{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,22]],"date-time":"2026-09-22T13:23:53Z","timestamp":1790083433919,"version":"4.0.1"},"reference-count":68,"publisher":"Oxford University Press (OUP)","issue":"5","license":[{"start":{"date-parts":[[2025,7,31]],"date-time":"2025-07-31T00:00:00Z","timestamp":1753920000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["RGPIN-2024-04608 to D.V.M."],"award-info":[{"award-number":["RGPIN-2024-04608 to D.V.M."]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,10,3]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Microbial adaptation is driven by the circulation of mobile genetic elements (MGEs) among bacteria. On the one hand, MGEs can be viewed as selfish genes that spread like infectious diseases in a host population. On the other hand, the horizontal transfer and the loss of these MGEs are often viewed as a form of sexual reproduction that reshuffles genetic diversity in a way that may sometimes be adaptive for bacteria cells. Here, we show how these 2 perspectives can be reconciled using a single unified framework capturing the dynamics of multiple, interacting MGEs. We apply this framework to study how interactions between MGEs affecting rates of horizontal gene transfer and segregation loss shape the short- and long-term evolutionary dynamics of MGEs and the bacteria population. We show that these interactions produce nonrandom MGE associations that can speed up or slow down microbial adaptation depending on the evolutionary conflicts between MGEs as well as between MGEs and their bacterial hosts. Moreover, we show how these interactions affect the evolutionary potential of the bacteria population. We discuss the implications of these predictions for the community response to environmental stressors such as antibiotic treatment or vaccination campaigns as well as the evolution of accessory genomes.<\/jats:p>","DOI":"10.1093\/evlett\/qraf024","type":"journal-article","created":{"date-parts":[[2025,7,14]],"date-time":"2025-07-14T14:07:59Z","timestamp":1752502079000},"page":"576-588","source":"Crossref","is-referenced-by-count":4,"title":["Horizontal gene transfer, segregation loss, and the speed of microbial adaptation"],"prefix":"10.1093","volume":"9","author":[{"given":"David V","family":"McLeod","sequence":"first","affiliation":[{"name":"Universit\u00e9 de Montr\u00e9al D\u00e9partement de Math\u00e9matiques et Statistique, , Montr\u00e9al ,","place":["Canada"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2624-7856","authenticated-orcid":false,"given":"Sylvain","family":"Gandon","sequence":"additional","affiliation":[{"name":"CEFE, CNRS, Univ Montpellier, EPHE, IRD , Montpellier ,","place":["France"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,7,31]]},"reference":[{"key":"2025100307191082800_bib1","doi-asserted-by":"publisher","first-page":"2452","DOI":"10.1038\/s41467-020-16282-w","article-title":"Large-scale network analysis captures biological features of bacterial plasmids","volume":"11","author":"Acman","year":"2020","journal-title":"Nature Communications"},{"key":"2025100307191082800_bib2","doi-asserted-by":"publisher","first-page":"20130031","DOI":"10.1098\/rsfs.2013.0031","article-title":"Co-infection and super-infection models in evolutionary epidemiology","volume":"3","author":"Alizon","year":"2013","journal-title":"Interface Focus"},{"key":"2025100307191082800_bib3","doi-asserted-by":"publisher","first-page":"921","DOI":"10.1111\/j.1558-5646.2012.01827.x","article-title":"Parasite co-transmission and the evolutionary epidemiology of virulence","volume":"67","author":"Alizon","year":"2013","journal-title":"Evolution"},{"key":"2025100307191082800_bib4","doi-asserted-by":"publisher","first-page":"11512","DOI":"10.1073\/pnas.0801925105","article-title":"Resistance, resilience, and redundancy in microbial communities","volume":"105","author":"Allison","year":"2008","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"2025100307191082800_bib5","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1038\/nrmicro2593","article-title":"Biased gene transfer in microbial evolution","volume":"12","author":"Andam","year":"2011","journal-title":"Nature Reviews Microbiology"},{"key":"2025100307191082800_bib6","doi-asserted-by":"publisher","first-page":"e3002796","DOI":"10.1371\/journal.pbio.3002796","article-title":"Hijackers, hitchhikers, or co-drivers? The mysteries of mobilizable genetic elements","volume":"22","author":"Ares-Arroyo","year":"2024","journal-title":"PLoS Biology"},{"key":"2025100307191082800_bib7","doi-asserted-by":"publisher","first-page":"e3000878","DOI":"10.1371\/journal.pbio.3000878","article-title":"Frequency-dependent selection can forecast evolution in Streptococcus pneumoniae","volume":"18","author":"Azarian","year":"2020","journal-title":"PLoS Biology"},{"key":"2025100307191082800_bib8","doi-asserted-by":"publisher","first-page":"489","DOI":"10.1016\/j.tree.2013.04.002","article-title":"Exploring the costs of horizontal gene transfer","volume":"28","author":"Baltrus","year":"2013","journal-title":"Trends in Ecology & Evolution"},{"key":"2025100307191082800_bib9","doi-asserted-by":"publisher","first-page":"e2212147120","DOI":"10.1073\/pnas.2212147120","article-title":"Host-specific plasmid evolution explains the variable spread of clinical antibiotic-resistance plasmids","volume":"120","author":"Benz","year":"2023","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"2025100307191082800_bib10","doi-asserted-by":"publisher","first-page":"1505","DOI":"10.1093\/genetics\/155.4.1505","article-title":"Natural selection, infectious transfer and the existence conditions for bacterial plasmids","volume":"155","author":"Bergstrom","year":"2000","journal-title":"Genetics"},{"key":"2025100307191082800_bib11","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1038\/s41579-019-0278-2","article-title":"The pan-immune system of bacteria: Antiviral defence as a community resource","volume":"18","author":"Bernheim","year":"2020","journal-title":"Nature Reviews Microbiology"},{"issue":"10","key":"2025100307191082800_bib12","doi-asserted-by":"crossref","first-page":"msae206","DOI":"10.1093\/molbev\/msae206","article-title":"Toxin-antitoxin systems reflect community interactions through horizontal gene transfer","volume":"41","author":"Bethke","year":"2024","journal-title":"Molecular Biology and Evolution"},{"key":"2025100307191082800_bib13","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1093\/genetics\/57.2.237","article-title":"Linkage and selection: Theoretical analysis of the deterministic two-locus random mating model","volume":"57","author":"Bodmer","year":"1967","journal-title":"Genetics"},{"key":"2025100307191082800_bib14","doi-asserted-by":"publisher","first-page":"442","DOI":"10.1038\/s41579-021-00534-7","article-title":"Examining horizontal gene transfer in microbial communities","volume":"19","author":"Brito","year":"2021","journal-title":"Nature Reviews Microbiology"},{"key":"2025100307191082800_bib15","doi-asserted-by":"publisher","first-page":"534","DOI":"10.1016\/j.tim.2021.11.001","article-title":"Ecological and evolutionary solutions to the plasmid paradox","volume":"30","author":"Brockhurst","year":"2022","journal-title":"Trends in Microbiology"},{"key":"2025100307191082800_bib16","doi-asserted-by":"crossref","first-page":"E105","DOI":"10.1086\/651587","article-title":"Mixed infections and the evolution of virulence: Effects of resource competition, parasite plasticity, and impaired host immunity","volume":"175","author":"Choisy","year":"2010","journal-title":"American Naturalist"},{"key":"2025100307191082800_bib17","doi-asserted-by":"publisher","first-page":"473","DOI":"10.1038\/s41564-019-0651-y","article-title":"Designing ecologically optimized pneumococcal vaccines using population genomics","volume":"5","author":"Colijn","year":"2020","journal-title":"Nature Microbiology"},{"key":"2025100307191082800_bib18","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1086\/285063","article-title":"The evolution of plasmids carrying multiple resistance genes: The role of segregation, transposition, and homologous recombination","volume":"135","author":"Condit","year":"1990","journal-title":"American Naturalist"},{"key":"2025100307191082800_bib19","doi-asserted-by":"publisher","first-page":"1950","DOI":"10.1038\/s41559-017-0337-x","article-title":"Frequency-dependent selection in vaccine-associated pneumococcal population dynamics","volume":"1","author":"Corander","year":"2017","journal-title":"Nature Ecology and Evolution"},{"issue":"11","key":"2025100307191082800_bib20","doi-asserted-by":"crossref","first-page":"e3001847","DOI":"10.1371\/journal.pbio.3001847","article-title":"Horizontal gene transfer and ecological interactions jointly control microbiome stability","volume":"20","author":"Coyte","year":"2022","journal-title":"PLOS Biology"},{"key":"2025100307191082800_bib21","first-page":"arXiv:2402.19388v1","article-title":"A model of pan-immunity maintenance by horizontal gene transfer in the ecological dynamics of bacteria and phages","author":"Cui","year":"2024","journal-title":"arXiv"},{"key":"2025100307191082800_bib22","doi-asserted-by":"crossref","first-page":"452","DOI":"10.1099\/mic.0.2006\/001784-0","article-title":"Stability of a promiscuous plasmid in different hosts: No guarantee for a long-term relationship","volume":"153","author":"De\u00a0Gelder","year":"2007","journal-title":"Microbiology"},{"key":"2025100307191082800_bib23","doi-asserted-by":"publisher","first-page":"1624","DOI":"10.1038\/s41559-021-01573-2","article-title":"Plasmids do not consistently stabilize cooperation across bacteria but may promote broad pathogen host-range","volume":"5","author":"Dewar","year":"2021","journal-title":"Nature of Ecology Evolution."},{"key":"2025100307191082800_bib24","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.plasmid.2019.01.003","article-title":"Interactions between plasmids and other mobile genetic elements affect their transmission and persistence","volume":"102","author":"Dionisio","year":"2019","journal-title":"Plasmid"},{"key":"2025100307191082800_bib25","first-page":"1","article-title":"Evolution in bacterial plasmids and levels of selection","volume":"65","author":"Eberhard","year":"1990","journal-title":"The Quartery Review of Biology"},{"key":"2025100307191082800_bib26","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1016\/j.plasmid.2017.08.004","article-title":"Co-resident plasmids travel together","volume":"93","author":"Gama","year":"2017","journal-title":"Plasmid"},{"key":"2025100307191082800_bib27","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1016\/j.plasmid.2017.08.003","article-title":"Conjugation efficiency depends on intra and intercellular interactions between distinct plasmids: Plasmids promote the immigration of other plasmids but repress co-colonizing plasmids","volume":"93","author":"Gama","year":"2017","journal-title":"Plasmid"},{"key":"2025100307191082800_bib28","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fmicb.2020.00001","article-title":"Plasmid interactions can improve plasmid persistence in bacterial populations","volume":"11","author":"Gama","year":"2020","journal-title":"Frontiers in Microbiology"},{"key":"2025100307191082800_bib29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.plasmid.2008.03.002","article-title":"Why is entry exclusion an essential feature of conjugative plasmids","volume":"60","author":"Garcillan-Barcia","year":"2008","journal-title":"Plasmid"},{"issue":"1","key":"2025100307191082800_bib30","doi-asserted-by":"publisher","first-page":"201","DOI":"10.1016\/j.biosystems.2007.09.003","article-title":"Rule-based modelling of conjugative plasmid transfer and incompatibility","volume":"91","author":"Gregory","year":"2008","journal-title":"Biosystems"},{"key":"2025100307191082800_bib31","doi-asserted-by":"publisher","first-page":"262","DOI":"10.1016\/j.tim.2012.04.003","article-title":"Plasmid-mediated horizontal gene transfer is a coevolutionary process","volume":"20","author":"Harrison","year":"2012","journal-title":"Trends in Microbiology"},{"key":"2025100307191082800_bib32","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1038\/s41396-020-00867-w","article-title":"Negative frequency-dependent selection and asymmetrical transformation stabilise multi-strain bacterial population structures","volume":"15","author":"Harrow","year":"2021","journal-title":"The ISME Journal"},{"key":"2025100307191082800_bib33","doi-asserted-by":"publisher","first-page":"226","DOI":"10.1007\/BF01245622","article-title":"Linkage disequilibrium in finite populations","volume":"38","author":"Hill","year":"1968","journal-title":"Theoretical and Applied Genetics"},{"key":"2025100307191082800_bib34","doi-asserted-by":"publisher","first-page":"102282","DOI":"10.1016\/j.mib.2023.102282","article-title":"How do interactions between mobile genetic elements affect horizontal gene transfer?","volume":"73","author":"Horne","year":"2023","journal-title":"Current Opinion in Microbiology"},{"key":"2025100307191082800_bib35","doi-asserted-by":"publisher","first-page":"20200478","DOI":"10.1098\/rstb.2020.0478","article-title":"Plasmid co-infection: Linking biological mechanisms to ecological and evolutionary dynamics","volume":"377","author":"Igler","year":"2021","journal-title":"Philosophical Transactions B"},{"key":"2025100307191082800_bib36","doi-asserted-by":"publisher","first-page":"e2414229121","DOI":"10.1073\/pnas.2414229121","article-title":"Bacterial defense and phage counterdefense lead to coexistence in a modeled ecosystem","volume":"121","author":"Kimchi","year":"2024","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"2025100307191082800_bib37","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1146\/annurev-micro-090816-093830","article-title":"Evolutionary genomics of defense systems in Archaea and Bacteria","volume":"71","author":"Koonin","year":"2017","journal-title":"Annual Review of Microbiology"},{"key":"2025100307191082800_bib38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1126\/science.abg2166","article-title":"Temporal shifts in antibiotic resistance elements govern phage-pathogen conflicts","volume":"373","author":"LeGault","year":"2021","journal-title":"Science"},{"key":"2025100307191082800_bib39","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1002\/evl3.226","article-title":"Evolutionary mechanisms that determine which bacterial genes are carried on plasmids","volume":"5","author":"Lehtinen","year":"2021","journal-title":"Evolution Letters"},{"key":"2025100307191082800_bib40","doi-asserted-by":"publisher","first-page":"425","DOI":"10.1093\/genetics\/94.2.425","article-title":"The population biology of bacterial plasmids: A priori conditions for the existence of mobilizable nonconjugative factors","volume":"94","author":"Levin","year":"1980","journal-title":"Genetics"},{"key":"2025100307191082800_bib41","first-page":"458","article-title":"The evolutionary dynamics of complex polymorphisms","volume":"14","author":"Lewontin","year":"1960","journal-title":"Evolution"},{"issue":"1","key":"2025100307191082800_bib42","doi-asserted-by":"publisher","first-page":"2","DOI":"10.1016\/j.epidem.2008.07.001","article-title":"No coexistence for free: Neutral null models for multistrain pathogens","volume":"1","author":"Lipsitch","year":"2009","journal-title":"Epidemics"},{"key":"2025100307191082800_bib43","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1111\/j.1558-5646.2010.01121.x","article-title":"Horizontal gene transfer and the evolution of bacterial cooperation","volume":"65","author":"McGinty","year":"2011","journal-title":"Evolution"},{"key":"2025100307191082800_bib44","doi-asserted-by":"publisher","first-page":"e2401578121","DOI":"10.1073\/pnas.2401578121","article-title":"A multilocus perspective on the evolutionary dynamics of multistrain pathogens","volume":"121","author":"McLeod","year":"2024","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"2025100307191082800_bib45","doi-asserted-by":"publisher","first-page":"20132173","DOI":"10.1098\/rspb.2013.2173","article-title":"Non-additive costs and interactions alter the competitive dynamics of co-occurring ecologically distinct plasmids","volume":"281","author":"Morton","year":"2014","journal-title":"Philosophical Transactions of the Royal Society B"},{"key":"2025100307191082800_bib46","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1093\/genetics\/75.1.213","article-title":"Linkage disequilibrium in subdivided populations","volume":"75","author":"Nei","year":"1973","journal-title":"Genetics"},{"key":"2025100307191082800_bib47","doi-asserted-by":"publisher","first-page":"1683","DOI":"10.1016\/j.cub.2009.08.056","article-title":"Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence","volume":"19","author":"Nogueira","year":"2009","journal-title":"Current Biology"},{"key":"2025100307191082800_bib48","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1128\/mr.51.4.381-395.1987","article-title":"Plasmid incompatibility","volume":"51","author":"Novick","year":"1987","journal-title":"Microbiology Reviews"},{"key":"2025100307191082800_bib49","doi-asserted-by":"publisher","first-page":"1721","DOI":"10.1093\/molbev\/msi167","article-title":"Mathematical modeling of evolution of horizontally transferred genes","volume":"22","author":"Novozhilov","year":"2005","journal-title":"Molecular Biology and Evolution"},{"key":"2025100307191082800_bib50","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1080\/2159256X.2015.1045115","article-title":"Evaluating the effect of horizontal transmission on the stability of plasmids under different selection regimes","volume":"5","author":"Pena-Miller","year":"2015","journal-title":"Mobile Genetic Elements"},{"key":"2025100307191082800_bib51","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/hdy.2010.24","article-title":"What traits are carried on mobile genetic elements, and why?","volume":"106","author":"Rankin","year":"2011","journal-title":"Heredity"},{"key":"2025100307191082800_bib52","doi-asserted-by":"publisher","first-page":"3602","DOI":"10.1038\/s41467-020-17278-2","article-title":"Pathways for horizontal gene transfer in bacteria revealed by a global map of their plasmids","volume":"11","author":"Redondo-Salvo","year":"2020","journal-title":"Nature Communications"},{"key":"2025100307191082800_bib53","doi-asserted-by":"publisher","first-page":"e3001514","DOI":"10.1371\/journal.pbio.3001514","article-title":"Microbial defenses against mobile genetic elements and viruses: Who defends whom from what?","volume":"20","author":"Rocha","year":"2022","journal-title":"PLoS Biology"},{"key":"2025100307191082800_bib54","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1038\/ismej.2013.182","article-title":"Positive epistasis between co-infecting plasmids promotes plasmid survival in bacterial populations","volume":"8","author":"San\u00a0Millan","year":"2014","journal-title":"The ISME Journal"},{"key":"2025100307191082800_bib55","first-page":"1","article-title":"Interactions between horizontally acquired genes create a fitness cost in Pseudomonas aeruginosa","volume":"6","author":"San\u00a0Millan","year":"2015","journal-title":"Nature Communications"},{"key":"2025100307191082800_bib56","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1093\/evlett\/qrad003","article-title":"Is cooperation favoured by horizontal gene transfer?","volume":"7","author":"Scott","year":"2023","journal-title":"Evolution Letters"},{"key":"2025100307191082800_bib57","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/molbev\/msad028","article-title":"Horizontal gene transfer, fitness costs and mobility shape the spread of antibiotic resistance genes in experimental populations of Acinetobacter Baylyi","volume":"40","author":"Sezmis","year":"2023","journal-title":"Molecular Biology and Evolution"},{"key":"2025100307191082800_bib58","doi-asserted-by":"publisher","first-page":"477","DOI":"10.1038\/nrg2361","article-title":"Linkage disequilibrium\u2014understanding the evolutionary past and mapping the medical future","volume":"9","author":"Slatkin","year":"2008","journal-title":"Nature Reviews Genetics"},{"key":"2025100307191082800_bib59","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1098\/rspb.2000.1330","article-title":"The social evolution of bacterial pathogenesis","volume":"268","author":"Smith","year":"2001","journal-title":"Philosophical Transactions of the Royal Society B"},{"key":"2025100307191082800_bib60","doi-asserted-by":"publisher","first-page":"472","DOI":"10.1038\/nrg3962","article-title":"Horizontal gene transfer: Building the web of life","volume":"16","author":"Soucy","year":"2015","journal-title":"Nature Reviews Genetics"},{"key":"2025100307191082800_bib61","doi-asserted-by":"publisher","first-page":"1930","DOI":"10.1038\/ismej.2017.42","article-title":"Gene mobility promotes the spread of resistance in bacterial populations","volume":"11","author":"Stevenson","year":"2017","journal-title":"The ISME Journal"},{"key":"2025100307191082800_bib62","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1093\/genetics\/87.2.209","article-title":"The population biology of bacterial plasmids: A priori conditions for the existence of conjugationally transmitted factors","volume":"87","author":"Stewart","year":"1977","journal-title":"Genetics"},{"key":"2025100307191082800_bib63","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1186\/1471-2148-11-130","article-title":"The evolution of plasmid-carried antibiotic resistance","volume":"11","author":"Svara","year":"2011","journal-title":"BMC Evolutionary Biology"},{"key":"2025100307191082800_bib64","first-page":"3079","article-title":"Why there are no essential genes on plasmids","volume":"32","author":"Tazzyman","year":"2014","journal-title":"Molecular Biology and Evolution"},{"key":"2025100307191082800_bib65","doi-asserted-by":"publisher","first-page":"2066","DOI":"10.1111\/evo.12423","article-title":"Plasmids and evolutionary rescue by drug resistance","volume":"68","author":"Tazzyman","year":"2014","journal-title":"Evolution"},{"key":"2025100307191082800_bib66","doi-asserted-by":"publisher","first-page":"309","DOI":"10.1093\/protein\/gzm005","article-title":"Plasmid incompatibility: More compatible than previously thought?","volume":"20","author":"Velappan","year":"2007","journal-title":"Protein Engineering, Design and Selection"},{"key":"2025100307191082800_bib67","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1016\/j.plasmid.2017.04.004","article-title":"Conjugative plasmids enable the maintenance of low cost non-transmissible plasmids","volume":"91","author":"Werisch","year":"2017","journal-title":"Plasmid"},{"key":"2025100307191082800_bib68","doi-asserted-by":"publisher","first-page":"26868","DOI":"10.1073\/pnas.2005331117","article-title":"Horizontal gene transfer potentiates adaptation by reducing selective constraints on the spread of genetic variation","volume":"117","author":"Woods","year":"2020","journal-title":"Proceedings of the National Academy of Sciences"}],"container-title":["Evolution Letters"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/evlett\/article-pdf\/9\/5\/576\/63898536\/qraf024.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/evlett\/article-pdf\/9\/5\/576\/63898536\/qraf024.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,3]],"date-time":"2025-10-03T11:19:22Z","timestamp":1759490362000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/evlett\/article\/9\/5\/576\/8219782"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,7,31]]},"references-count":68,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2025,7,31]]},"published-print":{"date-parts":[[2025,10,3]]}},"URL":"https:\/\/doi.org\/10.1093\/evlett\/qraf024","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2025.03.18.643975","asserted-by":"object"}]},"ISSN":["2056-3744"],"issn-type":[{"value":"2056-3744","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,10]]},"published":{"date-parts":[[2025,7,31]]}}}