{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,25]],"date-time":"2025-10-25T19:08:15Z","timestamp":1761419295454,"version":"3.37.3"},"reference-count":90,"publisher":"Oxford University Press (OUP)","issue":"20","license":[{"start":{"date-parts":[[2019,3,14]],"date-time":"2019-03-14T00:00:00Z","timestamp":1552521600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100005242","name":"Universit\u00e9 de Montr\u00e9al","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100005242","id-type":"DOI","asserted-by":"publisher"}]},{"name":"Universit\u00e9 de Montr\u00e9al's Facult\u00e9 des \u00e9tudes sup\u00e9rieures et postdoctorales"},{"name":"ENSEIRB-MATMECA Bordeaux"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2019,10,15]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Motivation<\/jats:title>\n                  <jats:p>Protein evolution is determined by forces at multiple levels of biological organization. Random mutations have an immediate effect on the biophysical properties, structure and function of proteins. These same mutations also affect the fitness of the organism. However, the evolutionary fate of mutations, whether they succeed to fixation or are purged, also depends on population size and dynamics. There is an emerging interest, both theoretically and experimentally, to integrate these two factors in protein evolution. Although there are several tools available for simulating protein evolution, most of them focus on either the biophysical or the population-level determinants, but not both. Hence, there is a need for a publicly available computational tool to explore both the effects of protein biophysics and population dynamics on protein evolution.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>To address this need, we developed SodaPop, a computational suite to simulate protein evolution in the context of the population dynamics of asexual populations. SodaPop accepts as input several fitness landscapes based on protein biochemistry or other user-defined fitness functions. The user can also provide as input experimental fitness landscapes derived from deep mutational scanning approaches or theoretical landscapes derived from physical force field estimates. Here, we demonstrate the broad utility of SodaPop with different applications describing the interplay of selection for protein properties and population dynamics. SodaPop is designed such that population geneticists can explore the influence of protein biochemistry on patterns of genetic variation, and that biochemists and biophysicists can explore the role of population size and demography on protein evolution.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Availability and implementation<\/jats:title>\n                  <jats:p>Source code and binaries are freely available at https:\/\/github.com\/louisgt\/SodaPop under the GNU GPLv3 license. The software is implemented in C++ and supported on Linux, Mac OS\/X and Windows.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Supplementary information<\/jats:title>\n                  <jats:p>Supplementary data are available at Bioinformatics online.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/bioinformatics\/btz175","type":"journal-article","created":{"date-parts":[[2019,3,13]],"date-time":"2019-03-13T04:20:50Z","timestamp":1552450850000},"page":"4053-4062","source":"Crossref","is-referenced-by-count":7,"title":["SodaPop: a forward simulation suite for the evolutionary dynamics of asexual populations on protein fitness landscapes"],"prefix":"10.1093","volume":"35","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1009-068X","authenticated-orcid":false,"given":"Louis","family":"Gauthier","sequence":"first","affiliation":[{"name":"D\u00e9partement de Biochimie, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"},{"name":"Centre Robert-Cedergren en Bioinformatique et G\u00e9nomique, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}]},{"given":"R\u00e9micia","family":"Di Franco","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"},{"name":"Centre Robert-Cedergren en Bioinformatique et G\u00e9nomique, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"},{"name":"Enseirb-Matmeca, Bordeaux Institute of Technology , Talence, France"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8369-982X","authenticated-orcid":false,"given":"Adrian W R","family":"Serohijos","sequence":"additional","affiliation":[{"name":"D\u00e9partement de Biochimie, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"},{"name":"Centre Robert-Cedergren en Bioinformatique et G\u00e9nomique, Universit\u00e9 de Montr\u00e9al , Montr\u00e9al, QC, Canada"}]}],"member":"286","published-online":{"date-parts":[[2019,3,14]]},"reference":[{"key":"2023013108271786200_btz175-B1","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1016\/j.tibtech.2011.04.003","article-title":"Deep mutational scanning: assessing protein function on a massive scale","volume":"29","author":"Araya","year":"2011","journal-title":"Trends Biotechnol"},{"key":"2023013108271786200_btz175-B2","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1038\/nrg3564","article-title":"Genome dynamics during experimental evolution","volume":"14","author":"Barrick","year":"2013","journal-title":"Nat. Rev. Genet"},{"key":"2023013108271786200_btz175-B3","doi-asserted-by":"crossref","first-page":"1065","DOI":"10.1006\/jmbi.1993.1105","article-title":"Empirical and structural models for insertions and deletions in the divergent evolution of proteins","volume":"229","author":"Benner","year":"1993","journal-title":"J. Mol. Biol"},{"key":"2023013108271786200_btz175-B4","doi-asserted-by":"crossref","first-page":"929","DOI":"10.1038\/nature05385","article-title":"Robustness-epistasis link shapes the fitness landscape of a randomly drifting protein","volume":"444","author":"Bershtein","year":"2006","journal-title":"Nature"},{"key":"2023013108271786200_btz175-B5","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.sbi.2016.10.013","article-title":"Bridging the physical scales in evolutionary biology: from protein sequence space to fitness of organisms and populations","volume":"42","author":"Bershtein","year":"2017","journal-title":"Curr. Opin. Struct. Biol"},{"key":"2023013108271786200_btz175-B6","doi-asserted-by":"crossref","first-page":"1956","DOI":"10.1093\/molbev\/msu173","article-title":"An experimentally determined evolutionary model dramatically improves phylogenetic fit","volume":"31","author":"Bloom","year":"2014","journal-title":"Mol. Biol. Evol"},{"key":"2023013108271786200_btz175-B7","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1534\/genetics.106.061754","article-title":"Thermodynamics of neutral protein evolution","volume":"175","author":"Bloom","year":"2007","journal-title":"Genetics"},{"key":"2023013108271786200_btz175-B8","doi-asserted-by":"crossref","first-page":"417","DOI":"10.1016\/j.ygeno.2014.09.005","article-title":"Beyond genome sequencing: lineage tracking with barcodes to study the dynamics of evolution, infection, and cancer","volume":"104","author":"Blundell","year":"2014","journal-title":"Genomics"},{"key":"2023013108271786200_btz175-B9","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1038\/416507a","article-title":"Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases","volume":"416","author":"Bucciantini","year":"2002","journal-title":"Nature"},{"key":"2023013108271786200_btz175-B10","doi-asserted-by":"crossref","first-page":"155","DOI":"10.2174\/138920208784340759","article-title":"Simulation of genomes: a review","volume":"9","author":"Carvajal-Rodriguez","year":"2008","journal-title":"Curr. Genom"},{"key":"2023013108271786200_btz175-B11","doi-asserted-by":"crossref","first-page":"1332","DOI":"10.1002\/pro.2915","article-title":"Evolutionary dynamics of viral escape under antibodies stress: a biophysical model","volume":"25","author":"Cheron","year":"2016","journal-title":"Protein Sci"},{"key":"2023013108271786200_btz175-B12","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1146\/annurev.biochem.77.062906.171838","article-title":"Macromolecular modeling with rosetta","volume":"77","author":"Das","year":"2008","journal-title":"Annu. Rev. Biochem"},{"key":"2023013108271786200_btz175-B13","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1038\/nrg1672","article-title":"Missense meanderings in sequence space: a biophysical view of protein evolution","volume":"6","author":"DePristo","year":"2005","journal-title":"Nat. Rev. Genet"},{"key":"2023013108271786200_btz175-B14","doi-asserted-by":"crossref","first-page":"1898","DOI":"10.1093\/bioinformatics\/btx077","article-title":"Oncosimulr: genetic simulation with arbitrary epistasis and mutator genes in asexual populations","volume":"33","author":"Diaz-Uriarte","year":"2017","journal-title":"Bioinformatics"},{"key":"2023013108271786200_btz175-B15","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/j.cell.2008.05.042","article-title":"Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution","volume":"134","author":"Drummond","year":"2008","journal-title":"Cell"},{"key":"2023013108271786200_btz175-B16","doi-asserted-by":"crossref","first-page":"1432","DOI":"10.1126\/science.282.5393.1432","article-title":"Experimental evolution of parasites","volume":"282","author":"Ebert","year":"1998","journal-title":"Science"},{"key":"2023013108271786200_btz175-B17","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1146\/annurev-biophys-070816-033819","article-title":"Biophysical models of protein evolution: understanding the patterns of evolutionary sequence divergence","volume":"46","author":"Echave","year":"2017","journal-title":"Annu. Rev. Biophys"},{"key":"2023013108271786200_btz175-B18","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1534\/genetics.106.057570","article-title":"The distribution of fitness effects of new deleterious amino acid mutations in humans","volume":"173","author":"Eyre-Walker","year":"2006","journal-title":"Genetics"},{"key":"2023013108271786200_btz175-B19","doi-asserted-by":"crossref","first-page":"1581","DOI":"10.1093\/molbev\/msu081","article-title":"A comprehensive, high-resolution map of a gene\u2019s fitness landscape","volume":"31","author":"Firnberg","year":"2014","journal-title":"Mol. Biol. Evol"},{"key":"2023013108271786200_btz175-B20","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1007\/BF02459576","article-title":"On the dominance ratio. 1922","volume":"52","author":"Fisher","year":"1990","journal-title":"Bull. Math. Biol"},{"key":"2023013108271786200_btz175-B21","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1038\/nmeth.3027","article-title":"Deep mutational scanning: a new style of protein science","volume":"11","author":"Fowler","year":"2014","journal-title":"Nat. Methods"},{"key":"2023013108271786200_btz175-B22","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1073\/pnas.1017570108","article-title":"Misfolded proteins impose a dosage-dependent fitness cost and trigger a cytosolic unfolded protein response in yeast","volume":"108","author":"Geiler-Samerotte","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023013108271786200_btz175-B23","doi-asserted-by":"crossref","first-page":"2610","DOI":"10.1182\/blood-2009-06-229757","article-title":"Cellular barcoding tool for clonal analysis in the hematopoietic system","volume":"115","author":"Gerrits","year":"2010","journal-title":"Blood"},{"key":"2023013108271786200_btz175-B24","doi-asserted-by":"crossref","first-page":"1396","DOI":"10.1002\/prot.22964","article-title":"The evolution and evolutionary consequences of marginal thermostability in proteins","volume":"79","author":"Goldstein","year":"2011","journal-title":"Proteins"},{"key":"2023013108271786200_btz175-B25","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1016\/j.cels.2017.11.003","article-title":"Quantitative missense variant effect prediction using large-scale mutagenesis data","volume":"6","author":"Gray","year":"2018","journal-title":"Cell Systems"},{"key":"2023013108271786200_btz175-B26","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1016\/S0022-2836(02)00442-4","article-title":"Predicting changes in the stability of proteins and protein complexes: a study of more than 1000 mutations","volume":"320","author":"Guerois","year":"2002","journal-title":"J. Mol. Biol"},{"key":"2023013108271786200_btz175-B27","doi-asserted-by":"crossref","first-page":"e1002158.","DOI":"10.1371\/journal.ppat.1002158","article-title":"Selection of resistant bacteria at very low antibiotic concentrations","volume":"7","author":"Gullberg","year":"2011","journal-title":"PLoS Pathog"},{"key":"2023013108271786200_btz175-B28","doi-asserted-by":"crossref","first-page":"910","DOI":"10.1093\/oxfordjournals.molbev.a025995","article-title":"Evolutionary distances for protein-coding sequences: modeling site-specific residue frequencies","volume":"15","author":"Halpern","year":"1998","journal-title":"Mol. Biol. Evol"},{"key":"2023013108271786200_btz175-B29","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1038\/nrg3540","article-title":"Evolutionary biochemistry: revealing the historical and physical causes of protein properties","volume":"14","author":"Harms","year":"2013","journal-title":"Nat. Rev. Genet"},{"key":"2023013108271786200_btz175-B30","doi-asserted-by":"crossref","first-page":"5270.","DOI":"10.1038\/s41467-018-07649-1","article-title":"Modeling genome-wide enzyme evolution predicts strong epistasis underlying catalytic turnover rates","volume":"9","author":"Heckmann","year":"2018","journal-title":"Nat. Commun"},{"key":"2023013108271786200_btz175-B31","doi-asserted-by":"crossref","first-page":"1615","DOI":"10.1126\/science.1122469","article-title":"An equivalence principle for the incorporation of favorable mutations in asexual populations","volume":"311","author":"Hegreness","year":"2006","journal-title":"Science"},{"key":"2023013108271786200_btz175-B32","doi-asserted-by":"crossref","first-page":"4258","DOI":"10.1073\/pnas.1009392108","article-title":"Topology of protein interaction network shapes protein abundances and strengths of their functional and nonspecific interactions","volume":"108","author":"Heo","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023013108271786200_btz175-B33","doi-asserted-by":"crossref","first-page":"2786","DOI":"10.1093\/bioinformatics\/btn522","article-title":"A flexible forward simulator for populations subject to selection and demography","volume":"24","author":"Hernandez","year":"2008","journal-title":"Bioinformatics"},{"key":"2023013108271786200_btz175-B90","doi-asserted-by":"crossref","first-page":"110 EP.","DOI":"10.1038\/nrg3130","article-title":"Computer simulations: tools for population and evolutionary genetics","volume":"13","author":"Hoban","year":"2012","journal-title":"Nat. Rev. Genet."},{"key":"2023013108271786200_btz175-B34","doi-asserted-by":"crossref","first-page":"293.","DOI":"10.1186\/1471-2105-9-293","article-title":"Indel pdb: a database of structural insertions and deletions derived from sequence alignments of closely related proteins","volume":"9","author":"Hsing","year":"2008","journal-title":"BMC Bioinformatics"},{"key":"2023013108271786200_btz175-B35","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1093\/bioinformatics\/btr722","article-title":"A method to infer positive selection from marker dynamics in an asexual population","volume":"28","author":"Illingworth","year":"2012","journal-title":"Bioinformatics"},{"key":"2023013108271786200_btz175-B36","doi-asserted-by":"crossref","first-page":"e0138022.","DOI":"10.1371\/journal.pone.0138022","article-title":"Structure based thermostability prediction models for protein single point mutations with machine learning tools","volume":"10","author":"Jia","year":"2015","journal-title":"PLoS One"},{"key":"2023013108271786200_btz175-B37","doi-asserted-by":"crossref","first-page":"576","DOI":"10.1093\/bioinformatics\/btt712","article-title":"Forqs: forward-in-time simulation of recombination, quantitative traits and selection","volume":"30","author":"Kessner","year":"2014","journal-title":"Bioinformatics"},{"key":"2023013108271786200_btz175-B38","doi-asserted-by":"crossref","first-page":"D204","DOI":"10.1093\/nar\/gkj103","article-title":"Protherm and pronit: thermodynamic databases for proteins and protein-nucleic acid interactions","volume":"34","author":"Kumar","year":"2006","journal-title":"Nucleic Acids Res"},{"key":"2023013108271786200_btz175-B39","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1186\/s12859-015-0548-6","article-title":"Maestro\u2014multi agent stability prediction upon point mutations","volume":"16","author":"Laimer","year":"2015","journal-title":"Bmc Bioinformatics"},{"key":"2023013108271786200_btz175-B40","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.1093\/molbev\/msh112","article-title":"A Bayesian mixture model for across-site heterogeneities in the amino-acid replacement process","volume":"21","author":"Lartillot","year":"2004","journal-title":"Mol. Biol. Evol"},{"key":"2023013108271786200_btz175-B41","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1038\/nature14279","article-title":"Quantitative evolutionary dynamics using high-resolution lineage tracking","volume":"519","author":"Levy","year":"2015","journal-title":"Nature"},{"key":"2023013108271786200_btz175-B42","doi-asserted-by":"crossref","first-page":"769","DOI":"10.1002\/pro.2071","article-title":"The interface of protein structure, protein biophysics, and molecular evolution","volume":"21","author":"Liberles","year":"2012","journal-title":"Protein Sci"},{"key":"2023013108271786200_btz175-B43","doi-asserted-by":"crossref","first-page":"1797","DOI":"10.1073\/pnas.1415895112","article-title":"Protein folding and binding can emerge as evolutionary spandrels through structural coupling","volume":"112","author":"Manhart","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023013108271786200_btz175-B44","doi-asserted-by":"crossref","first-page":"1072.","DOI":"10.1038\/nbt.2419","article-title":"Protein structure prediction from sequence variation","volume":"30","author":"Marks","year":"2012","journal-title":"Nat. Biotechnol"},{"key":"2023013108271786200_btz175-B45","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1016\/0022-2836(92)90387-Y","article-title":"Effect of active site residues in barnase on activity and stability","volume":"225","author":"Meiering","year":"1992","journal-title":"J. Mol. Biol"},{"key":"2023013108271786200_btz175-B46","doi-asserted-by":"crossref","first-page":"1037","DOI":"10.1534\/genetics.113.152181","article-title":"Slim: simulating evolution with selection and linkage","volume":"194","author":"Messer","year":"2013","journal-title":"Genetics"},{"key":"2023013108271786200_btz175-B47","doi-asserted-by":"crossref","first-page":"794","DOI":"10.1093\/gbe\/evt045","article-title":"An abc method for estimating the rate and distribution of effects of beneficial mutations","volume":"5","author":"Moura de Sousa","year":"2013","journal-title":"Genome Biol. Evol"},{"key":"2023013108271786200_btz175-B48","doi-asserted-by":"crossref","first-page":"1552","DOI":"10.1093\/bioinformatics\/btn219","article-title":"Quantinemo: an individual-based program to simulate quantitative traits with explicit genetic architecture in a dynamic metapopulation","volume":"24","author":"Neuenschwander","year":"2008","journal-title":"Bioinformatics"},{"key":"2023013108271786200_btz175-B49","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1093\/molbev\/msg147","article-title":"Estimating the distribution of selection coefficients from phylogenetic data with applications to mitochondrial and viral dna","volume":"20","author":"Nielsen","year":"2003","journal-title":"Mol. Biol. Evol"},{"key":"2023013108271786200_btz175-B50","doi-asserted-by":"crossref","first-page":"2417","DOI":"10.1534\/genetics.107.085332","article-title":"Exploring population genetic models with recombination using efficient forward-time simulations","volume":"178","author":"Padhukasahasram","year":"2008","journal-title":"Genetics"},{"key":"2023013108271786200_btz175-B51","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1016\/0022-2836(92)91008-D","article-title":"Analysis of insertions\/deletions in protein structures","volume":"224","author":"Pascarella","year":"1992","journal-title":"J. Mol. Biol"},{"key":"2023013108271786200_btz175-B52","doi-asserted-by":"crossref","first-page":"3686","DOI":"10.1093\/bioinformatics\/bti584","article-title":"Simupop: a forward-time population genetics simulation environment","volume":"21","author":"Peng","year":"2005","journal-title":"Bioinformatics"},{"key":"2023013108271786200_btz175-B53","doi-asserted-by":"crossref","first-page":"2135","DOI":"10.1534\/genetics.107.075697","article-title":"Analytical description of mutational effects in competing asexual populations","volume":"177","author":"Pinkel","year":"2007","journal-title":"Genetics"},{"key":"2023013108271786200_btz175-B54","doi-asserted-by":"crossref","first-page":"665","DOI":"10.1016\/0022-2836(74)90188-0","article-title":"A thermodynamic approach to the problem of stabilization of globular protein structure: a calorimetric study","volume":"86","author":"Privalov","year":"1974","journal-title":"J. Mol. Biol"},{"key":"2023013108271786200_btz175-B55","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1534\/genetics.111.128025","article-title":"The relationship between relative solvent accessibility and evolutionary rate in protein evolution","volume":"188","author":"Ramsey","year":"2011","journal-title":"Genetics"},{"key":"2023013108271786200_btz175-B56","doi-asserted-by":"crossref","first-page":"4629","DOI":"10.1073\/pnas.0910915107","article-title":"Mutation-selection models of coding sequence evolution with site-heterogeneous amino acid fitness profiles","volume":"107","author":"Rodrigue","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023013108271786200_btz175-B57","doi-asserted-by":"crossref","first-page":"866","DOI":"10.1038\/nrm2805","article-title":"Exploring protein fitness landscapes by directed evolution","volume":"10","author":"Romero","year":"2009","journal-title":"Nat. Rev. Mol. Cell Biol"},{"key":"2023013108271786200_btz175-B58","doi-asserted-by":"crossref","first-page":"2390","DOI":"10.1093\/molbev\/msy131","article-title":"Evolution on the biophysical fitness landscape of an rna virus","volume":"35","author":"Rotem","year":"2018","journal-title":"Mol. Biol. Evol"},{"key":"2023013108271786200_btz175-B59","doi-asserted-by":"crossref","first-page":"12773","DOI":"10.1073\/pnas.1712999114","article-title":"Adaptive benefits from small mutation supplies in an antibiotic resistance enzyme","volume":"114","author":"Salverda","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023013108271786200_btz175-B60","doi-asserted-by":"crossref","first-page":"179.","DOI":"10.1186\/1471-2148-12-179","article-title":"Modeling coding-sequence evolution within the context of residue solvent accessibility","volume":"12","author":"Scherrer","year":"2012","journal-title":"BMC Evol. Biol"},{"key":"2023013108271786200_btz175-B61","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1093\/molbev\/mst189","article-title":"Contribution of selection for protein folding stability in shaping the patterns of polymorphisms in coding regions","volume":"31","author":"Serohijos","year":"2014","journal-title":"Mol. Biol. Evol"},{"key":"2023013108271786200_btz175-B62","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/j.sbi.2014.05.005","article-title":"Merging molecular mechanism and evolution: theory and computation at the interface of biophysics and evolutionary population genetics","volume":"26","author":"Serohijos","year":"2014","journal-title":"Curr. Opin. Struct. Biol"},{"key":"2023013108271786200_btz175-B63","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/j.celrep.2012.06.022","article-title":"Protein biophysics explains why highly abundant proteins evolve slowly","volume":"2","author":"Serohijos","year":"2012","journal-title":"Cell Rep"},{"key":"2023013108271786200_btz175-B64","doi-asserted-by":"crossref","first-page":"L1","DOI":"10.1016\/j.bpj.2012.11.3838","article-title":"Highly abundant proteins favor more stable 3d structures in yeast","volume":"104","author":"Serohijos","year":"2013","journal-title":"Biophys. J"},{"key":"2023013108271786200_btz175-B65","doi-asserted-by":"crossref","first-page":"1559","DOI":"10.1021\/cr040425u","article-title":"Protein folding thermodynamics and dynamics: where physics, chemistry, and biology meet","volume":"106","author":"Shakhnovich","year":"2006","journal-title":"Chem Rev"},{"key":"2023013108271786200_btz175-B66","doi-asserted-by":"crossref","first-page":"7195","DOI":"10.1073\/pnas.90.15.7195","article-title":"Engineering of stable and fast-folding sequences of model proteins","volume":"90","author":"Shakhnovich","year":"1993","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023013108271786200_btz175-B67","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1002\/j.1538-7305.1948.tb01338.x","article-title":"A mathematical theory of communication","volume":"27","author":"Shannon","year":"1948","journal-title":"Bell Syst. Tech. J"},{"key":"2023013108271786200_btz175-B68","doi-asserted-by":"crossref","first-page":"e94.","DOI":"10.1371\/journal.pbio.0050094","article-title":"Understanding the evolutionary fate of finite populations: the dynamics of mutational effects","volume":"5","author":"Silander","year":"2007","journal-title":"PLoS Biol"},{"key":"2023013108271786200_btz175-B69","doi-asserted-by":"crossref","first-page":"W8","DOI":"10.1093\/nar\/gkt427","article-title":"Mistic: mutual information server to infer coevolution","volume":"41","author":"Simonetti","year":"2013","journal-title":"Nucleic Acids Res"},{"key":"2023013108271786200_btz175-B70","doi-asserted-by":"crossref","first-page":"678","DOI":"10.1007\/s00109-003-0464-5","article-title":"Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution","volume":"81","author":"Stefani","year":"2003","journal-title":"J. Mol. Med. (Berl)"},{"key":"2023013108271786200_btz175-B71","doi-asserted-by":"crossref","first-page":"294","DOI":"10.1093\/bioinformatics\/btw606","article-title":"Geneevolve: a fast and memory efficient forward-time simulator of realistic whole-genome sequence and snp data","volume":"33","author":"Tahmasbi","year":"2017","journal-title":"Bioinformatics"},{"key":"2023013108271786200_btz175-B72","doi-asserted-by":"crossref","first-page":"1101","DOI":"10.1534\/genetics.111.136432","article-title":"Estimating the distribution of selection coefficients from phylogenetic data using sitewise mutation-selection models","volume":"190","author":"Tamuri","year":"2012","journal-title":"Genetics"},{"key":"2023013108271786200_btz175-B73","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/(SICI)1097-0282(200001)53:1<1::AID-BIP1>3.0.CO;2-X","article-title":"The distribution of structures in evolving protein populations","volume":"53","author":"Taverna","year":"2000","journal-title":"Biopolymers"},{"key":"2023013108271786200_btz175-B74","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1002\/prot.10016","article-title":"Why are proteins marginally stable?","volume":"46","author":"Taverna","year":"2002","journal-title":"Proteins"},{"key":"2023013108271786200_btz175-B75","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1534\/genetics.114.165019","article-title":"A c++ template library for efficient forward-time population genetic simulation of large populations","volume":"198","author":"Thornton","year":"2014","journal-title":"Genetics"},{"key":"2023013108271786200_btz175-B76","doi-asserted-by":"crossref","first-page":"1318","DOI":"10.1016\/j.jmb.2007.03.069","article-title":"The stability effects of protein mutations appear to be universally distributed","volume":"369","author":"Tokuriki","year":"2007","journal-title":"J. Mol. Biol"},{"key":"2023013108271786200_btz175-B77","doi-asserted-by":"crossref","first-page":"1585","DOI":"10.1016\/j.cell.2016.08.002","article-title":"Development of a comprehensive genotype-to-fitness map of adaptation-driving mutations in yeast","volume":"166","author":"Venkataram","year":"2016","journal-title":"Cell"},{"key":"2023013108271786200_btz175-B78","first-page":"553","article-title":"Protein building blocks preserved by recombination","volume":"9","author":"Voigt","year":"2002","journal-title":"Nat. Struct. Biol"},{"key":"2023013108271786200_btz175-B79","doi-asserted-by":"crossref","first-page":"D358","DOI":"10.1093\/nar\/gks1116","article-title":"Orthodb: a hierarchical catalog of animal, fungal and bacterial orthologs","volume":"41","author":"Waterhouse","year":"2013","journal-title":"Nucleic Acids Res"},{"key":"2023013108271786200_btz175-B80","doi-asserted-by":"crossref","first-page":"7273","DOI":"10.1073\/pnas.0901808106","article-title":"The universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages","volume":"106","author":"Wolf","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023013108271786200_btz175-B81","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.sbi.2016.11.001","article-title":"Deep sequencing methods for protein engineering and design","volume":"45","author":"Wrenbeck","year":"2017","journal-title":"Curr. Opin. Struct. Biol"},{"key":"2023013108271786200_btz175-B82","doi-asserted-by":"crossref","first-page":"15695.","DOI":"10.1038\/ncomms15695","article-title":"Single-mutation fitness landscapes for an enzyme on multiple substrates reveal specificity is globally encoded","volume":"8","author":"Wrenbeck","year":"2017","journal-title":"Nat. Commun"},{"key":"2023013108271786200_btz175-B83","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1093\/genetics\/16.2.97","article-title":"Evolution in mendelian populations","volume":"16","author":"Wright","year":"1931","journal-title":"Genetics"},{"key":"2023013108271786200_btz175-B84","doi-asserted-by":"crossref","first-page":"9916","DOI":"10.1073\/pnas.1017572108","article-title":"A biophysical protein folding model accounts for most mutational fitness effects in viruses","volume":"108","author":"Wylie","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023013108271786200_btz175-B85","doi-asserted-by":"crossref","first-page":"908","DOI":"10.1093\/oxfordjournals.molbev.a004148","article-title":"Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages","volume":"19","author":"Yang","year":"2002","journal-title":"Mol. Biol. Evol"},{"key":"2023013108271786200_btz175-B86","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1038\/nmeth0607-466","article-title":"Eris: an automated estimator of protein stability","volume":"4","author":"Yin","year":"2007","journal-title":"Nat. Methods"},{"key":"2023013108271786200_btz175-B87","doi-asserted-by":"crossref","first-page":"3332","DOI":"10.1093\/bioinformatics\/bts633","article-title":"Ffpopsim: an efficient forward simulation package for the evolution of large populations","volume":"28","author":"Zanini","year":"2012","journal-title":"Bioinformatics"},{"key":"2023013108271786200_btz175-B88","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1038\/msb.2008.48","article-title":"Constraints imposed by non-functional protein-protein interactions on gene expression and proteome size","volume":"4","author":"Zhang","year":"2008","journal-title":"Mol. Syst. Biol"},{"key":"2023013108271786200_btz175-B89","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1016\/j.tpb.2011.11.005","article-title":"Estimation of the rate and effect of new beneficial mutations in asexual populations","volume":"81","author":"Zhang","year":"2012","journal-title":"Theor. Population Biol"}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/bioinformatics\/advance-article-pdf\/doi\/10.1093\/bioinformatics\/btz175\/28531719\/btz175.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/35\/20\/4053\/48975878\/bioinformatics_35_20_4053.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/35\/20\/4053\/48975878\/bioinformatics_35_20_4053.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,31]],"date-time":"2023-01-31T17:16:13Z","timestamp":1675185373000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/35\/20\/4053\/5380769"}},"subtitle":[],"editor":[{"given":"Alfonso","family":"Valencia","sequence":"additional","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2019,3,14]]},"references-count":90,"journal-issue":{"issue":"20","published-print":{"date-parts":[[2019,10,15]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btz175","relation":{},"ISSN":["1367-4803","1367-4811"],"issn-type":[{"type":"print","value":"1367-4803"},{"type":"electronic","value":"1367-4811"}],"subject":[],"published-other":{"date-parts":[[2019,10,15]]},"published":{"date-parts":[[2019,3,14]]}}}