[{"intvolume":"         8","date_updated":"2025-09-09T12:05:51Z","date_published":"2024-04-23T00:00:00Z","tmp":{"short":"CC BY-NC (4.0)","name":"Creative Commons Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)","image":"/images/cc_by_nc.png","legal_code_url":"https://creativecommons.org/licenses/by-nc/4.0/legalcode"},"citation":{"ista":"Le Moan A, Stankowski S, Rafajlović M, Ortega-Martinez O, Faria R, Butlin RK, Johannesson K. 2024. Coupling of twelve putative chromosomal inversions maintains a strong barrier to gene flow between snail ecotypes. Evolution Letters. 8(4), 575–586.","chicago":"Le Moan, Alan, Sean Stankowski, Marina Rafajlović, Olga Ortega-Martinez, Rui Faria, Roger K Butlin, and Kerstin Johannesson. “Coupling of Twelve Putative Chromosomal Inversions Maintains a Strong Barrier to Gene Flow between Snail Ecotypes.” <i>Evolution Letters</i>. Oxford University Press, 2024. <a href=\"https://doi.org/10.1093/evlett/qrae014\">https://doi.org/10.1093/evlett/qrae014</a>.","ama":"Le Moan A, Stankowski S, Rafajlović M, et al. Coupling of twelve putative chromosomal inversions maintains a strong barrier to gene flow between snail ecotypes. <i>Evolution Letters</i>. 2024;8(4):575-586. doi:<a href=\"https://doi.org/10.1093/evlett/qrae014\">10.1093/evlett/qrae014</a>","apa":"Le Moan, A., Stankowski, S., Rafajlović, M., Ortega-Martinez, O., Faria, R., Butlin, R. K., &#38; Johannesson, K. (2024). Coupling of twelve putative chromosomal inversions maintains a strong barrier to gene flow between snail ecotypes. <i>Evolution Letters</i>. Oxford University Press. <a href=\"https://doi.org/10.1093/evlett/qrae014\">https://doi.org/10.1093/evlett/qrae014</a>","short":"A. Le Moan, S. Stankowski, M. Rafajlović, O. Ortega-Martinez, R. Faria, R.K. Butlin, K. Johannesson, Evolution Letters 8 (2024) 575–586.","ieee":"A. Le Moan <i>et al.</i>, “Coupling of twelve putative chromosomal inversions maintains a strong barrier to gene flow between snail ecotypes,” <i>Evolution Letters</i>, vol. 8, no. 4. Oxford University Press, pp. 575–586, 2024.","mla":"Le Moan, Alan, et al. “Coupling of Twelve Putative Chromosomal Inversions Maintains a Strong Barrier to Gene Flow between Snail Ecotypes.” <i>Evolution Letters</i>, vol. 8, no. 4, Oxford University Press, 2024, pp. 575–86, doi:<a href=\"https://doi.org/10.1093/evlett/qrae014\">10.1093/evlett/qrae014</a>."},"abstract":[{"lang":"eng","text":"Chromosomal rearrangements can lead to the coupling of reproductive barriers, but whether and how they contribute to the completion of speciation remains unclear. Marine snails of the genus Littorina repeatedly form hybrid zones between populations segregating for multiple inversion arrangements, providing opportunities to study their barrier effects. Here, we analyzed 2 adjacent transects across hybrid zones between 2 ecotypes of Littorina fabalis (“large” and “dwarf”) adapted to different wave exposure conditions on a Swedish island. Applying whole-genome sequencing, we found 12 putative inversions on 9 of 17 chromosomes. Nine of the putative inversions reached near differential fixation between the 2 ecotypes, and all were in strong linkage disequilibrium. These inversions cover 20% of the genome and carry 93% of divergent single nucleotide polymorphisms (SNPs). Bimodal hybrid zones in both transects indicated that the 2 ecotypes of Littorina fabalis maintain their genetic and phenotypic integrity following contact. The bimodality reflects the strong coupling between inversion clines and the extension of the barrier effect across the whole genome. Demographic inference suggests that coupling arose during a period of allopatry and has been maintained for &amp;gt; 1,000 generations after secondary contact. Overall, this study shows that the coupling of multiple chromosomal inversions contributes to strong reproductive isolation. Notably, 2 of the putative inversions overlap with inverted genomic regions associated with ecotype differences in a closely related species (Littorina saxatilis), suggesting the same regions, with similar structural variants, repeatedly contribute to ecotype evolution in distinct species."}],"has_accepted_license":"1","month":"04","ddc":["570"],"acknowledgement":"The computations and data handling were enabled by resources provided by the Swedish National Infrastructure for Computing at UPPMAX partially funded by the Swedish Research Council through grant agreement no. 2018-05973. We thank all the member of the Littorina team for the stimulating discussions about the manuscripts, James Reeves for his help the implementation of Hsplit, and Thomas Broquet for his useful comments in the latter stage of manuscript revisions.","volume":8,"file":[{"file_id":"18909","success":1,"file_name":"2024_EvolutionLetter_Moan.pdf","content_type":"application/pdf","file_size":24356661,"access_level":"open_access","date_created":"2025-01-27T13:33:14Z","creator":"dernst","date_updated":"2025-01-27T13:33:14Z","checksum":"2f7780b7b6b3489755f1815f476639c6","relation":"main_file"}],"page":"575-586","author":[{"first_name":"Alan","last_name":"Le Moan","full_name":"Le Moan, Alan"},{"first_name":"Sean","last_name":"Stankowski","full_name":"Stankowski, Sean","id":"43161670-5719-11EA-8025-FABC3DDC885E"},{"full_name":"Rafajlović, Marina","first_name":"Marina","last_name":"Rafajlović"},{"full_name":"Ortega-Martinez, Olga","last_name":"Ortega-Martinez","first_name":"Olga"},{"full_name":"Faria, Rui","first_name":"Rui","last_name":"Faria"},{"full_name":"Butlin, Roger K","last_name":"Butlin","first_name":"Roger K"},{"first_name":"Kerstin","last_name":"Johannesson","full_name":"Johannesson, Kerstin"}],"status":"public","publication":"Evolution Letters","issue":"4","quality_controlled":"1","isi":1,"date_created":"2025-01-27T13:30:27Z","OA_place":"publisher","language":[{"iso":"eng"}],"file_date_updated":"2025-01-27T13:33:14Z","article_type":"letter_note","scopus_import":"1","oa_version":"Published Version","_id":"18908","doi":"10.1093/evlett/qrae014","title":"Coupling of twelve putative chromosomal inversions maintains a strong barrier to gene flow between snail ecotypes","article_processing_charge":"Yes","license":"https://creativecommons.org/licenses/by-nc/4.0/","user_id":"317138e5-6ab7-11ef-aa6d-ffef3953e345","publication_identifier":{"issn":["2056-3744"]},"department":[{"_id":"NiBa"}],"publisher":"Oxford University Press","publication_status":"published","OA_type":"gold","year":"2024","oa":1,"day":"23","external_id":{"pmid":["39479507"],"isi":["001206532900001"]},"pmid":1,"type":"journal_article"},{"date_published":"2023-02-01T00:00:00Z","related_material":{"record":[{"id":"18531","relation":"dissertation_contains","status":"public"}]},"tmp":{"short":"CC BY (4.0)","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","image":"/images/cc_by.png","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"abstract":[{"text":"Differentiated X chromosomes are expected to have higher rates of adaptive divergence than autosomes, if new beneficial mutations are recessive (the “faster-X effect”), largely because these mutations are immediately exposed to selection in males. The evolution of X chromosomes after they stop recombining in males, but before they become hemizygous, has not been well explored theoretically. We use the diffusion approximation to infer substitution rates of beneficial and deleterious mutations under such a scenario. Our results show that selection is less efficient on diploid X loci than on autosomal and hemizygous X loci under a wide range of parameters. This “slower-X” effect is stronger for genes affecting primarily (or only) male fitness, and for sexually antagonistic genes. These unusual dynamics suggest that some of the peculiar features of X chromosomes, such as the differential accumulation of genes with sex-specific functions, may start arising earlier than previously appreciated.","lang":"eng"}],"citation":{"ista":"Mrnjavac A, Khudiakova K, Barton NH, Vicoso B. 2023. Slower-X: Reduced efficiency of selection in the early stages of X chromosome evolution. Evolution Letters. 7(1), qrac004.","apa":"Mrnjavac, A., Khudiakova, K., Barton, N. H., &#38; Vicoso, B. (2023). Slower-X: Reduced efficiency of selection in the early stages of X chromosome evolution. <i>Evolution Letters</i>. Oxford University Press. <a href=\"https://doi.org/10.1093/evlett/qrac004\">https://doi.org/10.1093/evlett/qrac004</a>","mla":"Mrnjavac, Andrea, et al. “Slower-X: Reduced Efficiency of Selection in the Early Stages of X Chromosome Evolution.” <i>Evolution Letters</i>, vol. 7, no. 1, qrac004, Oxford University Press, 2023, doi:<a href=\"https://doi.org/10.1093/evlett/qrac004\">10.1093/evlett/qrac004</a>.","ieee":"A. Mrnjavac, K. Khudiakova, N. H. Barton, and B. Vicoso, “Slower-X: Reduced efficiency of selection in the early stages of X chromosome evolution,” <i>Evolution Letters</i>, vol. 7, no. 1. Oxford University Press, 2023.","short":"A. Mrnjavac, K. Khudiakova, N.H. Barton, B. Vicoso, Evolution Letters 7 (2023).","chicago":"Mrnjavac, Andrea, Kseniia Khudiakova, Nicholas H Barton, and Beatriz Vicoso. “Slower-X: Reduced Efficiency of Selection in the Early Stages of X Chromosome Evolution.” <i>Evolution Letters</i>. Oxford University Press, 2023. <a href=\"https://doi.org/10.1093/evlett/qrac004\">https://doi.org/10.1093/evlett/qrac004</a>.","ama":"Mrnjavac A, Khudiakova K, Barton NH, Vicoso B. Slower-X: Reduced efficiency of selection in the early stages of X chromosome evolution. <i>Evolution Letters</i>. 2023;7(1). doi:<a href=\"https://doi.org/10.1093/evlett/qrac004\">10.1093/evlett/qrac004</a>"},"has_accepted_license":"1","corr_author":"1","intvolume":"         7","keyword":["Genetics","Ecology","Evolution","Behavior and Systematics"],"date_updated":"2026-05-17T22:30:30Z","author":[{"id":"353FAC84-AE61-11E9-8BFC-00D3E5697425","full_name":"Mrnjavac, Andrea","last_name":"Mrnjavac","first_name":"Andrea"},{"orcid":"0000-0002-6246-1465","last_name":"Khudiakova","first_name":"Kseniia","id":"4E6DC800-AE37-11E9-AC72-31CAE5697425","full_name":"Khudiakova, Kseniia"},{"orcid":"0000-0002-8548-5240","last_name":"Barton","first_name":"Nicholas H","full_name":"Barton, Nicholas H","id":"4880FE40-F248-11E8-B48F-1D18A9856A87"},{"first_name":"Beatriz","orcid":"0000-0002-4579-8306","last_name":"Vicoso","full_name":"Vicoso, Beatriz","id":"49E1C5C6-F248-11E8-B48F-1D18A9856A87"}],"status":"public","issue":"1","publication":"Evolution Letters","month":"02","ddc":["570"],"article_number":"qrac004","volume":7,"ec_funded":1,"acknowledgement":"We thank the Vicoso and Barton groups and ISTA Scientific Computing Unit. We also thank two anonymous reviewers for their valuable comments. This work was supported by the European Research Council under the European Union’s Horizon 2020 research and innovation program (grant agreements no. 715257 and no. 716117).","file":[{"file_id":"14068","file_name":"2023_EvLetters_Mrnjavac.pdf","success":1,"content_type":"application/pdf","file_size":2592189,"date_created":"2023-08-16T11:43:33Z","access_level":"open_access","date_updated":"2023-08-16T11:43:33Z","creator":"dernst","checksum":"a240a041cb9b9b7c8ba93a4706674a3f","relation":"main_file"}],"language":[{"iso":"eng"}],"file_date_updated":"2023-08-16T11:43:33Z","article_type":"original","scopus_import":"1","oa_version":"Published Version","_id":"12521","doi":"10.1093/evlett/qrac004","quality_controlled":"1","project":[{"_id":"256E75B8-B435-11E9-9278-68D0E5697425","name":"Optimal Transport and Stochastic Dynamics","call_identifier":"H2020","grant_number":"716117"},{"grant_number":"715257","name":"Prevalence and Influence of Sexual Antagonism on Genome Evolution","_id":"250BDE62-B435-11E9-9278-68D0E5697425","call_identifier":"H2020"}],"isi":1,"date_created":"2023-02-06T13:59:12Z","department":[{"_id":"GradSch"},{"_id":"BeVi"}],"publisher":"Oxford University Press","publication_status":"published","year":"2023","oa":1,"pmid":1,"external_id":{"isi":["001021692200001"],"pmid":["37065438"]},"day":"01","type":"journal_article","title":"Slower-X: Reduced efficiency of selection in the early stages of X chromosome evolution","article_processing_charge":"Yes (via OA deal)","license":"https://creativecommons.org/licenses/by/4.0/","user_id":"2DF688A6-F248-11E8-B48F-1D18A9856A87","publication_identifier":{"issn":["2056-3744"]}},{"publisher":"Wiley","publication_status":"published","year":"2018","department":[{"_id":"BeVi"}],"type":"journal_article","oa":1,"day":"20","external_id":{"pmid":["30283683"],"isi":["000446774400004"]},"pmid":1,"title":"Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow","article_processing_charge":"Yes","user_id":"c635000d-4b10-11ee-a964-aac5a93f6ac1","publication_identifier":{"issn":["2056-3744"],"eissn":["2056-3744"]},"article_type":"letter_note","file_date_updated":"2021-08-16T07:48:03Z","language":[{"iso":"eng"}],"doi":"10.1002/evl3.74","oa_version":"Published Version","scopus_import":"1","_id":"9917","quality_controlled":"1","date_created":"2021-08-16T07:45:38Z","isi":1,"author":[{"first_name":"Anja M","last_name":"Westram","orcid":"0000-0003-1050-4969","id":"3C147470-F248-11E8-B48F-1D18A9856A87","full_name":"Westram, Anja M"},{"last_name":"Rafajlović","first_name":"Marina","full_name":"Rafajlović, Marina"},{"full_name":"Chaube, Pragya","last_name":"Chaube","first_name":"Pragya"},{"full_name":"Faria, Rui","last_name":"Faria","first_name":"Rui"},{"first_name":"Tomas","last_name":"Larsson","full_name":"Larsson, Tomas"},{"full_name":"Panova, Marina","last_name":"Panova","first_name":"Marina"},{"full_name":"Ravinet, Mark","last_name":"Ravinet","first_name":"Mark"},{"first_name":"Anders","last_name":"Blomberg","full_name":"Blomberg, Anders"},{"last_name":"Mehlig","first_name":"Bernhard","full_name":"Mehlig, Bernhard"},{"first_name":"Kerstin","last_name":"Johannesson","full_name":"Johannesson, Kerstin"},{"first_name":"Roger","last_name":"Butlin","full_name":"Butlin, Roger"}],"status":"public","issue":"4","publication":"Evolution Letters","ddc":["570"],"acknowledgement":"We are very grateful to people who helped with fieldwork, snail processing, and DNA extractions, particularly Laura Brettell, Mårten Duvetorp, Juan Galindo, Anne-Lise Liabot and Irena Senčić. We would also like to thank Magnus Alm Rosenblad and Mats Töpel for their contribution to assembling the Littorina saxatilis genome, Carl André, Pasi Rastas, and Romain Villoutreix for discussion, and two anonymous reviewers for their helpful comments on the manuscript. We are grateful to RapidGenomics for library preparation and sequencing. We thank the Natural Environment Research Council, the European Research Council and the Swedish Research Councils VR and Formas (Linnaeus grant to the Centre for Marine Evolutionary Biology and Tage Erlander Guest Professorship) for funding. P.C. was funded by the University of Sheffield Vice-chancellor's India scholarship. R.F. is funded by the European Union's Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement no. 706376. M. Raf. was supported by the Adlerbert Research Foundation.","volume":2,"month":"08","page":"297-309","file":[{"content_type":"application/pdf","file_size":764299,"file_id":"9918","success":1,"file_name":"2018_EvolutionLetters_Westram.pdf","checksum":"8524e72507d521416be3f8ccfcd5e3f5","relation":"main_file","date_created":"2021-08-16T07:48:03Z","access_level":"open_access","creator":"asandaue","date_updated":"2021-08-16T07:48:03Z"}],"related_material":{"record":[{"relation":"research_data","status":"public","id":"9930"}]},"tmp":{"short":"CC BY (4.0)","name":"Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)","image":"/images/cc_by.png","legal_code_url":"https://creativecommons.org/licenses/by/4.0/legalcode"},"date_published":"2018-08-20T00:00:00Z","has_accepted_license":"1","abstract":[{"text":"Adaptive divergence and speciation may happen despite opposition by gene flow. Identifying the genomic basis underlying divergence with gene flow is a major task in evolutionary genomics. Most approaches (e.g., outlier scans) focus on genomic regions of high differentiation. However, not all genomic architectures potentially underlying divergence are expected to show extreme differentiation. Here, we develop an approach that combines hybrid zone analysis (i.e., focuses on spatial patterns of allele frequency change) with system-specific simulations to identify loci inconsistent with neutral evolution. We apply this to a genome-wide SNP set from an ideally suited study organism, the intertidal snail Littorina saxatilis, which shows primary divergence between ecotypes associated with different shore habitats. We detect many SNPs with clinal patterns, most of which are consistent with neutrality. Among non-neutral SNPs, most are located within three large putative inversions differentiating ecotypes. Many non-neutral SNPs show relatively low levels of differentiation. We discuss potential reasons for this pattern, including loose linkage to selected variants, polygenic adaptation and a component of balancing selection within populations (which may be expected for inversions). Our work is in line with theory predicting a role for inversions in divergence, and emphasizes that genomic regions contributing to divergence may not always be accessible with methods purely based on allele frequency differences. These conclusions call for approaches that take spatial patterns of allele frequency change into account in other systems.","lang":"eng"}],"citation":{"apa":"Westram, A. M., Rafajlović, M., Chaube, P., Faria, R., Larsson, T., Panova, M., … Butlin, R. (2018). Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow. <i>Evolution Letters</i>. Wiley. <a href=\"https://doi.org/10.1002/evl3.74\">https://doi.org/10.1002/evl3.74</a>","short":"A.M. Westram, M. Rafajlović, P. Chaube, R. Faria, T. Larsson, M. Panova, M. Ravinet, A. Blomberg, B. Mehlig, K. Johannesson, R. Butlin, Evolution Letters 2 (2018) 297–309.","mla":"Westram, Anja M., et al. “Clines on the Seashore: The Genomic Architecture Underlying Rapid Divergence in the Face of Gene Flow.” <i>Evolution Letters</i>, vol. 2, no. 4, Wiley, 2018, pp. 297–309, doi:<a href=\"https://doi.org/10.1002/evl3.74\">10.1002/evl3.74</a>.","ieee":"A. M. Westram <i>et al.</i>, “Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow,” <i>Evolution Letters</i>, vol. 2, no. 4. Wiley, pp. 297–309, 2018.","chicago":"Westram, Anja M, Marina Rafajlović, Pragya Chaube, Rui Faria, Tomas Larsson, Marina Panova, Mark Ravinet, et al. “Clines on the Seashore: The Genomic Architecture Underlying Rapid Divergence in the Face of Gene Flow.” <i>Evolution Letters</i>. Wiley, 2018. <a href=\"https://doi.org/10.1002/evl3.74\">https://doi.org/10.1002/evl3.74</a>.","ama":"Westram AM, Rafajlović M, Chaube P, et al. Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow. <i>Evolution Letters</i>. 2018;2(4):297-309. doi:<a href=\"https://doi.org/10.1002/evl3.74\">10.1002/evl3.74</a>","ista":"Westram AM, Rafajlović M, Chaube P, Faria R, Larsson T, Panova M, Ravinet M, Blomberg A, Mehlig B, Johannesson K, Butlin R. 2018. Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow. Evolution Letters. 2(4), 297–309."},"intvolume":"         2","date_updated":"2024-10-21T06:02:42Z"}]