Systematics"],"month":"09","language":[{"iso":"eng"}],"doi":"10.1111/jeb.14005","year":"2022","ddc":["570"],"date_created":"2023-01-16T09:59:24Z","_id":"12264","date_published":"2022-09-01T00:00:00Z","scopus_import":"1","pmid":1,"related_material":{"record":[{"status":"public","relation":"other","id":"12265"}]},"abstract":[{"lang":"eng","text":"Reproductive isolation (RI) is a core concept in evolutionary biology. It has been the central focus of speciation research since the modern synthesis and is the basis by which biological species are defined. Despite this, the term is used in seemingly different ways, and attempts to quantify RI have used very different approaches. After showing that the field lacks a clear definition of the term, we attempt to clarify key issues, including what RI is, how it can be quantified in principle, and how it can be measured in practice. Following other definitions with a genetic focus, we propose that RI is a quantitative measure of the effect that genetic differences between populations have on gene flow. Specifically, RI compares the flow of neutral alleles in the presence of these genetic differences to the flow without any such differences. RI is thus greater than zero when genetic differences between populations reduce the flow of neutral alleles between populations. We show how RI can be quantified in a range of scenarios. A key conclusion is that RI depends strongly on circumstances—including the spatial, temporal and genomic context—making it difficult to compare across systems. After reviewing methods for estimating RI from data, we conclude that it is difficult to measure in practice. We discuss our findings in light of the goals of speciation research and encourage the use of methods for estimating RI that integrate organismal and genetic approaches."}],"author":[{"id":"3C147470-F248-11E8-B48F-1D18A9856A87","full_name":"Westram, Anja M","first_name":"Anja M","last_name":"Westram","orcid":"0000-0003-1050-4969"},{"id":"43161670-5719-11EA-8025-FABC3DDC885E","full_name":"Stankowski, Sean","last_name":"Stankowski","first_name":"Sean"},{"id":"455235B8-F248-11E8-B48F-1D18A9856A87","full_name":"Surendranadh, Parvathy","last_name":"Surendranadh","first_name":"Parvathy"},{"id":"4880FE40-F248-11E8-B48F-1D18A9856A87","full_name":"Barton, Nicholas H","first_name":"Nicholas H","last_name":"Barton","orcid":"0000-0002-8548-5240"}],"issue":"9","publisher":"Wiley","title":"What is reproductive isolation?","status":"public","department":[{"_id":"NiBa"}],"has_accepted_license":"1","file_date_updated":"2023-01-30T10:05:31Z","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","publication":"Journal of Evolutionary Biology","article_processing_charge":"Yes (via OA deal)","acknowledgement":"We are grateful to the participants of the ESEB satellite symposium ‘Understanding reproductive isolation: bridging conceptual barriers in  speciation  research’  in  2021  for  the  interesting  discussions  that  helped  us  clarify  the  thoughts  presented  in  this  article.  We  thank  Roger Butlin, Michael Turelli and two anonymous reviewers for their thoughtful comments on this manuscript. We are also very grateful to Roger Butlin and the Barton Group for the continued conversa-tions about RI. In addition, we thank all participants of the speciation survey. Part of this work was funded by the Austrian Science Fund FWF (grant P 32166)","external_id":{"isi":["000849851100002"],"pmid":["36063156"]},"project":[{"name":"The maintenance of alternative adaptive peaks in snapdragons","_id":"05959E1C-7A3F-11EA-A408-12923DDC885E","grant_number":"P32166"}],"file":[{"file_size":3146793,"file_name":"2022_JourEvoBiology_Westram.pdf","content_type":"application/pdf","relation":"main_file","file_id":"12448","creator":"dernst","success":1,"date_created":"2023-01-30T10:05:31Z","date_updated":"2023-01-30T10:05:31Z","checksum":"f08de57112330a7ee88d2e1b20576a1e","access_level":"open_access"}],"page":"1143-1164","volume":35,"oa_version":"Published Version","article_type":"review","tmp":{"image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)"},"day":"01","oa":1,"citation":{"ama":"Westram AM, Stankowski S, Surendranadh P, Barton NH. What is reproductive isolation? <i>Journal of Evolutionary Biology</i>. 2022;35(9):1143-1164. doi:<a href=\"https://doi.org/10.1111/jeb.14005\">10.1111/jeb.14005</a>","mla":"Westram, Anja M., et al. “What Is Reproductive Isolation?” <i>Journal of Evolutionary Biology</i>, vol. 35, no. 9, Wiley, 2022, pp. 1143–64, doi:<a href=\"https://doi.org/10.1111/jeb.14005\">10.1111/jeb.14005</a>.","apa":"Westram, A. M., Stankowski, S., Surendranadh, P., &#38; Barton, N. H. (2022). What is reproductive isolation? <i>Journal of Evolutionary Biology</i>. Wiley. <a href=\"https://doi.org/10.1111/jeb.14005\">https://doi.org/10.1111/jeb.14005</a>","ista":"Westram AM, Stankowski S, Surendranadh P, Barton NH. 2022. What is reproductive isolation? Journal of Evolutionary Biology. 35(9), 1143–1164.","short":"A.M. Westram, S. Stankowski, P. Surendranadh, N.H. Barton, Journal of Evolutionary Biology 35 (2022) 1143–1164.","chicago":"Westram, Anja M, Sean Stankowski, Parvathy Surendranadh, and Nicholas H Barton. “What Is Reproductive Isolation?” <i>Journal of Evolutionary Biology</i>. Wiley, 2022. <a href=\"https://doi.org/10.1111/jeb.14005\">https://doi.org/10.1111/jeb.14005</a>.","ieee":"A. M. Westram, S. Stankowski, P. Surendranadh, and N. H. Barton, “What is reproductive isolation?,” <i>Journal of Evolutionary Biology</i>, vol. 35, no. 9. Wiley, pp. 1143–1164, 2022."},"isi":1,"quality_controlled":"1","publication_identifier":{"eissn":["1420-9101"],"issn":["1010-061X"]}},{"project":[{"name":"The maintenance of alternative adaptive peaks in snapdragons","_id":"05959E1C-7A3F-11EA-A408-12923DDC885E","grant_number":"P32166"}],"acknowledgement":"We  are  very  grateful  to  the  authors  of  the  commentaries  for  the  interesting discussion and to Luke Holman for handling this set of manuscripts. Part of this work was funded by the Austrian Science Fund FWF (grant P 32166).","external_id":{"isi":["000849851100009"]},"article_processing_charge":"Yes (via OA deal)","publication":"Journal of Evolutionary Biology","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","file_date_updated":"2023-01-30T10:14:09Z","title":"Reproductive isolation, speciation, and the value of disagreement: A reply to the commentaries on ‘What is reproductive isolation?’","has_accepted_license":"1","status":"public","department":[{"_id":"NiBa"}],"publisher":"Wiley","publication_identifier":{"issn":["1010-061X"],"eissn":["1420-9101"]},"quality_controlled":"1","isi":1,"citation":{"chicago":"Westram, Anja M, Sean Stankowski, Parvathy Surendranadh, and Nicholas H Barton. “Reproductive Isolation, Speciation, and the Value of Disagreement: A Reply to the Commentaries on ‘What Is Reproductive Isolation?’” <i>Journal of Evolutionary Biology</i>. Wiley, 2022. <a href=\"https://doi.org/10.1111/jeb.14082\">https://doi.org/10.1111/jeb.14082</a>.","ieee":"A. M. Westram, S. Stankowski, P. Surendranadh, and N. H. Barton, “Reproductive isolation, speciation, and the value of disagreement: A reply to the commentaries on ‘What is reproductive isolation?,’” <i>Journal of Evolutionary Biology</i>, vol. 35, no. 9. Wiley, pp. 1200–1205, 2022.","short":"A.M. Westram, S. Stankowski, P. Surendranadh, N.H. Barton, Journal of Evolutionary Biology 35 (2022) 1200–1205.","ista":"Westram AM, Stankowski S, Surendranadh P, Barton NH. 2022. Reproductive isolation, speciation, and the value of disagreement: A reply to the commentaries on ‘What is reproductive isolation?’ Journal of Evolutionary Biology. 35(9), 1200–1205.","apa":"Westram, A. M., Stankowski, S., Surendranadh, P., &#38; Barton, N. H. (2022). Reproductive isolation, speciation, and the value of disagreement: A reply to the commentaries on ‘What is reproductive isolation?’ <i>Journal of Evolutionary Biology</i>. Wiley. <a href=\"https://doi.org/10.1111/jeb.14082\">https://doi.org/10.1111/jeb.14082</a>","mla":"Westram, Anja M., et al. “Reproductive Isolation, Speciation, and the Value of Disagreement: A Reply to the Commentaries on ‘What Is Reproductive Isolation?’” <i>Journal of Evolutionary Biology</i>, vol. 35, no. 9, Wiley, 2022, pp. 1200–05, doi:<a href=\"https://doi.org/10.1111/jeb.14082\">10.1111/jeb.14082</a>.","ama":"Westram AM, Stankowski S, Surendranadh P, Barton NH. Reproductive isolation, speciation, and the value of disagreement: A reply to the commentaries on ‘What is reproductive isolation?’ <i>Journal of Evolutionary Biology</i>. 2022;35(9):1200-1205. doi:<a href=\"https://doi.org/10.1111/jeb.14082\">10.1111/jeb.14082</a>"},"oa":1,"day":"01","tmp":{"image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)"},"article_type":"letter_note","page":"1200-1205","oa_version":"Published Version","volume":35,"file":[{"checksum":"27268009e5eec030bc10667a4ac5ed4c","access_level":"open_access","date_created":"2023-01-30T10:14:09Z","date_updated":"2023-01-30T10:14:09Z","file_name":"2022_JourEvoBiology_Westram_Response.pdf","relation":"main_file","content_type":"application/pdf","creator":"dernst","file_id":"12449","success":1,"file_size":349603}],"ddc":["570"],"year":"2022","doi":"10.1111/jeb.14082","language":[{"iso":"eng"}],"month":"09","intvolume":"        35","keyword":["Ecology","Evolution","Behavior and Systematics"],"publication_status":"published","date_updated":"2023-08-04T09:53:41Z","type":"journal_article","issue":"9","author":[{"full_name":"Westram, Anja M","last_name":"Westram","orcid":"0000-0003-1050-4969","first_name":"Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Stankowski","first_name":"Sean","full_name":"Stankowski, Sean","id":"43161670-5719-11EA-8025-FABC3DDC885E"},{"id":"455235B8-F248-11E8-B48F-1D18A9856A87","full_name":"Surendranadh, Parvathy","last_name":"Surendranadh","first_name":"Parvathy"},{"full_name":"Barton, Nicholas H","first_name":"Nicholas H","orcid":"0000-0002-8548-5240","last_name":"Barton","id":"4880FE40-F248-11E8-B48F-1D18A9856A87"}],"related_material":{"record":[{"relation":"other","status":"public","id":"12264"}]},"scopus_import":"1","date_published":"2022-09-01T00:00:00Z","_id":"12265","date_created":"2023-01-16T09:59:37Z"},{"doi":"10.1111/mec.15861","year":"2021","ddc":["570"],"month":"08","language":[{"iso":"eng"}],"publication_status":"published","intvolume":"        30","keyword":["Genetics","Ecology","Evolution","Behavior and Systematics"],"type":"journal_article","date_updated":"2023-09-05T16:02:19Z","author":[{"last_name":"Westram","orcid":"0000-0003-1050-4969","first_name":"Anja M","full_name":"Westram, Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Faria, Rui","first_name":"Rui","last_name":"Faria"},{"full_name":"Johannesson, Kerstin","first_name":"Kerstin","last_name":"Johannesson"},{"full_name":"Butlin, Roger","last_name":"Butlin","first_name":"Roger"}],"abstract":[{"lang":"eng","text":"Combining hybrid zone analysis with genomic data is a promising approach to understanding the genomic basis of adaptive divergence. It allows for the identification of genomic regions underlying barriers to gene flow. It also provides insights into spatial patterns of allele frequency change, informing about the interplay between environmental factors, dispersal and selection. However, when only a single hybrid zone is analysed, it is difficult to separate patterns generated by selection from those resulting from chance. Therefore, it is beneficial to look for repeatable patterns across replicate hybrid zones in the same system. We applied this approach to the marine snail Littorina saxatilis, which contains two ecotypes, adapted to wave-exposed rocks vs. high-predation boulder fields. The existence of numerous hybrid zones between ecotypes offered the opportunity to test for the repeatability of genomic architectures and spatial patterns of divergence. We sampled and phenotyped snails from seven replicate hybrid zones on the Swedish west coast and genotyped them for thousands of single nucleotide polymorphisms. Shell shape and size showed parallel clines across all zones. Many genomic regions showing steep clines and/or high differentiation were shared among hybrid zones, consistent with a common evolutionary history and extensive gene flow between zones, and supporting the importance of these regions for divergence. In particular, we found that several large putative inversions contribute to divergence in all locations. Additionally, we found evidence for consistent displacement of clines from the boulder–rock transition. Our results demonstrate patterns of spatial variation that would not be accessible without continuous spatial sampling, a large genomic data set and replicate hybrid zones."}],"issue":"15","date_published":"2021-08-01T00:00:00Z","scopus_import":"1","pmid":1,"date_created":"2022-03-08T11:28:32Z","_id":"10838","external_id":{"pmid":["33638231"],"isi":["000669439700001"]},"acknowledgement":"We thank everyone who helped with fieldwork, snail processing and DNA extractions, particularly Laura Brettell, Mårten Duvetorp, Juan Galindo, Anne-Lise Liabot, Mark Ravinet, Irena Senčić and Zuzanna Zagrodzka. We are also grateful to Edinburgh Genomics for library preparation and sequencing, to Stuart Baird and Mark Ravinet for helpful discussions, and to three anonymous reviewers for their constructive comments. This work was supported by the Natural Environment Research Council (NE/K014021/1), the European Research Council (AdG-693030-BARRIERS), Swedish Research Councils Formas and Vetenskapsrådet through a Linnaeus grant to the Centre for Marine Evolutionary Biology (217-2008-1719), the European Regional Development Fund (POCI-01-0145-FEDER-030628), and the Fundação para a iência e a Tecnologia,\r\nPortugal (PTDC/BIA-EVL/\r\n30628/2017). A.M.W. and R.F. were\r\nfunded by the European Union’s Horizon 2020 research and innovation\r\nprogramme under Marie Skłodowska-Curie\r\ngrant agreements\r\nno. 754411/797747 and no. 706376, respectively.","publication":"Molecular Ecology","article_processing_charge":"No","has_accepted_license":"1","department":[{"_id":"BeVi"}],"status":"public","title":"Using replicate hybrid zones to understand the genomic basis of adaptive divergence","file_date_updated":"2022-03-08T11:31:30Z","user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","publisher":"Wiley","isi":1,"quality_controlled":"1","publication_identifier":{"issn":["0962-1083"],"eissn":["1365-294X"]},"day":"01","oa":1,"citation":{"ama":"Westram AM, Faria R, Johannesson K, Butlin R. Using replicate hybrid zones to understand the genomic basis of adaptive divergence. <i>Molecular Ecology</i>. 2021;30(15):3797-3814. doi:<a href=\"https://doi.org/10.1111/mec.15861\">10.1111/mec.15861</a>","mla":"Westram, Anja M., et al. “Using Replicate Hybrid Zones to Understand the Genomic Basis of Adaptive Divergence.” <i>Molecular Ecology</i>, vol. 30, no. 15, Wiley, 2021, pp. 3797–814, doi:<a href=\"https://doi.org/10.1111/mec.15861\">10.1111/mec.15861</a>.","apa":"Westram, A. M., Faria, R., Johannesson, K., &#38; Butlin, R. (2021). Using replicate hybrid zones to understand the genomic basis of adaptive divergence. <i>Molecular Ecology</i>. Wiley. <a href=\"https://doi.org/10.1111/mec.15861\">https://doi.org/10.1111/mec.15861</a>","ista":"Westram AM, Faria R, Johannesson K, Butlin R. 2021. Using replicate hybrid zones to understand the genomic basis of adaptive divergence. Molecular Ecology. 30(15), 3797–3814.","short":"A.M. Westram, R. Faria, K. Johannesson, R. Butlin, Molecular Ecology 30 (2021) 3797–3814.","ieee":"A. M. Westram, R. Faria, K. Johannesson, and R. Butlin, “Using replicate hybrid zones to understand the genomic basis of adaptive divergence,” <i>Molecular Ecology</i>, vol. 30, no. 15. Wiley, pp. 3797–3814, 2021.","chicago":"Westram, Anja M, Rui Faria, Kerstin Johannesson, and Roger Butlin. “Using Replicate Hybrid Zones to Understand the Genomic Basis of Adaptive Divergence.” <i>Molecular Ecology</i>. Wiley, 2021. <a href=\"https://doi.org/10.1111/mec.15861\">https://doi.org/10.1111/mec.15861</a>."},"tmp":{"image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)"},"file":[{"file_size":1726548,"creator":"dernst","file_id":"10839","success":1,"file_name":"2021_MolecularEcology_Westram.pdf","relation":"main_file","content_type":"application/pdf","date_updated":"2022-03-08T11:31:30Z","date_created":"2022-03-08T11:31:30Z","access_level":"open_access","checksum":"d5611f243ceb63a0e091d6662ebd9cda"}],"volume":30,"page":"3797-3814","oa_version":"Published Version","article_type":"original"},{"volume":2,"oa_version":"None","_id":"14984","date_created":"2024-02-14T12:05:50Z","series_title":"eLS","date_published":"2021-05-28T00:00:00Z","citation":{"ieee":"S. Stankowski, D. Shipilina, and A. M. Westram, “Hybrid Zones,” in <i>Encyclopedia of Life Sciences</i>, vol. 2, Wiley, 2021.","chicago":"Stankowski, Sean, Daria Shipilina, and Anja M Westram. “Hybrid Zones.” In <i>Encyclopedia of Life Sciences</i>, Vol. 2. ELS. Wiley, 2021. <a href=\"https://doi.org/10.1002/9780470015902.a0029355\">https://doi.org/10.1002/9780470015902.a0029355</a>.","short":"S. Stankowski, D. Shipilina, A.M. Westram, in:, Encyclopedia of Life Sciences, Wiley, 2021.","ista":"Stankowski S, Shipilina D, Westram AM. 2021.Hybrid Zones. In: Encyclopedia of Life Sciences. vol. 2.","mla":"Stankowski, Sean, et al. “Hybrid Zones.” <i>Encyclopedia of Life Sciences</i>, vol. 2, Wiley, 2021, doi:<a href=\"https://doi.org/10.1002/9780470015902.a0029355\">10.1002/9780470015902.a0029355</a>.","ama":"Stankowski S, Shipilina D, Westram AM. Hybrid Zones. In: <i>Encyclopedia of Life Sciences</i>. Vol 2. eLS. Wiley; 2021. doi:<a href=\"https://doi.org/10.1002/9780470015902.a0029355\">10.1002/9780470015902.a0029355</a>","apa":"Stankowski, S., Shipilina, D., &#38; Westram, A. M. (2021). Hybrid Zones. In <i>Encyclopedia of Life Sciences</i> (Vol. 2). Wiley. <a href=\"https://doi.org/10.1002/9780470015902.a0029355\">https://doi.org/10.1002/9780470015902.a0029355</a>"},"day":"28","publication_identifier":{"isbn":["9780470016176"],"eisbn":["9780470015902"]},"quality_controlled":"1","abstract":[{"lang":"eng","text":"Hybrid zones are narrow geographic regions where different populations, races or interbreeding species meet and mate, producing mixed ‘hybrid’ offspring. They are relatively common and can be found in a diverse range of organisms and environments. The study of hybrid zones has played an important role in our understanding of the origin of species, with hybrid zones having been described as ‘natural laboratories’. This is because they allow us to study,in situ, the conditions and evolutionary forces that enable divergent taxa to remain distinct despite some ongoing gene exchange between them."}],"author":[{"id":"43161670-5719-11EA-8025-FABC3DDC885E","full_name":"Stankowski, Sean","first_name":"Sean","last_name":"Stankowski"},{"id":"428A94B0-F248-11E8-B48F-1D18A9856A87","full_name":"Shipilina, Daria","first_name":"Daria","orcid":"0000-0002-1145-9226","last_name":"Shipilina"},{"id":"3C147470-F248-11E8-B48F-1D18A9856A87","orcid":"0000-0003-1050-4969","last_name":"Westram","first_name":"Anja M","full_name":"Westram, Anja M"}],"type":"book_chapter","date_updated":"2024-02-19T09:54:18Z","publisher":"Wiley","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","publication_status":"published","title":"Hybrid Zones","intvolume":"         2","department":[{"_id":"NiBa"}],"status":"public","language":[{"iso":"eng"}],"article_processing_charge":"No","month":"05","publication":"Encyclopedia of Life Sciences","doi":"10.1002/9780470015902.a0029355","year":"2021"},{"issue":"3","author":[{"full_name":"Koch, Eva L.","last_name":"Koch","first_name":"Eva L."},{"first_name":"Hernán E.","last_name":"Morales","full_name":"Morales, Hernán E."},{"full_name":"Larsson, Jenny","first_name":"Jenny","last_name":"Larsson"},{"id":"3C147470-F248-11E8-B48F-1D18A9856A87","full_name":"Westram, Anja M","orcid":"0000-0003-1050-4969","last_name":"Westram","first_name":"Anja M"},{"full_name":"Faria, Rui","last_name":"Faria","first_name":"Rui"},{"last_name":"Lemmon","first_name":"Alan R.","full_name":"Lemmon, Alan R."},{"full_name":"Lemmon, E. Moriarty","first_name":"E. Moriarty","last_name":"Lemmon"},{"first_name":"Kerstin","last_name":"Johannesson","full_name":"Johannesson, Kerstin"},{"full_name":"Butlin, Roger K.","first_name":"Roger K.","last_name":"Butlin"}],"ec_funded":1,"abstract":[{"lang":"eng","text":"Chromosomal inversions have long been recognized for their role in local adaptation. By suppressing recombination in heterozygous individuals, they can maintain coadapted gene complexes and protect them from homogenizing effects of gene flow. However, to fully understand their importance for local adaptation we need to know their influence on phenotypes under divergent selection. For this, the marine snail Littorina saxatilis provides an ideal study system. Divergent ecotypes adapted to wave action and crab predation occur in close proximity on intertidal shores with gene flow between them. Here, we used F2 individuals obtained from crosses between the ecotypes to test for associations between genomic regions and traits distinguishing the Crab‐/Wave‐adapted ecotypes including size, shape, shell thickness, and behavior. We show that most of these traits are influenced by two previously detected inversion regions that are divergent between ecotypes. We thus gain a better understanding of one important underlying mechanism responsible for the rapid and repeated formation of ecotypes: divergent selection acting on inversions. We also found that some inversions contributed to more than one trait suggesting that they may contain several loci involved in adaptation, consistent with the hypothesis that suppression of recombination within inversions facilitates differentiation in the presence of gene flow."}],"related_material":{"record":[{"id":"12987","relation":"research_data","status":"public"}]},"scopus_import":"1","date_published":"2021-05-07T00:00:00Z","_id":"9394","date_created":"2021-05-16T22:01:47Z","ddc":["570"],"year":"2021","doi":"10.1002/evl3.227","language":[{"iso":"eng"}],"month":"05","intvolume":"         5","publication_status":"published","date_updated":"2023-08-08T13:34:08Z","type":"journal_article","publication_identifier":{"eissn":["2056-3744"]},"quality_controlled":"1","isi":1,"citation":{"ista":"Koch EL, Morales HE, Larsson J, Westram AM, Faria R, Lemmon AR, Lemmon EM, Johannesson K, Butlin RK. 2021. Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis. Evolution Letters. 5(3), 196–213.","ama":"Koch EL, Morales HE, Larsson J, et al. Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis. <i>Evolution Letters</i>. 2021;5(3):196-213. doi:<a href=\"https://doi.org/10.1002/evl3.227\">10.1002/evl3.227</a>","mla":"Koch, Eva L., et al. “Genetic Variation for Adaptive Traits Is Associated with Polymorphic Inversions in Littorina Saxatilis.” <i>Evolution Letters</i>, vol. 5, no. 3, Wiley, 2021, pp. 196–213, doi:<a href=\"https://doi.org/10.1002/evl3.227\">10.1002/evl3.227</a>.","apa":"Koch, E. L., Morales, H. E., Larsson, J., Westram, A. M., Faria, R., Lemmon, A. R., … Butlin, R. K. (2021). Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis. <i>Evolution Letters</i>. Wiley. <a href=\"https://doi.org/10.1002/evl3.227\">https://doi.org/10.1002/evl3.227</a>","chicago":"Koch, Eva L., Hernán E. Morales, Jenny Larsson, Anja M Westram, Rui Faria, Alan R. Lemmon, E. Moriarty Lemmon, Kerstin Johannesson, and Roger K. Butlin. “Genetic Variation for Adaptive Traits Is Associated with Polymorphic Inversions in Littorina Saxatilis.” <i>Evolution Letters</i>. Wiley, 2021. <a href=\"https://doi.org/10.1002/evl3.227\">https://doi.org/10.1002/evl3.227</a>.","ieee":"E. L. Koch <i>et al.</i>, “Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis,” <i>Evolution Letters</i>, vol. 5, no. 3. Wiley, pp. 196–213, 2021.","short":"E.L. Koch, H.E. Morales, J. Larsson, A.M. Westram, R. Faria, A.R. Lemmon, E.M. Lemmon, K. Johannesson, R.K. Butlin, Evolution Letters 5 (2021) 196–213."},"oa":1,"day":"07","tmp":{"image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)"},"article_type":"original","page":"196-213","volume":5,"oa_version":"Published Version","file":[{"file_size":3021108,"relation":"main_file","content_type":"application/pdf","file_name":"2021_EvolutionLetters_Koch.pdf","success":1,"file_id":"10142","creator":"cchlebak","date_created":"2021-10-15T08:26:02Z","date_updated":"2021-10-15T08:26:02Z","checksum":"023b1608e311f0fda30593ba3d0a4e0b","access_level":"open_access"}],"project":[{"call_identifier":"H2020","grant_number":"797747","_id":"265B41B8-B435-11E9-9278-68D0E5697425","name":"Theoretical and empirical approaches to understanding Parallel Adaptation"}],"acknowledgement":"We are very grateful to Irena Senčić for technical assistance and to Michelle Kortyna and Sean Holland at the Center for Anchored Phylogenomics for assistance with data collection. RKB was funded by the Natural Environment Research Council and by the European Research Council. KJ was funded by the Swedish Research Councils VR and Formas (Linnaeus Grant: 217‐2008‐1719). JL was funded by a studentship from the Leverhulme Centre for Advanced Biological Modelling. AMW was funded by the European Union's Horizon 2020 research and innovation program under Marie Skłodowska‐Curie Grant agreement no. 797747. RF was funded by the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska‐Curie Grant agreement No. 706376 and by FEDER Funds through the Operational Competitiveness Factors Program—COMPETE and by National Funds through FCT—Foundation for Science and Technology within the scope of the project “Hybrabbid” (PTDC/BIA‐EVL/30628/2017‐ POCI‐01‐0145‐FEDER‐030628). We are grateful to other members of the Littorina research group for helpful discussions. We thank Claire Mérot and an anonymous referee for insightful comments on an earlier version. ","external_id":{"isi":["000647846200001"]},"article_processing_charge":"No","publication":"Evolution Letters","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","file_date_updated":"2021-10-15T08:26:02Z","status":"public","has_accepted_license":"1","title":"Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis","department":[{"_id":"NiBa"}],"publisher":"Wiley"},{"date_published":"2021-06-01T00:00:00Z","scopus_import":"1","_id":"9470","date_created":"2021-06-06T22:01:31Z","issue":"12","ec_funded":1,"author":[{"full_name":"Berdan, Emma L.","last_name":"Berdan","first_name":"Emma L."},{"full_name":"Blanckaert, Alexandre","last_name":"Blanckaert","first_name":"Alexandre"},{"first_name":"Tanja","last_name":"Slotte","full_name":"Slotte, Tanja"},{"last_name":"Suh","first_name":"Alexander","full_name":"Suh, Alexander"},{"first_name":"Anja M","orcid":"0000-0003-1050-4969","last_name":"Westram","full_name":"Westram, Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Fragata, Inês","first_name":"Inês","last_name":"Fragata"}],"abstract":[{"text":"A key step in understanding the genetic basis of different evolutionary outcomes (e.g., adaptation) is to determine the roles played by different mutation types (e.g., SNPs, translocations and inversions). To do this we must simultaneously consider different mutation types in an evolutionary framework. Here, we propose a research framework that directly utilizes the most important characteristics of mutations, their population genetic effects, to determine their relative evolutionary significance in a given scenario. We review known population genetic effects of different mutation types and show how these may be connected to different evolutionary outcomes. We provide examples of how to implement this framework and pinpoint areas where more data, theory and synthesis are needed. Linking experimental and theoretical approaches to examine different mutation types simultaneously is a critical step towards understanding their evolutionary significance.","lang":"eng"}],"publication_status":"published","intvolume":"        30","type":"journal_article","date_updated":"2023-08-08T13:59:18Z","ddc":["570"],"doi":"10.1111/mec.15936","year":"2021","language":[{"iso":"eng"}],"month":"06","tmp":{"short":"CC BY-NC (4.0)","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode","name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","image":"/images/cc_by_nc.png"},"oa_version":"Published Version","volume":30,"page":"2710-2723","file":[{"date_updated":"2021-06-11T15:34:53Z","date_created":"2021-06-11T15:34:53Z","checksum":"e6f4731365bde2614b333040a08265d8","access_level":"open_access","file_size":1031978,"file_id":"9545","creator":"kschuh","success":1,"file_name":"2021_MolecularEcology_Berdan.pdf","content_type":"application/pdf","relation":"main_file"}],"publication_identifier":{"issn":["09621083"],"eissn":["1365294X"]},"isi":1,"quality_controlled":"1","oa":1,"citation":{"ieee":"E. L. Berdan, A. Blanckaert, T. Slotte, A. Suh, A. M. Westram, and I. Fragata, “Unboxing mutations: Connecting mutation types with evolutionary consequences,” <i>Molecular Ecology</i>, vol. 30, no. 12. Wiley, pp. 2710–2723, 2021.","chicago":"Berdan, Emma L., Alexandre Blanckaert, Tanja Slotte, Alexander Suh, Anja M Westram, and Inês Fragata. “Unboxing Mutations: Connecting Mutation Types with Evolutionary Consequences.” <i>Molecular Ecology</i>. Wiley, 2021. <a href=\"https://doi.org/10.1111/mec.15936\">https://doi.org/10.1111/mec.15936</a>.","short":"E.L. Berdan, A. Blanckaert, T. Slotte, A. Suh, A.M. Westram, I. Fragata, Molecular Ecology 30 (2021) 2710–2723.","ista":"Berdan EL, Blanckaert A, Slotte T, Suh A, Westram AM, Fragata I. 2021. Unboxing mutations: Connecting mutation types with evolutionary consequences. Molecular Ecology. 30(12), 2710–2723.","ama":"Berdan EL, Blanckaert A, Slotte T, Suh A, Westram AM, Fragata I. Unboxing mutations: Connecting mutation types with evolutionary consequences. <i>Molecular Ecology</i>. 2021;30(12):2710-2723. doi:<a href=\"https://doi.org/10.1111/mec.15936\">10.1111/mec.15936</a>","mla":"Berdan, Emma L., et al. “Unboxing Mutations: Connecting Mutation Types with Evolutionary Consequences.” <i>Molecular Ecology</i>, vol. 30, no. 12, Wiley, 2021, pp. 2710–23, doi:<a href=\"https://doi.org/10.1111/mec.15936\">10.1111/mec.15936</a>.","apa":"Berdan, E. L., Blanckaert, A., Slotte, T., Suh, A., Westram, A. M., &#38; Fragata, I. (2021). Unboxing mutations: Connecting mutation types with evolutionary consequences. <i>Molecular Ecology</i>. Wiley. <a href=\"https://doi.org/10.1111/mec.15936\">https://doi.org/10.1111/mec.15936</a>"},"day":"01","file_date_updated":"2021-06-11T15:34:53Z","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","department":[{"_id":"NiBa"}],"title":"Unboxing mutations: Connecting mutation types with evolutionary consequences","has_accepted_license":"1","status":"public","publisher":"Wiley","project":[{"name":"Theoretical and empirical approaches to understanding Parallel Adaptation","_id":"265B41B8-B435-11E9-9278-68D0E5697425","call_identifier":"H2020","grant_number":"797747"}],"acknowledgement":"We thank the editor, two helpful reviewers, Roger Butlin, Kerstin Johannesson, Valentina Peona, Rike Stelkens, Julie Blommaert, Nick Barton, and João Alpedrinha for helpful comments that improved the manuscript. The authors acknowledge funding from the Swedish Research Council Formas (2017-01597 to AS), the Swedish Research Council Vetenskapsrådet (2016-05139 to AS, 2019-04452 to TS) and from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement no. 757451 to TS). ELB was funded by a Carl Tryggers grant awarded to Tanja Slotte. Anja M. Westram was funded by the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 797747. Inês Fragata was funded by a Junior Researcher contract from FCT (CEECIND/02616/2018).","external_id":{"isi":["000652056400001"]},"article_processing_charge":"No","publication":"Molecular Ecology"},{"main_file_link":[{"url":"https://doi.org/10.5061/dryad.zgmsbccb4","open_access":"1"}],"tmp":{"short":"CC0 (1.0)","legal_code_url":"https://creativecommons.org/publicdomain/zero/1.0/legalcode","name":"Creative Commons Public Domain Dedication (CC0 1.0)","image":"/images/cc_0.png"},"date_published":"2021-04-10T00:00:00Z","_id":"12987","oa_version":"Published Version","date_created":"2023-05-16T12:34:09Z","author":[{"first_name":"Eva","last_name":"Koch","full_name":"Koch, Eva"},{"first_name":"Hernán E.","last_name":"Morales","full_name":"Morales, Hernán E."},{"full_name":"Larsson, Jenny","last_name":"Larsson","first_name":"Jenny"},{"id":"3C147470-F248-11E8-B48F-1D18A9856A87","first_name":"Anja M","last_name":"Westram","orcid":"0000-0003-1050-4969","full_name":"Westram, Anja M"},{"last_name":"Faria","first_name":"Rui","full_name":"Faria, Rui"},{"last_name":"Lemmon","first_name":"Alan R.","full_name":"Lemmon, Alan R."},{"first_name":"E. Moriarty","last_name":"Lemmon","full_name":"Lemmon, E. Moriarty"},{"full_name":"Johannesson, Kerstin","last_name":"Johannesson","first_name":"Kerstin"},{"first_name":"Roger K.","last_name":"Butlin","full_name":"Butlin, Roger K."}],"abstract":[{"text":"Chromosomal inversion polymorphisms, segments of chromosomes that are flipped in orientation and occur in reversed order in some individuals, have long been recognized to play an important role in local adaptation. They can reduce recombination in heterozygous individuals and thus help to maintain sets of locally adapted alleles. In a wide range of organisms, populations adapted to different habitats differ in frequency of inversion arrangements. However, getting a full understanding of the importance of inversions for adaptation requires confirmation of their influence on traits under divergent selection. Here, we studied a marine snail, Littorina saxatilis, that has evolved ecotypes adapted to wave exposure or crab predation. These two types occur in close proximity on different parts of the shore. Gene flow between them exists in contact zones. However, they exhibit strong phenotypic divergence in several traits under habitat-specific selection, including size, shape and behaviour. We used crosses between these ecotypes to identify genomic regions that explain variation in these traits by using QTL analysis and variance partitioning across linkage groups. We could show that previously detected inversion regions contribute to adaptive divergence. Some inversions influenced multiple traits suggesting that they contain sets of locally adaptive alleles. Our study also identified regions without known inversions that are important for phenotypic divergence. Thus, we provide a more complete overview of the importance of inversions in relation to the remaining genome.","lang":"eng"}],"citation":{"short":"E. Koch, H.E. Morales, J. Larsson, A.M. Westram, R. Faria, A.R. Lemmon, E.M. Lemmon, K. Johannesson, R.K. Butlin, (2021).","ieee":"E. Koch <i>et al.</i>, “Data from: Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis.” Dryad, 2021.","chicago":"Koch, Eva, Hernán E. Morales, Jenny Larsson, Anja M Westram, Rui Faria, Alan R. Lemmon, E. Moriarty Lemmon, Kerstin Johannesson, and Roger K. Butlin. “Data from: Genetic Variation for Adaptive Traits Is Associated with Polymorphic Inversions in Littorina Saxatilis.” Dryad, 2021. <a href=\"https://doi.org/10.5061/DRYAD.ZGMSBCCB4\">https://doi.org/10.5061/DRYAD.ZGMSBCCB4</a>.","mla":"Koch, Eva, et al. <i>Data from: Genetic Variation for Adaptive Traits Is Associated with Polymorphic Inversions in Littorina Saxatilis</i>. Dryad, 2021, doi:<a href=\"https://doi.org/10.5061/DRYAD.ZGMSBCCB4\">10.5061/DRYAD.ZGMSBCCB4</a>.","ama":"Koch E, Morales HE, Larsson J, et al. Data from: Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis. 2021. doi:<a href=\"https://doi.org/10.5061/DRYAD.ZGMSBCCB4\">10.5061/DRYAD.ZGMSBCCB4</a>","apa":"Koch, E., Morales, H. E., Larsson, J., Westram, A. M., Faria, R., Lemmon, A. R., … Butlin, R. K. (2021). Data from: Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis. Dryad. <a href=\"https://doi.org/10.5061/DRYAD.ZGMSBCCB4\">https://doi.org/10.5061/DRYAD.ZGMSBCCB4</a>","ista":"Koch E, Morales HE, Larsson J, Westram AM, Faria R, Lemmon AR, Lemmon EM, Johannesson K, Butlin RK. 2021. Data from: Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis, Dryad, <a href=\"https://doi.org/10.5061/DRYAD.ZGMSBCCB4\">10.5061/DRYAD.ZGMSBCCB4</a>."},"related_material":{"record":[{"status":"public","relation":"used_in_publication","id":"9394"}]},"oa":1,"day":"10","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","status":"public","department":[{"_id":"NiBa"}],"title":"Data from: Genetic variation for adaptive traits is associated with polymorphic inversions in Littorina saxatilis","has_accepted_license":"1","date_updated":"2023-08-08T13:34:07Z","type":"research_data_reference","publisher":"Dryad","ddc":["570"],"year":"2021","doi":"10.5061/DRYAD.ZGMSBCCB4","article_processing_charge":"No","month":"04"},{"quality_controlled":"1","isi":1,"publication_identifier":{"issn":["00143820"],"eissn":["15585646"]},"day":"01","citation":{"apa":"Perini, S., Rafajlović, M., Westram, A. M., Johannesson, K., &#38; Butlin, R. K. (2020). Assortative mating, sexual selection, and their consequences for gene flow in Littorina. <i>Evolution</i>. Wiley. <a href=\"https://doi.org/10.1111/evo.14027\">https://doi.org/10.1111/evo.14027</a>","ama":"Perini S, Rafajlović M, Westram AM, Johannesson K, Butlin RK. Assortative mating, sexual selection, and their consequences for gene flow in Littorina. <i>Evolution</i>. 2020;74(7):1482-1497. doi:<a href=\"https://doi.org/10.1111/evo.14027\">10.1111/evo.14027</a>","mla":"Perini, Samuel, et al. “Assortative Mating, Sexual Selection, and Their Consequences for Gene Flow in Littorina.” <i>Evolution</i>, vol. 74, no. 7, Wiley, 2020, pp. 1482–97, doi:<a href=\"https://doi.org/10.1111/evo.14027\">10.1111/evo.14027</a>.","ista":"Perini S, Rafajlović M, Westram AM, Johannesson K, Butlin RK. 2020. Assortative mating, sexual selection, and their consequences for gene flow in Littorina. Evolution. 74(7), 1482–1497.","short":"S. Perini, M. Rafajlović, A.M. Westram, K. Johannesson, R.K. Butlin, Evolution 74 (2020) 1482–1497.","ieee":"S. Perini, M. Rafajlović, A. M. Westram, K. Johannesson, and R. K. Butlin, “Assortative mating, sexual selection, and their consequences for gene flow in Littorina,” <i>Evolution</i>, vol. 74, no. 7. Wiley, pp. 1482–1497, 2020.","chicago":"Perini, Samuel, Marina Rafajlović, Anja M Westram, Kerstin Johannesson, and Roger K. Butlin. “Assortative Mating, Sexual Selection, and Their Consequences for Gene Flow in Littorina.” <i>Evolution</i>. Wiley, 2020. <a href=\"https://doi.org/10.1111/evo.14027\">https://doi.org/10.1111/evo.14027</a>."},"oa":1,"tmp":{"image":"/images/cc_by.png","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode","short":"CC BY (4.0)"},"file":[{"relation":"main_file","content_type":"application/pdf","file_name":"2020_Evolution_Perini.pdf","success":1,"file_id":"8808","creator":"dernst","file_size":1080810,"access_level":"open_access","checksum":"56235bf1e2a9e25f96196bb13b6b754d","date_created":"2020-11-25T10:49:48Z","date_updated":"2020-11-25T10:49:48Z"}],"article_type":"original","page":"1482-1497","oa_version":"Published Version","volume":74,"acknowledgement":"We are very grateful to I. Sencic, L. Brettell, A.‐L. Liabot, J. Galindo, M. Ravinet, and A. Butlin for their help with field sampling and mating experiments. This work was funded by the Natural Environment Research Council, European Research Council and Swedish Research Council VR and we are also very grateful for the support of the Linnaeus Centre for Marine Evolutionary Biology at the University of Gothenburg. The simulations were performed on resources at Chalmers Centre for Computational Science and Engineering (C3SE) provided by the Swedish National Infrastructure for Computing (SNIC). AMW was funded by the European Union's Horizon 2020 research and innovation program under Marie Skłodowska‐Curie grant agreement no. 797747.","external_id":{"isi":["000539780800001"]},"project":[{"_id":"265B41B8-B435-11E9-9278-68D0E5697425","grant_number":"797747","call_identifier":"H2020","name":"Theoretical and empirical approaches to understanding Parallel Adaptation"}],"publication":"Evolution","article_processing_charge":"No","has_accepted_license":"1","title":"Assortative mating, sexual selection, and their consequences for gene flow in Littorina","status":"public","department":[{"_id":"NiBa"}],"user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","file_date_updated":"2020-11-25T10:49:48Z","publisher":"Wiley","ec_funded":1,"author":[{"last_name":"Perini","first_name":"Samuel","full_name":"Perini, Samuel"},{"first_name":"Marina","last_name":"Rafajlović","full_name":"Rafajlović, Marina"},{"orcid":"0000-0003-1050-4969","last_name":"Westram","first_name":"Anja M","full_name":"Westram, Anja M","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"full_name":"Johannesson, Kerstin","first_name":"Kerstin","last_name":"Johannesson"},{"last_name":"Butlin","first_name":"Roger K.","full_name":"Butlin, Roger K."}],"abstract":[{"text":"When divergent populations are connected by gene flow, the establishment of complete reproductive isolation usually requires the joint action of multiple barrier effects. One example where multiple barrier effects are coupled consists of a single trait that is under divergent natural selection and also mediates assortative mating. Such multiple‐effect traits can strongly reduce gene flow. However, there are few cases where patterns of assortative mating have been described quantitatively and their impact on gene flow has been determined. Two ecotypes of the coastal marine snail, Littorina saxatilis , occur in North Atlantic rocky‐shore habitats dominated by either crab predation or wave action. There is evidence for divergent natural selection acting on size, and size‐assortative mating has previously been documented. Here, we analyze the mating pattern in L. saxatilis with respect to size in intensively sampled transects across boundaries between the habitats. We show that the mating pattern is mostly conserved between ecotypes and that it generates both assortment and directional sexual selection for small male size. Using simulations, we show that the mating pattern can contribute to reproductive isolation between ecotypes but the barrier to gene flow is likely strengthened more by sexual selection than by assortment.","lang":"eng"}],"issue":"7","related_material":{"record":[{"id":"8809","relation":"research_data","status":"public"}]},"scopus_import":"1","date_published":"2020-07-01T00:00:00Z","date_created":"2020-06-22T09:14:21Z","_id":"7995","year":"2020","doi":"10.1111/evo.14027","ddc":["570"],"month":"07","language":[{"iso":"eng"}],"intvolume":"        74","publication_status":"published","date_updated":"2023-08-22T07:13:38Z","type":"journal_article"},{"_id":"8167","date_created":"2020-07-26T22:01:01Z","pmid":1,"date_published":"2020-07-12T00:00:00Z","scopus_import":"1","issue":"1806","abstract":[{"lang":"eng","text":"The evolution of strong reproductive isolation (RI) is fundamental to the origins and maintenance of biological diversity, especially in situations where geographical distributions of taxa broadly overlap. But what is the history behind strong barriers currently acting in sympatry? Using whole-genome sequencing and single nucleotide polymorphism genotyping, we inferred (i) the evolutionary relationships, (ii) the strength of RI, and (iii) the demographic history of divergence between two broadly sympatric taxa of intertidal snail. Despite being cryptic, based on external morphology, Littorina arcana and Littorina saxatilis differ in their mode of female reproduction (egg-laying versus brooding), which may generate a strong post-zygotic barrier. We show that egg-laying and brooding snails are closely related, but genetically distinct. Genotyping of 3092 snails from three locations failed to recover any recent hybrid or backcrossed individuals, confirming that RI is strong. There was, however, evidence for a very low level of asymmetrical introgression, suggesting that isolation remains incomplete. The presence of strong, asymmetrical RI was further supported by demographic analysis of these populations. Although the taxa are currently broadly sympatric, demographic modelling suggests that they initially diverged during a short period of geographical separation involving very low gene flow. Our study suggests that some geographical separation may kick-start the evolution of strong RI, facilitating subsequent coexistence of taxa in sympatry. The strength of RI needed to achieve sympatry and the subsequent effect of sympatry on RI remain open questions."}],"author":[{"id":"43161670-5719-11EA-8025-FABC3DDC885E","first_name":"Sean","last_name":"Stankowski","full_name":"Stankowski, Sean"},{"full_name":"Westram, Anja M","first_name":"Anja M","orcid":"0000-0003-1050-4969","last_name":"Westram","id":"3C147470-F248-11E8-B48F-1D18A9856A87"},{"last_name":"Zagrodzka","first_name":"Zuzanna B.","full_name":"Zagrodzka, Zuzanna B."},{"last_name":"Eyres","first_name":"Isobel","full_name":"Eyres, Isobel"},{"full_name":"Broquet, Thomas","first_name":"Thomas","last_name":"Broquet"},{"last_name":"Johannesson","first_name":"Kerstin","full_name":"Johannesson, Kerstin"},{"last_name":"Butlin","first_name":"Roger K.","full_name":"Butlin, Roger K."}],"type":"journal_article","date_updated":"2023-08-22T08:22:13Z","publication_status":"published","intvolume":"       375","language":[{"iso":"eng"}],"month":"07","doi":"10.1098/rstb.2019.0545","year":"2020","oa_version":"Published Version","volume":375,"article_type":"original","main_file_link":[{"url":"https://doi.org/10.1098/rstb.2019.0545","open_access":"1"}],"oa":1,"citation":{"apa":"Stankowski, S., Westram, A. M., Zagrodzka, Z. B., Eyres, I., Broquet, T., Johannesson, K., &#38; Butlin, R. K. (2020). The evolution of strong reproductive isolation between sympatric intertidal snails. <i>Philosophical Transactions of the Royal Society. Series B: Biological Sciences</i>. The Royal Society. <a href=\"https://doi.org/10.1098/rstb.2019.0545\">https://doi.org/10.1098/rstb.2019.0545</a>","ama":"Stankowski S, Westram AM, Zagrodzka ZB, et al. The evolution of strong reproductive isolation between sympatric intertidal snails. <i>Philosophical Transactions of the Royal Society Series B: Biological Sciences</i>. 2020;375(1806). doi:<a href=\"https://doi.org/10.1098/rstb.2019.0545\">10.1098/rstb.2019.0545</a>","mla":"Stankowski, Sean, et al. “The Evolution of Strong Reproductive Isolation between Sympatric Intertidal Snails.” <i>Philosophical Transactions of the Royal Society. Series B: Biological Sciences</i>, vol. 375, no. 1806, 20190545, The Royal Society, 2020, doi:<a href=\"https://doi.org/10.1098/rstb.2019.0545\">10.1098/rstb.2019.0545</a>.","ista":"Stankowski S, Westram AM, Zagrodzka ZB, Eyres I, Broquet T, Johannesson K, Butlin RK. 2020. The evolution of strong reproductive isolation between sympatric intertidal snails. Philosophical Transactions of the Royal Society. Series B: Biological Sciences. 375(1806), 20190545.","short":"S. Stankowski, A.M. Westram, Z.B. Zagrodzka, I. Eyres, T. Broquet, K. Johannesson, R.K. Butlin, Philosophical Transactions of the Royal Society. Series B: Biological Sciences 375 (2020).","ieee":"S. Stankowski <i>et al.</i>, “The evolution of strong reproductive isolation between sympatric intertidal snails,” <i>Philosophical Transactions of the Royal Society. Series B: Biological Sciences</i>, vol. 375, no. 1806. The Royal Society, 2020.","chicago":"Stankowski, Sean, Anja M Westram, Zuzanna B. Zagrodzka, Isobel Eyres, Thomas Broquet, Kerstin Johannesson, and Roger K. Butlin. “The Evolution of Strong Reproductive Isolation between Sympatric Intertidal Snails.” <i>Philosophical Transactions of the Royal Society. Series B: Biological Sciences</i>. The Royal Society, 2020. <a href=\"https://doi.org/10.1098/rstb.2019.0545\">https://doi.org/10.1098/rstb.2019.0545</a>."},"article_number":"20190545","day":"12","publication_identifier":{"eissn":["1471-2970"]},"isi":1,"quality_controlled":"1","publisher":"The Royal Society","user_id":"4359f0d1-fa6c-11eb-b949-802e58b17ae8","department":[{"_id":"NiBa"}],"title":"The evolution of strong reproductive isolation between sympatric intertidal snails","status":"public","article_processing_charge":"No","publication":"Philosophical Transactions of the Royal Society. Series B: Biological Sciences","external_id":{"pmid":["32654639"],"isi":["000552662100014"]},"acknowledgement":"Funding was provided by the Natural Environment Research Council (NERC) and the European Research Council. We thank Rui Faria, Nicola Nadeau, Martin Garlovsky and Hernan Morales for advice and/or useful discussion during the project. Richard Turney, Graciela Sotelo, Jenny Larson, Stéphane Loisel and Meghan Wharton participated in the collection and processing of samples. Mark Dunning helped with the development of bioinformatic pipelines. The analysis of genomic data was conducted on the University of Sheffield High-performance computer, ShARC. Jeffrey Feder and an anonymous reviewer provided comments that improved the manuscript."}]
