{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,27]],"date-time":"2026-10-27T23:58:04Z","timestamp":1793145484883,"version":"4.5.0"},"reference-count":58,"publisher":"The Royal Society","issue":"203","license":[{"start":{"date-parts":[[2025,8,14]],"date-time":"2025-08-14T00:00:00Z","timestamp":1755129600000},"content-version":"vor","delay-in-days":805,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2025,8,14]],"date-time":"2025-08-14T00:00:00Z","timestamp":1755129600000},"content-version":"vor","delay-in-days":805,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2025,8,14]],"date-time":"2025-08-14T00:00:00Z","timestamp":1755129600000},"content-version":"vor","delay-in-days":805,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2023,6,1]],"date-time":"2023-06-01T00:00:00Z","timestamp":1685577600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/royalsociety.org\/journals\/ethics-policies\/data-sharing-mining\/"}],"funder":[{"DOI":"10.13039\/501100001921","name":"Public Health Research Programme","doi-asserted-by":"crossref","award":["Health Protection Research Unit in Genomics and En"],"award-info":[{"award-number":["Health Protection Research Unit in Genomics and En"]}],"id":[{"id":"10.13039\/501100001921","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"crossref","award":["EP\/S022244\/1"],"award-info":[{"award-number":["EP\/S022244\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100001921","name":"Public Health Research Programme","doi-asserted-by":"crossref","award":["Health Protection Research Unit in Genomics and En"],"award-info":[{"award-number":["Health Protection Research Unit in Genomics and En"]}],"id":[{"id":"10.13039\/501100001921","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"crossref","award":["EP\/S022244\/1"],"award-info":[{"award-number":["EP\/S022244\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["royalsocietypublishing.org"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2023,6,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Increasing levels of antibiotic resistance in many bacterial pathogen populations are a major threat to public health. Resistance to an antibiotic provides a fitness benefit when the bacteria are exposed to this antibiotic, but resistance also often comes at a cost to the resistant pathogen relative to susceptible counterparts. We lack a good understanding of these benefits and costs of resistance for many bacterial pathogens and antibiotics, but estimating them could lead to better use of antibiotics in a way that reduces or prevents the spread of resistance. Here, we propose a new model for the joint epidemiology of susceptible and resistant variants, which includes explicit parameters for the cost and benefit of resistance. We show how Bayesian inference can be performed under this model using phylogenetic data from susceptible and resistant lineages and that by combining data from both we are able to disentangle and estimate the resistance cost and benefit parameters separately. We applied our inferential methodology to several simulated datasets to demonstrate good scalability and accuracy. We analysed a dataset of Neisseria gonorrhoeae genomes collected between 2000 and 2013 in the USA. We found that two unrelated lineages resistant to fluoroquinolones shared similar epidemic dynamics and resistance parameters. Fluoroquinolones were abandoned for the treatment of gonorrhoea due to increasing levels of resistance, but our results suggest that they could be used to treat a minority of around 10% of cases without causing resistance to grow again.<\/jats:p>","DOI":"10.1098\/rsif.2023.0074","type":"journal-article","created":{"date-parts":[[2023,6,14]],"date-time":"2023-06-14T03:00:45Z","timestamp":1686711645000},"update-policy":"https:\/\/doi.org\/10.1098\/crossmark-policy","source":"Crossref","is-referenced-by-count":26,"title":["Estimating the fitness cost and benefit of antimicrobial resistance from pathogen genomic data"],"prefix":"10.1098","volume":"20","author":[{"given":"David","family":"Helekal","sequence":"first","affiliation":[{"name":"Coventry, UK 1","department":["Centre for Doctoral Training in Mathematics for Real-World Systems, University of Warwick"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4639-4765","authenticated-orcid":true,"given":"Matt","family":"Keeling","sequence":"additional","affiliation":[{"name":"Coventry, UK 2","department":["Mathematics Institute and School of Life Sciences, University of Warwick"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5646-1314","authenticated-orcid":true,"given":"Yonatan H.","family":"Grad","sequence":"additional","affiliation":[{"name":"Boston, MA, USA 4","department":["Department of Immunology and Infectious Diseases, TH Chan School of Public Health, Harvard University"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1885-500X","authenticated-orcid":true,"given":"Xavier","family":"Didelot","sequence":"additional","affiliation":[{"name":"Coventry, UK 3","department":["School of Life Sciences and Department of Statistics, University of Warwick"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"175","published-online":{"date-parts":[[2023,6,14]]},"reference":[{"key":"2026010520265454000_RSIF20230074C1","volume-title":"Antibiotic resistance threats in the United States, 2013","author":"CDC","year":"2013"},{"key":"2026010520265454000_RSIF20230074C2","volume-title":"Tackling drug-resistant infections globally: final report and recommendations","author":"O\u2019Neill","year":"2016"},{"key":"2026010520265454000_RSIF20230074C3","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/S0140-6736(21)02724-0","article-title":"Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis","volume":"399","author":"Murray","year":"2022","journal-title":"Lancet"},{"key":"2026010520265454000_RSIF20230074C4","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1038\/nchembio.2007.24","article-title":"Targeting virulence: a new paradigm for antimicrobial therapy","volume":"3","author":"Clatworthy","year":"2007","journal-title":"Nat. Chem. Biol."},{"key":"2026010520265454000_RSIF20230074C5","doi-asserted-by":"crossref","first-page":"12 106","DOI":"10.1073\/pnas.94.22.12106","article-title":"Evaluating treatment protocols to prevent antibiotic resistance","volume":"94","author":"Bonhoeffer","year":"1997","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2026010520265454000_RSIF20230074C6","doi-asserted-by":"crossref","first-page":"1152","DOI":"10.1073\/pnas.96.3.1152","article-title":"The relationship between the volume of antimicrobial consumption in human communities and the frequency of resistance","volume":"96","author":"Austin","year":"1999","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2026010520265454000_RSIF20230074C7","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1093\/aje\/kwt017","article-title":"A modeling framework for the evolution and spread of antibiotic resistance: literature review and model categorization","volume":"178","author":"Spicknall","year":"2013","journal-title":"Am. J. Epidemiol."},{"key":"2026010520265454000_RSIF20230074C8","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/S1369-5274(99)00005-3","article-title":"The biological cost of antibiotic resistance","volume":"2","author":"Andersson","year":"1999","journal-title":"Curr. Opin. Microbiol."},{"key":"2026010520265454000_RSIF20230074C9","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1038\/nrmicro2319","article-title":"Antibiotic resistance and its cost: is it possible to reverse resistance?","volume":"8","author":"Andersson","year":"2010","journal-title":"Nat. Rev. Microbiol."},{"key":"2026010520265454000_RSIF20230074C10","doi-asserted-by":"crossref","first-page":"e1002416","DOI":"10.1371\/journal.pmed.1002416","article-title":"Estimating the fitness benefit and cost of cefixime resistance in Neisseria gonorrhoeae to inform prescription policy: a modelling study","volume":"14","author":"Whittles","year":"2017","journal-title":"PLoS Med."},{"key":"2026010520265454000_RSIF20230074C11","doi-asserted-by":"crossref","unstructured":"Rubin\n              DH\n            , MaKC, WesterveltKA, HullahalliK, WaldorMK, GradYH. 2022Variation in supplemental carbon dioxide requirements defines lineage-specific antibiotic resistance acquisition in Neisseria gonorrhoeae. bioRxiv. (doi:10.1101\/2022.02.24.481660)","DOI":"10.1101\/2022.02.24.481660"},{"key":"2026010520265454000_RSIF20230074C12","doi-asserted-by":"crossref","first-page":"e1007763","DOI":"10.1371\/journal.ppat.1007763","article-title":"On the evolutionary ecology of multidrug resistance in bacteria","volume":"15","author":"Lehtinen","year":"2019","journal-title":"PLoS Pathog."},{"key":"2026010520265454000_RSIF20230074C13","doi-asserted-by":"crossref","first-page":"540","DOI":"10.1038\/nrg2583","article-title":"Evolutionary analysis of the dynamics of viral infectious disease","volume":"10","author":"Pybus","year":"2009","journal-title":"Nat. Rev. Genet."},{"key":"2026010520265454000_RSIF20230074C14","doi-asserted-by":"crossref","first-page":"20140945","DOI":"10.1098\/rsif.2014.0945","article-title":"Sampling through time and phylodynamic inference with coalescent and birth? Death models","volume":"11","author":"Volz","year":"2014","journal-title":"J. R. Soc. Interface"},{"key":"2026010520265454000_RSIF20230074C15","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1093\/sysbio\/syy007","article-title":"Modeling the growth and decline of pathogen effective population size provides insight into epidemic dynamics and drivers of antimicrobial resistance","volume":"67","author":"Volz","year":"2018","journal-title":"Syst. Biol."},{"key":"2026010520265454000_RSIF20230074C16","doi-asserted-by":"crossref","first-page":"e1006895","DOI":"10.1371\/journal.ppat.1006895","article-title":"Quantifying the fitness cost of HIV-1 drug resistance mutations through phylodynamics","volume":"14","author":"K\u00fchnert","year":"2018","journal-title":"PLoS Pathog."},{"key":"2026010520265454000_RSIF20230074C17","doi-asserted-by":"crossref","first-page":"100471","DOI":"10.1016\/j.epidem.2021.100471","article-title":"Quantifying transmission fitness costs of multi-drug resistant tuberculosis","volume":"36","author":"Pecerska","year":"2021","journal-title":"Epidemics"},{"key":"2026010520265454000_RSIF20230074C18","doi-asserted-by":"crossref","first-page":"423","DOI":"10.1111\/j.1755-0998.2011.02988.x","article-title":"Skyline-plot methods for estimating demographic history from nucleotide sequences","volume":"11","author":"Ho","year":"2011","journal-title":"Mol. Ecol. Resourc."},{"key":"2026010520265454000_RSIF20230074C19","doi-asserted-by":"crossref","first-page":"1421","DOI":"10.1534\/genetics.109.106021","article-title":"Phylodynamics of infectious disease epidemics","volume":"183","author":"Volz","year":"2009","journal-title":"Genetics"},{"key":"2026010520265454000_RSIF20230074C20","doi-asserted-by":"crossref","first-page":"20120314","DOI":"10.1098\/rstb.2012.0314","article-title":"Coalescent inference for infectious disease: meta-analysis of hepatitis C","volume":"368","author":"Dearlove","year":"2013","journal-title":"Phil. Trans. R. Soc. B"},{"key":"2026010520265454000_RSIF20230074C21","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1038\/nrg3226","article-title":"Transforming clinical microbiology with bacterial genome sequencing","volume":"13","author":"Didelot","year":"2012","journal-title":"Nat. Rev. Genet."},{"key":"2026010520265454000_RSIF20230074C22","doi-asserted-by":"crossref","first-page":"vey016","DOI":"10.1093\/ve\/vey016","article-title":"Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10","volume":"4","author":"Suchard","year":"2018","journal-title":"Virus Evol."},{"key":"2026010520265454000_RSIF20230074C23","doi-asserted-by":"crossref","first-page":"e1006650","DOI":"10.1371\/journal.pcbi.1006650","article-title":"BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis","volume":"15","author":"Bouckaert","year":"2019","journal-title":"PLoS Comput. Biol."},{"key":"2026010520265454000_RSIF20230074C24","doi-asserted-by":"crossref","first-page":"e134","DOI":"10.1093\/nar\/gky783","article-title":"Bayesian inference of ancestral dates on bacterial phylogenetic trees","volume":"46","author":"Didelot","year":"2018","journal-title":"Nucleic Acids Res."},{"key":"2026010520265454000_RSIF20230074C25","doi-asserted-by":"crossref","first-page":"20210246","DOI":"10.1098\/rstb.2021.0246","article-title":"A scalable analytical approach from bacterial genomes to epidemiology","volume":"377","author":"Didelot","year":"2022","journal-title":"Phil. Trans. R. Soc. B"},{"key":"2026010520265454000_RSIF20230074C26","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1080\/10236190310001603680","article-title":"SIS epidemic models with multiple pathogen strains","volume":"10","author":"Allen","year":"2004","journal-title":"J. Differ. Equ. Appl."},{"key":"2026010520265454000_RSIF20230074C27","doi-asserted-by":"crossref","DOI":"10.1515\/9781400841035","volume-title":"Modeling infectious diseases in humans and animals","author":"Keeling","year":"2008"},{"key":"2026010520265454000_RSIF20230074C28","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1534\/genetics.111.134627","article-title":"Complex population dynamics and the coalescent under neutrality","volume":"190","author":"Volz","year":"2012","journal-title":"Genetics"},{"key":"2026010520265454000_RSIF20230074C29","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1098\/rstb.1994.0079","article-title":"Sampling theory for neutral alleles in a varying environment","volume":"344","author":"Griffiths","year":"1994","journal-title":"Phil. Trans. R. Soc. B"},{"key":"2026010520265454000_RSIF20230074C30","doi-asserted-by":"crossref","first-page":"713","DOI":"10.1093\/molbev\/mss265","article-title":"Improving Bayesian population dynamics inference: a coalescent-based model for multiple loci","volume":"30","author":"Gill","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"2026010520265454000_RSIF20230074C31","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/S0040-5809(03)00075-3","article-title":"The frequency spectrum of a mutation, and its age, in a general diffusion model","volume":"64","author":"Griffiths","year":"2003","journal-title":"Theor. Popul. Biol."},{"key":"2026010520265454000_RSIF20230074C32","doi-asserted-by":"crossref","first-page":"685","DOI":"10.1214\/105051606000000114","article-title":"An approximate sampling formula under genetic hitchhiking","volume":"16","author":"Etheridge","year":"2006","journal-title":"Ann. Appl. Probab."},{"key":"2026010520265454000_RSIF20230074C33","unstructured":"Rasmussen\n              CE\n            \n          . 2004Gaussian processes in machine learning, pp. 63\u201371. Berlin, Germany: Springer. (doi:10.1007\/978-3-540-28650-9_4)"},{"key":"2026010520265454000_RSIF20230074C34","doi-asserted-by":"crossref","unstructured":"Riutort-Mayol\n              G\n            , B\u00fcrknerP-C, AndersenMR, SolinA, VehtariA. 2022Practical Hilbert space approximate Bayesian Gaussian processes for probabilistic programming. (https:\/\/arxiv.org\/abs\/2004.11408)","DOI":"10.1007\/s11222-022-10167-2"},{"key":"2026010520265454000_RSIF20230074C35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v076.i01","article-title":"Stan: a probabilistic programming language","volume":"76","author":"Carpenter","year":"2017","journal-title":"J. Stat. Softw."},{"key":"2026010520265454000_RSIF20230074C36","first-page":"667","article-title":"Rank-normalization, folding, and localization: an improved R hat for assessing convergence of MCMC","volume":"16","author":"Vehtarh","year":"2021","journal-title":"Bayesian Anal."},{"key":"2026010520265454000_RSIF20230074C37","doi-asserted-by":"crossref","first-page":"1716","DOI":"10.1063\/1.1378322","article-title":"Approximate accelerated stochastic simulation of chemically reacting systems","volume":"115","author":"Gillespie","year":"2001","journal-title":"J. Chem. Phys."},{"key":"2026010520265454000_RSIF20230074C38","doi-asserted-by":"crossref","first-page":"1579","DOI":"10.1093\/infdis\/jiw420","article-title":"Genomic epidemiology of gonococcal resistance to extended spectrum Cephalosporins, Macrolides, and Fluoroquinolones in the US, 2000\u20132013","volume":"214","author":"Grad","year":"2016","journal-title":"J. Infect. Dis."},{"key":"2026010520265454000_RSIF20230074C39","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1093\/sysbio\/syq010","article-title":"New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0","volume":"59","author":"Guindon","year":"2010","journal-title":"Syst. Biol."},{"key":"2026010520265454000_RSIF20230074C40","doi-asserted-by":"crossref","first-page":"e1004041","DOI":"10.1371\/journal.pcbi.1004041","article-title":"ClonalFrameML: efficient inference of recombination in whole bacterial genomes","volume":"11","author":"Didelot","year":"2015","journal-title":"PLoS Comput. Biol."},{"key":"2026010520265454000_RSIF20230074C41","doi-asserted-by":"crossref","first-page":"884","DOI":"10.1093\/sysbio\/syaa009","article-title":"Identification of hidden population structure in time-scaled phylogenies","volume":"69","author":"Volz","year":"2020","journal-title":"Syst. Biol."},{"key":"2026010520265454000_RSIF20230074C42","first-page":"733","article-title":"Posterior predictive assessment of model fitness via realized discrepancies","volume":"6","author":"Gelman","year":"1996","journal-title":"Stat. Sinica"},{"key":"2026010520265454000_RSIF20230074C43","doi-asserted-by":"crossref","first-page":"e1005611","DOI":"10.1371\/journal.ppat.1005611","article-title":"Antibiotic-resistant Neisseria gonorrhoeae spread faster with more treatment, not more sexual partners","volume":"12","author":"Fingerhuth","year":"2016","journal-title":"PLoS Pathog."},{"key":"2026010520265454000_RSIF20230074C44","doi-asserted-by":"crossref","first-page":"e1006748","DOI":"10.1371\/journal.pcbi.1006748","article-title":"A dynamic power-law sexual network model of gonorrhoea outbreaks","volume":"15","author":"Whittles","year":"2019","journal-title":"PLoS Comput. Biol."},{"key":"2026010520265454000_RSIF20230074C45","doi-asserted-by":"crossref","first-page":"vex025","DOI":"10.1093\/ve\/vex025","article-title":"Scalable relaxed clock phylogenetic dating","volume":"3","author":"Volz","year":"2017","journal-title":"Virus Evol."},{"key":"2026010520265454000_RSIF20230074C46","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/S0169-5347(03)00216-7","article-title":"Measurably evolving populations","volume":"18","author":"Drummond","year":"2003","journal-title":"Trends Ecol. Evol."},{"key":"2026010520265454000_RSIF20230074C47","doi-asserted-by":"crossref","first-page":"306","DOI":"10.1016\/j.tree.2015.03.009","article-title":"Measurably evolving pathogens in the genomic era","volume":"30","author":"Biek","year":"2015","journal-title":"Trends Ecol. Evol."},{"key":"2026010520265454000_RSIF20230074C48","first-page":"e000094","article-title":"Genome-scale rates of evolutionary change in bacteria","volume":"2","author":"Duch\u00eane","year":"2016","journal-title":"Microbial Genom."},{"key":"2026010520265454000_RSIF20230074C49","doi-asserted-by":"crossref","first-page":"e019921","DOI":"10.1136\/bmjopen-2017-019921","article-title":"Openprescribing: normalised data and software tool to research trends in English NHS primary care prescribing 1998\u20132016","volume":"8","author":"Curtis","year":"2018","journal-title":"BMJ open"},{"key":"2026010520265454000_RSIF20230074C50","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s12976-018-0097-6","article-title":"Assessing parameter identifiability in compartmental dynamic models using a computational approach: application to infectious disease transmission models","volume":"16","author":"Roosa","year":"2019","journal-title":"Theor. Biol. Med. Modell."},{"key":"2026010520265454000_RSIF20230074C51","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1201\/9781315222912-13","volume-title":"Handbook of infectious disease data analysis","author":"Klinkenberg","year":"2019"},{"key":"2026010520265454000_RSIF20230074C52","doi-asserted-by":"crossref","first-page":"1501","DOI":"10.1093\/genetics\/146.4.1501","article-title":"Structured coalescent processes on different time scales","volume":"146","author":"Nordborg","year":"1997","journal-title":"Genetics"},{"key":"2026010520265454000_RSIF20230074C53","doi-asserted-by":"crossref","first-page":"1879","DOI":"10.1098\/rstb.2010.0060","article-title":"Viral phylodynamics and the search for an \u2018effective number of infections\u2019","volume":"365","author":"Frost","year":"2010","journal-title":"Phil. Trans. R. Soc. B"},{"key":"2026010520265454000_RSIF20230074C54","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/ve\/vex020","article-title":"Biased phylodynamic inferences from analysing clusters of viral sequences","volume":"3","author":"Dearlove","year":"2017","journal-title":"Virus Evol."},{"key":"2026010520265454000_RSIF20230074C55","first-page":"syab095","article-title":"Bayesian inference of clonal expansions in a dated phylogeny","volume":"71","author":"Helekal","year":"2021","journal-title":"Syst. Biol."},{"key":"2026010520265454000_RSIF20230074C56","doi-asserted-by":"crossref","first-page":"145","DOI":"10.3389\/fpubh.2014.00145","article-title":"The antimicrobial resistance crisis: causes, consequences, and management","volume":"2","author":"Michael","year":"2014","journal-title":"Front. Public Health"},{"key":"2026010520265454000_RSIF20230074C57","doi-asserted-by":"crossref","first-page":"176","DOI":"10.1016\/S0140-6736(15)00473-0","article-title":"Understanding the mechanisms and drivers of antimicrobial resistance","volume":"387","author":"Holmes","year":"2016","journal-title":"Lancet"},{"key":"2026010520265454000_RSIF20230074C58","author":"Helekal","year":"2023"}],"container-title":["Journal of the Royal Society Interface"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/royalsocietypublishing.org\/doi\/pdf\/10.1098\/rsif.2023.0074","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/doi\/full-xml\/10.1098\/rsif.2023.0074","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/royalsocietypublishing.org\/rsif\/article-pdf\/doi\/10.1098\/rsif.2023.0074\/476050\/rsif.2023.0074.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/royalsocietypublishing.org\/rsif\/article-pdf\/doi\/10.1098\/rsif.2023.0074\/476050\/rsif.2023.0074.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,6]],"date-time":"2026-01-06T01:27:04Z","timestamp":1767662824000},"score":1,"resource":{"primary":{"URL":"https:\/\/royalsocietypublishing.org\/rsif\/article\/20\/203\/20230074\/65041\/Estimating-the-fitness-cost-and-benefit-of"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,1]]},"references-count":58,"journal-issue":{"issue":"203","published-print":{"date-parts":[[2023,6,1]]}},"URL":"https:\/\/doi.org\/10.1098\/rsif.2023.0074","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2022.12.02.518824","asserted-by":"object"}]},"ISSN":["1742-5662"],"issn-type":[{"value":"1742-5662","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,1]]},"assertion":[{"value":"2023-02-15","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-05-22","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2023-06-14","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"20230074"}}