{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,7]],"date-time":"2026-08-07T15:25:54Z","timestamp":1786116354358,"version":"build-2736575974"},"reference-count":63,"publisher":"Wiley","license":[{"start":{"date-parts":[[2026,8,6]],"date-time":"2026-08-06T00:00:00Z","timestamp":1785974400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2026,8,6]],"date-time":"2026-08-06T00:00:00Z","timestamp":1785974400000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/doi.wiley.com\/10.1002\/tdm_license_1.1"}],"funder":[{"DOI":"10.13039\/501100000266","name":"Engineering and Physical Sciences Research Council","doi-asserted-by":"publisher","award":["EP\/W523835\/1"],"award-info":[{"award-number":["EP\/W523835\/1"]}],"id":[{"id":"10.13039\/501100000266","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000288","name":"Royal Society","doi-asserted-by":"publisher","award":["211179\/Z\/18\/Z"],"award-info":[{"award-number":["211179\/Z\/18\/Z"]}],"id":[{"id":"10.13039\/501100000288","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000289","name":"Cancer Research UK","doi-asserted-by":"publisher","award":["DRCPFA\u2010Nov23\/100003"],"award-info":[{"award-number":["DRCPFA\u2010Nov23\/100003"]}],"id":[{"id":"10.13039\/501100000289","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100010269","name":"Wellcome Trust","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100010269","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000833","name":"Rosetrees Trust","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000833","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100014653","name":"Manchester Biomedical Research Centre","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100014653","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["advanced.onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Advanced Science"],"abstract":"<jats:title>ABSTRACT<\/jats:title>\n                  <jats:p>Computational simulations of tumor evolution are increasingly used to infer the rules underlying cancer growth. To make reliable inferences, such models must be able to reflect the properties of real tumors. Recent work has shown that lung tumors undergo frequent and late subclonal expansions, which are associated with poor prognosis. This paper tests three candidate simulations of three\u2010dimensional tumor growth, which make different assumptions about the nature of competition between cells, for their ability to replicate these late expansions. The study identifies a computationally\u2010efficient model which can produce multi\u2010region sequencing data realistic to lung tumors. This model assumes two distinct stages of growth, with the second stage involving local competition for space and resources within and between small tissue areas in a fixed\u2010size tumor. When inferring the model\u2010specific fitness effect of driver mutations in a large cohort of lung cancers, the study finds that inference pipelines based on a two\u2010stage model imply much larger selection effects than those based on single\u2010stage models, driven by model\u2010specific assumptions about the practical consequences of selection strength. This work emphasizes the importance of model assumptions to the results of tumor\u2010specific, simulation\u2010based inferences.<\/jats:p>","DOI":"10.1002\/advs.76764","type":"journal-article","created":{"date-parts":[[2026,8,6]],"date-time":"2026-08-06T09:20:03Z","timestamp":1786008003000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Agent\u2010Based Simulations of Lung Tumor Evolution Suggest That Ongoing Cell Competition Drives Realistic Clonal Expansions"],"prefix":"10.1002","author":[{"given":"Helena","family":"Coggan","sequence":"first","affiliation":[{"name":"Cancer Research UK Lung Cancer Centre of Excellence University College London Cancer Institute London UK"},{"name":"Computational Cancer Biology Research Group University College London Cancer Institute London UK"},{"name":"Department of Mathematics University College London London UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James R. M.","family":"Black","sequence":"additional","affiliation":[{"name":"Cancer Research UK Lung Cancer Centre of Excellence University College London Cancer Institute London UK"},{"name":"Cancer Genome Evolution Research Group University College London Cancer Institute London UK"},{"name":"Cancer Evolution and Genome Instability Laboratory the Francis Crick Institute London UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carlos","family":"Mart\u00ednez\u2010Ruiz","sequence":"additional","affiliation":[{"name":"Cancer Research UK Lung Cancer Centre of Excellence University College London Cancer Institute London UK"},{"name":"Cancer Genome Evolution Research Group University College London Cancer Institute London UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kristiana","family":"Grigoriadis","sequence":"additional","affiliation":[{"name":"Cancer Research UK Lung Cancer Centre of Excellence University College London Cancer Institute London UK"},{"name":"Cancer Genome Evolution Research Group University College London Cancer Institute London UK"},{"name":"Cancer Evolution and Genome Instability Laboratory the Francis Crick Institute London UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jasmin","family":"Fisher","sequence":"additional","affiliation":[{"name":"Computational Cancer Biology Research Group University College London Cancer Institute London UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9537-4045","authenticated-orcid":false,"given":"Nicholas","family":"McGranahan","sequence":"additional","affiliation":[{"name":"Cancer Research UK Lung Cancer Centre of Excellence University College London Cancer Institute London UK"},{"name":"Cancer Genome Evolution Research Group University College London Cancer Institute London UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2026,8,6]]},"reference":[{"key":"e_1_2_8_2_1","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1038\/s44222-023-00089-7","article-title":"Computational Approaches to Modelling and Optimizing Cancer Treatment","volume":"1","author":"McDonald T. O.","year":"2023","journal-title":"Nature Reviews Bioengineering"},{"issue":"5","key":"e_1_2_8_3_1","doi-asserted-by":"crossref","DOI":"10.1111\/eva.13687","article-title":"A Seven\u2010Step Guide to Spatial, Agent\u2010Based Modelling of Tumour Evolution","volume":"17","author":"Colyer B.","year":"2024","journal-title":"Evolutionary Applications"},{"key":"e_1_2_8_4_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0084654","article-title":"Dynamics Between Cancer Cell Subpopulations Reveals a Model Coordinating with Both Hierarchical and Stochastic Concepts","volume":"9","author":"Wang W.","year":"2014","journal-title":"PLoS ONE"},{"key":"e_1_2_8_5_1","doi-asserted-by":"crossref","first-page":"1995","DOI":"10.1038\/s41467-017-01516-1","article-title":"Spatial Competition Constrains Resistance to Targeted Cancer Therapy","volume":"8","author":"Bacevic K.","year":"2017","journal-title":"Nature Communications"},{"key":"e_1_2_8_6_1","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1186\/s12885-019-5597-1","article-title":"How Many Samples Are Needed to Infer Truly Clonal Mutations from Heterogenous Tumours?","volume":"19","author":"Opasic L.","year":"2019","journal-title":"BMC Cancer"},{"key":"e_1_2_8_7_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1007243","article-title":"Spatially Constrained Tumour Growth Affects the Patterns of Clonal Selection and Neutral Drift in Cancer Genomic Data","volume":"15","author":"Chkhaidze K.","year":"2019","journal-title":"PLoS Computational Biology"},{"key":"e_1_2_8_8_1","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1038\/s41551-021-00710-3","article-title":"Computational Modelling of Perivascular\u2010Niche Dynamics for the Optimization of Treatment Schedules for Glioblastoma","volume":"5","author":"Randles A.","year":"2021","journal-title":"Nature Biomedical Engineering"},{"key":"e_1_2_8_9_1","doi-asserted-by":"crossref","first-page":"744","DOI":"10.1038\/s41586-022-05311-x","article-title":"Phenotypic Plasticity and Genetic Control in Colorectal Cancer Evolution","volume":"611","author":"Househam J.","year":"2022","journal-title":"Nature"},{"key":"e_1_2_8_10_1","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1038\/s41559-021-01615-9","article-title":"Spatial Structure Governs the Mode of Tumour Evolution","volume":"6","author":"Noble R.","year":"2022","journal-title":"Nature Ecology and Evolution"},{"key":"e_1_2_8_11_1","doi-asserted-by":"crossref","first-page":"1015","DOI":"10.1038\/ng.3891","article-title":"Between\u2010Region Genetic Divergence Reflects the Mode and Tempo of Tumor Evolution","volume":"49","author":"Sun R.","year":"2017","journal-title":"Nature Genetics"},{"key":"e_1_2_8_12_1","doi-asserted-by":"crossref","first-page":"1113","DOI":"10.1038\/s41588-019-0423-x","article-title":"Quantitative Evidence for Early Metastatic Seeding in Colorectal Cancer","volume":"51","author":"Hu Z.","year":"2019","journal-title":"Nature Genetics"},{"key":"e_1_2_8_13_1","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1038\/s41588-020-0628-z","article-title":"Multi\u2010Cancer Analysis of Clonality and the Timing of Systemic Spread in Paired Primary Tumors and Metastases","volume":"52","author":"Hu Z.","year":"2020","journal-title":"Nature Genetics"},{"key":"e_1_2_8_14_1","doi-asserted-by":"crossref","first-page":"2060","DOI":"10.1038\/s41467-021-22123-1","article-title":"Normal Tissue Architecture Determines the Evolutionary Course of Cancer","volume":"12","author":"West J.","year":"2021","journal-title":"Nature Communications"},{"key":"e_1_2_8_15_1","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1186\/s12859-022-04779-8","article-title":"J\u2010Space: A Julia Package for the Simulation of Spatial Models of Cancer Evolution and of Sequencing Experiments","volume":"23","author":"Angaroni F.","year":"2022","journal-title":"BMC Bioinformatics"},{"key":"e_1_2_8_16_1","doi-asserted-by":"crossref","first-page":"1560","DOI":"10.1126\/science.1133755","article-title":"Five Rules for the Evolution of Cooperation","volume":"314","author":"Nowak M. A.","year":"2006","journal-title":"Science"},{"key":"e_1_2_8_17_1","doi-asserted-by":"crossref","DOI":"10.1103\/PhysRevLett.95.238701","article-title":"Coevolutionary Dynamics: From Finite to Infinite Populations","volume":"95","author":"Traulsen A.","year":"2005","journal-title":"Physical Review Letters"},{"key":"e_1_2_8_18_1","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1017\/S0305004100033193","article-title":"Random Processes in Genetics","volume":"54","author":"Moran P. A. P.","year":"1958","journal-title":"Mathematical Proceedings of the Cambridge Philosophical Society"},{"issue":"4","key":"e_1_2_8_19_1","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1093\/genetics\/49.4.561","article-title":"The Stepping Stone Model of Population Structure and the Decrease of Genetic Correlation with Distance","volume":"49","author":"Kimura M.","year":"1964","journal-title":"Genetics"},{"issue":"7","key":"e_1_2_8_20_1","doi-asserted-by":"crossref","first-page":"1573","DOI":"10.1007\/s11538-005-9046-8","article-title":"Spatial Stochastic Models for Cancer Initiation and Progression","volume":"68","author":"Komarova N. L.","year":"2006","journal-title":"Bulletin of Mathematical Biology"},{"issue":"3","key":"e_1_2_8_21_1","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1111\/j.1558-5646.1981.tb04911.x","article-title":"Fixation Probabilities and Fixation Times in a Subdivided Population","volume":"35","author":"Slatkin M.","year":"1981","journal-title":"Evolution"},{"issue":"1","key":"e_1_2_8_22_1","doi-asserted-by":"crossref","first-page":"104","DOI":"10.1214\/13-AAP989","article-title":"Spatial Moran Models I. Stochastic Tunneling in the Neutral Case","volume":"25","author":"Durrett R.","year":"2015","journal-title":"The Annals of Applied Probability"},{"issue":"5","key":"e_1_2_8_23_1","doi-asserted-by":"crossref","first-page":"1369","DOI":"10.1007\/s00285-015-0912-1","article-title":"Spatial Moran Models, II: Cancer Initiation in Spatially Structured Tissue","volume":"72","author":"Durrett R.","year":"2016","journal-title":"Journal of Mathematical Biology"},{"issue":"4","key":"e_1_2_8_24_1","doi-asserted-by":"crossref","DOI":"10.1098\/rsos.140465","article-title":"The Duality of Spatial Death\u2013Birth and Birth\u2013Death Processes and Limitations of the Isothermal Theorem","volume":"2","author":"Kaveh K.","year":"2015","journal-title":"Royal Society Open Science"},{"key":"e_1_2_8_25_1","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1143\/ptp\/88.6.1035","article-title":"Statistical Mechanics of Population: The Lattice Lotka\u2010Volterra Model","volume":"88","author":"Matsuda H.","year":"1992","journal-title":"Progress of Theoretical Physics"},{"key":"e_1_2_8_26_1","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1038\/nature03204","article-title":"Evolutionary Dynamics on Graphs","volume":"433","author":"Lieberman E.","year":"2005","journal-title":"Nature"},{"key":"e_1_2_8_27_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0054639","article-title":"Consolidating Birth\u2010Death and Death\u2010Birth Processes in Structured Populations","volume":"8","author":"Zukewich J.","year":"2013","journal-title":"PLoS ONE"},{"key":"e_1_2_8_28_1","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1038\/nature04605","article-title":"A Simple Rule for the Evolution of Cooperation on Graphs and Social Networks","volume":"441","author":"Ohtsuki H.","year":"2006","journal-title":"Nature"},{"key":"e_1_2_8_29_1","doi-asserted-by":"crossref","DOI":"10.1098\/rsif.2018.0918","article-title":"Evolution of Cooperation in an Epithelium","volume":"16","author":"Renton J.","year":"2019","journal-title":"Journal of The Royal Society Interface"},{"key":"e_1_2_8_30_1","doi-asserted-by":"crossref","DOI":"10.1016\/j.jtbi.2021.110838","article-title":"Cooperative Success in Epithelial Public Goods Games","volume":"528","author":"Renton J.","year":"2021","journal-title":"Journal of Theoretical Biology"},{"key":"e_1_2_8_31_1","doi-asserted-by":"crossref","DOI":"10.1098\/rsos.240413","article-title":"An Agent\u2010Based Modelling Framework to Study Growth Mechanisms in EGFR\u2010L858R Mutant Cell Alveolar Type II Cells","volume":"11","author":"Coggan H.","year":"2024","journal-title":"Royal Society Open Science"},{"key":"e_1_2_8_32_1","doi-asserted-by":"crossref","unstructured":"K. D.Siegmund P.Marjoram Y.\u2010J.Woo S.Tavar\u00e9 andD.Shibata \u201cInferring Clonal Expansion and Cancer Stem Cell Dynamics from DNA Methylation Patterns in Colorectal Cancers \u201dProceedings of the National Academy of Sciences of the United States of America106(March 2009): 4828\u201333.","DOI":"10.1073\/pnas.0810276106"},{"key":"e_1_2_8_33_1","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1038\/ng.3214","article-title":"A Big Bang Model of Human Colorectal Tumor Growth","volume":"47","author":"Sottoriva A.","year":"2015","journal-title":"Nature Genetics"},{"key":"e_1_2_8_34_1","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.jtbi.2014.05.027","article-title":"Ancestral Inference in Tumors: How Much Can We Know?","volume":"359","author":"Zhao J.","year":"2014","journal-title":"Journal of Theoretical Biology"},{"key":"e_1_2_8_35_1","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1038\/nature14971","article-title":"A Spatial Model Predicts That Dispersal and Cell Turnover Limit Intratumour Heterogeneity","volume":"525","author":"Waclaw B.","year":"2015","journal-title":"Nature"},{"key":"e_1_2_8_36_1","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1038\/s41588-018-0128-6","article-title":"Quantification of Subclonal Selection in Cancer from Bulk Sequencing Data","volume":"50","author":"Williams M. J.","year":"2018","journal-title":"Nature Genetics"},{"key":"e_1_2_8_37_1","doi-asserted-by":"crossref","DOI":"10.1093\/bioinformatics\/btad102","article-title":"SMITH: Spatially Constrained Stochastic Model for Simulation of Intra\u2010Tumour Heterogeneity","volume":"39","author":"Streck A.","year":"2023","journal-title":"Bioinformatics"},{"key":"e_1_2_8_38_1","doi-asserted-by":"crossref","DOI":"10.1002\/cso2.1033","article-title":"SITH: An R Package for Visualizing and Analyzing a Spatial Model of Intratumor Heterogeneity","volume":"2","author":"Nicol P. B.","year":"2022","journal-title":"Computational and Systems Oncology"},{"key":"e_1_2_8_39_1","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1186\/1742-4682-4-50","article-title":"Simulating Non\u2010Small Cell Lung Cancer with a Multiscale Agent\u2010Based Model","volume":"4","author":"Wang Z.","year":"2007","journal-title":"Theoretical Biology and Medical Modelling"},{"key":"e_1_2_8_40_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0184229","article-title":"Simulation Framework for Generating Intratumor Heterogeneity Patterns in a Cancer Cell Population","volume":"12","author":"Iwasaki W. M.","year":"2017","journal-title":"PLoS ONE"},{"key":"e_1_2_8_41_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1005991","article-title":"PhysiCell: An Open Source Physics\u2010Based Cell Simulator for 3\u2010D Multicellular Systems","volume":"14","author":"Ghaffarizadeh A.","year":"2018","journal-title":"PLOS Computational Biology"},{"key":"e_1_2_8_42_1","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.jtbi.2007.01.027","article-title":"An Evolutionary Hybrid Cellular Automaton Model of Solid Tumour Growth","volume":"246","author":"Gerlee P.","year":"2007","journal-title":"Journal of Theoretical Biology"},{"key":"e_1_2_8_43_1","doi-asserted-by":"crossref","first-page":"385","DOI":"10.3934\/mbe.2010.7.385","article-title":"Diffusion\u2010Limited Tumour Growth: Simulations and Analysis","volume":"7","author":"Gerlee P.","year":"2010","journal-title":"Mathematical Biosciences and Engineering"},{"key":"e_1_2_8_44_1","first-page":"209","article-title":"Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries","volume":"71","author":"Sung H.","year":"2021","journal-title":"CA: A Cancer Journal for Clinicians"},{"key":"e_1_2_8_45_1","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1016\/j.pulmoe.2020.02.005","article-title":"Conquering Lung Cancer: Current Status and Prospects for the Future","volume":"26","author":"Pirker R.","year":"2020","journal-title":"Pulmonology"},{"key":"e_1_2_8_46_1","doi-asserted-by":"crossref","first-page":"525","DOI":"10.1038\/s41586-023-05783-5","article-title":"The Evolution of Lung Cancer and Impact of Subclonal Selection in TRACERx","volume":"616","author":"Frankell A. M.","year":"2023","journal-title":"Nature"},{"issue":"12","key":"e_1_2_8_47_1","doi-asserted-by":"crossref","first-page":"1232","DOI":"10.1038\/s41567-020-0978-6","article-title":"Universal Scaling Laws Rule Explosive Growth in Human Cancers","volume":"16","author":"P\u00e9rez\u2010Garc\u00eda V. M.","year":"2020","journal-title":"Nature Physics"},{"issue":"2","key":"e_1_2_8_48_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1008266","article-title":"A Mesoscopic Simulator to Uncover Heterogeneity and Evolutionary Dynamics in Tumors","volume":"17","author":"Jim\u00e9nez\u2010S\u00e1nchez J.","year":"2021","journal-title":"PLOS Computational Biology"},{"issue":"7","key":"e_1_2_8_49_1","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pcbi.1010254","article-title":"Simulations of Tumor Growth and Response to Immunotherapy by Coupling a Spatial Agent\u2010Based Model with a Whole\u2010Patient Quantitative Systems Pharmacology Model","volume":"18","author":"Ruiz\u2010Martinez A.","year":"2022","journal-title":"PLOS Computational Biology"},{"issue":"3","key":"e_1_2_8_50_1","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1038\/s41580-022-00538-y","article-title":"Cell Competition in Development, Homeostasis and Cancer","volume":"24","author":"Van Neerven S. M.","year":"2023","journal-title":"Nature Reviews Molecular Cell Biology"},{"key":"e_1_2_8_51_1","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1038\/s41467-020-14844-6","article-title":"Measuring Single Cell Divisions in Human Tissues from Multi\u2010Region Sequencing Data","volume":"11","author":"Werner B.","year":"2020","journal-title":"Nature Communications"},{"key":"e_1_2_8_52_1","doi-asserted-by":"crossref","first-page":"14254","DOI":"10.1073\/pnas.0805217105","article-title":"The Infinite Sites Model of Genome Evolution","volume":"105","author":"Ma J.","year":"2008","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"e_1_2_8_53_1","doi-asserted-by":"crossref","first-page":"18545","DOI":"10.1073\/pnas.1010978107","article-title":"Accumulation of Driver and Passenger Mutations During Tumor Progression","volume":"107","author":"Bozic I.","year":"2010","journal-title":"Proceedings of the National Academy of Sciences"},{"key":"e_1_2_8_54_1","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1126\/science.aau3879","article-title":"Somatic Mutant Clones Colonize the Human Esophagus with Age","volume":"362","author":"Martincorena I.","year":"2018","journal-title":"Science"},{"issue":"1","key":"e_1_2_8_55_1","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/0360-3016(89)90020-5","article-title":"Response of Human Tumor Cell Lines In Vitro to Fractionated Irradiation","volume":"16","author":"Matthews J. H.","year":"1989","journal-title":"International Journal of Radiation Oncology, Biology, Physics"},{"key":"e_1_2_8_56_1","doi-asserted-by":"crossref","first-page":"764","DOI":"10.1126\/science.1199784","article-title":"Proteome Half\u2010Life Dynamics in Living Human Cells","volume":"331","author":"Eden E.","year":"2011","journal-title":"Science"},{"key":"e_1_2_8_57_1","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.48714","article-title":"Measuring the Distribution of Fitness Effects in Somatic Evolution by Combining Clonal Dynamics with dN\/dS Ratios","volume":"9","author":"Williams M. J.","year":"2020","journal-title":"eLife"},{"key":"e_1_2_8_58_1","doi-asserted-by":"crossref","first-page":"534","DOI":"10.1038\/s41586-023-05729-x","article-title":"The Evolution of Non\u2010Small Cell Lung Cancer Metastases in TRACERx","volume":"616","author":"Bakir M. A.","year":"2023","journal-title":"Nature"},{"key":"e_1_2_8_59_1","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1038\/s41586-019-1907-7","article-title":"The Evolutionary History of 2,658 Cancers","volume":"578","author":"Gerstung M.","year":"2020","journal-title":"Nature"},{"key":"e_1_2_8_60_1","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1056\/NEJMoa1113205","article-title":"Intratumor Heterogeneity and Branched Evolution Revealed by Multiregion Sequencing","volume":"366","author":"Gerlinger M.","year":"2012","journal-title":"New England Journal of Medicine"},{"key":"e_1_2_8_61_1","doi-asserted-by":"crossref","first-page":"2109","DOI":"10.1056\/NEJMoa1616288","article-title":"Tracking the Evolution of Non\u2013Small\u2010Cell Lung Cancer","volume":"376","author":"Jamal\u2010Hanjani M.","year":"2017","journal-title":"New England Journal of Medicine"},{"issue":"12","key":"e_1_2_8_62_1","doi-asserted-by":"crossref","first-page":"1620","DOI":"10.1038\/s41588-018-0217-6","article-title":"Currently Available Bulk Sequencing Data Do Not Necessarily Support a Model of Neutral Tumor Evolution","volume":"50","author":"McDonald T. O.","year":"2018","journal-title":"Nature Genetics"},{"key":"e_1_2_8_63_1","doi-asserted-by":"crossref","first-page":"594","DOI":"10.1038\/s41586-022-05425-2","article-title":"Spatial Genomics Maps the Structure, Nature and Evolution of Cancer Clones","volume":"611","author":"Lomakin A.","year":"2022","journal-title":"Nature"},{"key":"e_1_2_8_64_1","doi-asserted-by":"crossref","first-page":"103","DOI":"10.1038\/s41588-024-01989-z","article-title":"Characterizing the Evolutionary Dynamics of Cancer Proliferation in Single\u2010Cell Clones with SPRINTER","volume":"57","author":"Lucas O.","year":"2024","journal-title":"Nature Genetics"}],"container-title":["Advanced Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/advanced.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/advs.76764","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/advanced.onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/advs.76764","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/advanced.onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/advs.76764","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,6]],"date-time":"2026-08-06T09:20:13Z","timestamp":1786008013000},"score":1,"resource":{"primary":{"URL":"https:\/\/advanced.onlinelibrary.wiley.com\/doi\/10.1002\/advs.76764"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,8,6]]},"references-count":63,"alternative-id":["10.1002\/advs.76764"],"URL":"https:\/\/doi.org\/10.1002\/advs.76764","archive":["Portico"],"relation":{},"ISSN":["2198-3844","2198-3844"],"issn-type":[{"value":"2198-3844","type":"print"},{"value":"2198-3844","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,8,6]]},"assertion":[{"value":"2026-04-20","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-07-09","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2026-08-06","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e76764"}}