{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,24]],"date-time":"2026-10-24T06:07:31Z","timestamp":1792822051005,"version":"4.5.0"},"update-to":[{"DOI":"10.1371\/journal.pgen.1011549","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,1,24]],"date-time":"2025-01-24T00:00:00Z","timestamp":1737676800000}}],"reference-count":132,"publisher":"Public Library of Science (PLoS)","issue":"1","license":[{"start":{"date-parts":[[2025,1,13]],"date-time":"2025-01-13T00:00:00Z","timestamp":1736726400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000038","name":"NSERC","doi-asserted-by":"crossref","award":["RGPIN-2023-05390"],"award-info":[{"award-number":["RGPIN-2023-05390"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"crossref"}]},{"name":"NIH","award":["K99GM137041-01A1"],"award-info":[{"award-number":["K99GM137041-01A1"]}]},{"DOI":"10.13039\/501100000245","name":"Michael Smith Health Research BC","doi-asserted-by":"publisher","award":["SCH-2024-03818"],"award-info":[{"award-number":["SCH-2024-03818"]}],"id":[{"id":"10.13039\/501100000245","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100001021","name":"Damon Runyon Cancer Research Foundation","doi-asserted-by":"publisher","award":["DRG 2438-21"],"award-info":[{"award-number":["DRG 2438-21"]}],"id":[{"id":"10.13039\/100001021","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosgenetics.org"],"crossmark-restriction":false},"short-container-title":["PLoS Genet"],"abstract":"<jats:p>\n                    The synaptonemal complex (SC) is a protein-rich structure essential for meiotic recombination and faithful chromosome segregation. Acting like a zipper to paired homologous chromosomes during early prophase I, the complex is a symmetrical structure where central elements are connected on two sides by the transverse filaments to the chromatin-anchoring lateral elements. Despite being found in most major eukaryotic taxa implying a deeply conserved evolutionary origin, several components of the complex exhibit unusually high rates of sequence turnover. This is puzzlingly exemplified by the SC of\n                    <jats:italic>Drosophila<\/jats:italic>\n                    , where the central elements and transverse filaments display no identifiable homologs outside of the genus. Here, we exhaustively examine the evolutionary history of the SC in\n                    <jats:italic>Drosophila<\/jats:italic>\n                    taking a comparative phylogenomic approach with high species density to circumvent obscured homology due to rapid sequence evolution. Contrasting starkly against other genes involved in meiotic chromosome pairing, SC genes show significantly elevated rates of coding evolution due to a combination of relaxed constraint and recurrent, widespread positive selection. In particular, the central element\n                    <jats:italic>cona<\/jats:italic>\n                    and transverse filament\n                    <jats:italic>c(3)G<\/jats:italic>\n                    have diversified through tandem and retro-duplications, repeatedly generating paralogs with novel germline activity. In a striking case of molecular convergence,\n                    <jats:italic>c(3)G<\/jats:italic>\n                    paralogs that independently arose in distant lineages evolved under positive selection to have convergent truncations to the protein termini and elevated testes expression. Surprisingly, the expression of SC genes in the germline is prone to change suggesting recurrent regulatory evolution which, in many species, resulted in high testes expression even though\n                    <jats:italic>Drosophila<\/jats:italic>\n                    males are achiasmic. Overall, our study recapitulates the poor conservation of SC components, and further uncovers that the lack of conservation extends to other modalities including copy number, genomic locale, and germline regulation. Considering the elevated testes expression in many\n                    <jats:italic>Drosophila<\/jats:italic>\n                    species and the common ancestor, we suggest that the activity of SC genes in the male germline, while still poorly understood, may be a prime target of constant evolutionary pressures driving repeated adaptations and innovations.\n                  <\/jats:p>","DOI":"10.1371\/journal.pgen.1011549","type":"journal-article","created":{"date-parts":[[2025,1,13]],"date-time":"2025-01-13T14:08:53Z","timestamp":1736777333000},"page":"e1011549","update-policy":"https:\/\/doi.org\/10.1371\/journal.pgen.corrections_policy","source":"Crossref","is-referenced-by-count":14,"title":["Diversification and recurrent adaptation of the synaptonemal complex in Drosophila"],"prefix":"10.1371","volume":"21","author":[{"given":"Rana","family":"Zakerzade","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9361-1190","authenticated-orcid":true,"given":"Ching-Ho","family":"Chang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1835-710X","authenticated-orcid":true,"given":"Kamalakar","family":"Chatla","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-3427-2716","authenticated-orcid":true,"given":"Ananya","family":"Krishnapura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3350-9204","authenticated-orcid":true,"given":"Samuel P.","family":"Appiah","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0007-6895-5355","authenticated-orcid":true,"given":"Jacki","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8586-7137","authenticated-orcid":true,"given":"Robert L.","family":"Unckless","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6221-9292","authenticated-orcid":true,"given":"Justin P.","family":"Blumenstiel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9724-9467","authenticated-orcid":true,"given":"Doris","family":"Bachtrog","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1694-9582","authenticated-orcid":true,"given":"Kevin H-C.","family":"Wei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2025,1,13]]},"reference":[{"key":"pgen.1011549.ref001","doi-asserted-by":"crossref","first-page":"250","DOI":"10.1159\/000086896","article-title":"Effect of meiotic recombination on the production of aneuploid gametes in humans","volume":"111","author":"NE Lamb","year":"2005","journal-title":"Cytogenet Genome Res"},{"key":"pgen.1011549.ref002","first-page":"7","article-title":"Meiotic Recombination: The Essence of Heredity","author":"N. Hunter","year":"2015","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"pgen.1011549.ref003","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1093\/genetics\/142.2.507","article-title":"Differences in crossover frequency and distribution among three sibling species of Drosophila","volume":"142","author":"JR True","year":"1996","journal-title":"Genetics"},{"key":"pgen.1011549.ref004","doi-asserted-by":"crossref","first-page":"530","DOI":"10.1073\/pnas.12.8.530","article-title":"An Effect of Temperature and Age on Crossing-Over in the First Chromosome of Drosophila Melanogaster","volume":"12","author":"C. 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Anderson","year":"2005","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1011549.ref044","doi-asserted-by":"crossref","first-page":"D439","DOI":"10.1093\/nar\/gkab1061","article-title":"AlphaFold Protein Structure Database: massively expanding the structural coverage of protein-sequence space with high-accuracy models","volume":"50","author":"M Varadi","year":"2022","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011549.ref045","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1038\/s41592-022-01488-1","article-title":"ColabFold: making protein folding accessible to all.","volume":"19","author":"M Mirdita","year":"2022","journal-title":"Nat Methods"},{"key":"pgen.1011549.ref046","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/S0968-0004(99)01540-6","article-title":"NPS@: network protein sequence analysis","volume":"25","author":"C Combet","year":"2000","journal-title":"Trends Biochem 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temperate Drosophila melanogaster","author":"S Voigt","year":"2023","journal-title":"Genetics"},{"key":"pgen.1011549.ref066","doi-asserted-by":"crossref","first-page":"D445","DOI":"10.1093\/nar\/gkac998","article-title":"OrthoDB v11: annotation of orthologs in the widest sampling of organismal diversity","volume":"51","author":"D Kuznetsov","year":"2023","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011549.ref067","doi-asserted-by":"crossref","first-page":"e1005184","DOI":"10.1371\/journal.pgen.1005184","article-title":"Parallel Gene Expression Differences between Low and High Latitude Populations of Drosophila melanogaster and D. simulans","volume":"11","author":"L Zhao","year":"2015","journal-title":"PLoS Genet"},{"key":"pgen.1011549.ref068","first-page":"227","article-title":"FlyBase: updates to the Drosophila genes and genomes database","author":"A \u00d6zt\u00fcrk-\u00c7olak","year":"2024","journal-title":"Genetics"},{"key":"pgen.1011549.ref069","article-title":"Expansion and loss of sperm nuclear basic protein genes in Drosophila correspond with genetic conflicts between sex chromosomes.","volume":"12","author":"C-H Chang","year":"2023","journal-title":"Elife."},{"key":"pgen.1011549.ref070","doi-asserted-by":"crossref","first-page":"e2312380120","DOI":"10.1073\/pnas.2312380120","article-title":"Decoupled evolution of the Sex Peptide gene family and Sex Peptide Receptor in Drosophilidae","volume":"121","author":"BR Hopkins","year":"2024","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1011549.ref071","article-title":"Benchmarking of long-read correction methods.","volume":"2","author":"JC Dohm","year":"2020","journal-title":"NAR Genom Bioinform."},{"key":"pgen.1011549.ref072","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1186\/s13059-021-02282-6","article-title":"Homopolish: a method for the removal of systematic errors in nanopore sequencing by homologous polishing","volume":"22","author":"Y-T Huang","year":"2021","journal-title":"Genome Biol"},{"key":"pgen.1011549.ref073","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1038\/nature12962","article-title":"Diversity and dynamics of the Drosophila transcriptome","volume":"512","author":"JB Brown","year":"2014","journal-title":"Nature"},{"key":"pgen.1011549.ref074","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.1101\/gr.199547.115","article-title":"Critical roles of long noncoding RNAs in Drosophila spermatogenesis","volume":"26","author":"K Wen","year":"2016","journal-title":"Genome Res"},{"key":"pgen.1011549.ref075","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.1534\/genetics.106.069245","article-title":"Evidence for de novo evolution of testis-expressed genes in the Drosophila yakuba\/Drosophila erecta clade","volume":"176","author":"DJ Begun","year":"2007","journal-title":"Genetics"},{"key":"pgen.1011549.ref076","doi-asserted-by":"crossref","first-page":"9935","DOI":"10.1073\/pnas.0509809103","article-title":"Novel genes derived from noncoding DNA in Drosophila melanogaster are frequently X-linked and exhibit testis-biased expression","volume":"103","author":"MT Levine","year":"2006","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1011549.ref077","doi-asserted-by":"crossref","first-page":"1313","DOI":"10.1101\/gr.101386.109","article-title":"evolution, and phenotypic impact of new genes","volume":"20","author":"Kaessmann H. Origins","year":"2010","journal-title":"Genome Res"},{"key":"pgen.1011549.ref078","first-page":"8","article-title":"Testis single-cell RNA-seq reveals the dynamics of de novo gene transcription and germline mutational bias in Drosophila","author":"E Witt","year":"2019","journal-title":"Elife"},{"key":"pgen.1011549.ref079","doi-asserted-by":"crossref","first-page":"6854","DOI":"10.1038\/s41467-021-27136-4","article-title":"A transposon expression burst accompanies the activation of Y-chromosome fertility genes during Drosophila spermatogenesis.","volume":"12","author":"MA Lawlor","year":"2021","journal-title":"Nat Commun"},{"key":"pgen.1011549.ref080","doi-asserted-by":"crossref","first-page":"768","DOI":"10.1016\/S0960-9822(02)00589-4","article-title":"Transcriptional promiscuity in testes","volume":"6","author":"EE Schmidt","year":"1996","journal-title":"Curr Biol"},{"key":"pgen.1011549.ref081","doi-asserted-by":"crossref","first-page":"1841","DOI":"10.1101\/gad.303131.117","article-title":"New genes often acquire male-specific functions but rarely become essential in Drosophila","volume":"31","author":"S Kondo","year":"2017","journal-title":"Genes Dev"},{"key":"pgen.1011549.ref082","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/j.cell.2019.12.015","article-title":"Widespread transcriptional scanning in the testis modulates gene evolution rates","volume":"180","author":"B Xia","year":"2020","journal-title":"Cell"},{"key":"pgen.1011549.ref083","doi-asserted-by":"crossref","first-page":"17409","DOI":"10.1073\/pnas.1313759110","article-title":"Neofunctionalization of young duplicate genes in Drosophila","volume":"110","author":"R Assis","year":"2013","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1011549.ref084","first-page":"10","article-title":"An actin-related protein that is most highly expressed in Drosophila testes is critical for embryonic development","author":"CM Schroeder","year":"2021","journal-title":"Elife"},{"key":"pgen.1011549.ref085","article-title":"Single cell RNA-seq in Drosophila testis reveals evolutionary trajectory of sex chromosome regulation","author":"KH-C Wei","year":"2022","journal-title":"bioRxiv"},{"key":"pgen.1011549.ref086","doi-asserted-by":"crossref","first-page":"1604","DOI":"10.1038\/s41559-021-01543-8","article-title":"Satellite DNA-mediated diversification of a sex-ratio meiotic drive gene family","volume":"5","author":"CA Muirhead","year":"2021","journal-title":"Drosophila. Nat Ecol Evol"},{"key":"pgen.1011549.ref087","doi-asserted-by":"crossref","first-page":"1613","DOI":"10.1038\/s41559-021-01592-z","article-title":"Rapid evolutionary dynamics of an expanding family of meiotic drive factors and their hpRNA suppressors.","volume":"5","author":"J Vedanayagam","year":"2021","journal-title":"Nat Ecol Evol"},{"key":"pgen.1011549.ref088","first-page":"20191430","article-title":"Meiotic drive mechanisms: lessons from Drosophila","volume":"286","author":"C Courret","year":"2019","journal-title":"Proc Biol Sci"},{"key":"pgen.1011549.ref089","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1093\/genetics\/26.5.506","article-title":"A Relation between Larval Nutrition and the Frequency of Crossing over in the Third Chromosome of Drosophila Melanogaster","volume":"26","author":"JV Neel","year":"1941","journal-title":"Genetics"},{"key":"pgen.1011549.ref090","first-page":"220","article-title":"Diet effects on mouse meiotic recombination: a warning for recombination studies","author":"A Belmonte-Tebar","year":"2022","journal-title":"Genetics"},{"key":"pgen.1011549.ref091","volume-title":"The effect of temperature on crossing-over in Drosophila","author":"HH Plough","year":"1917"},{"key":"pgen.1011549.ref092","doi-asserted-by":"crossref","first-page":"1409","DOI":"10.1534\/genetics.117.300588","article-title":"Plasticity of Meiotic Recombination Rates in Response to Temperature in Arabidopsis","volume":"208","author":"A Lloyd","year":"2018","journal-title":"Genetics"},{"key":"pgen.1011549.ref093","doi-asserted-by":"crossref","first-page":"747","DOI":"10.1126\/science.aab1768","article-title":"Fruit flies diversify their offspring in response to parasite infection","volume":"349","author":"ND Singh","year":"2015","journal-title":"Science"},{"key":"pgen.1011549.ref094","doi-asserted-by":"crossref","first-page":"e1002251","DOI":"10.1371\/journal.pgen.1002251","article-title":"Age-dependent recombination rates in human pedigrees.","volume":"7","author":"J Hussin","year":"2011","journal-title":"PLoS Genet"},{"key":"pgen.1011549.ref095","doi-asserted-by":"crossref","first-page":"1409","DOI":"10.1534\/g3.116.027631","article-title":"Genetic Background, Maternal Age, and Interaction Effects Mediate Rates of Crossing Over in Drosophila melanogaster Females.","volume":"6","author":"CM Hunter","year":"2016","journal-title":"G3."},{"key":"pgen.1011549.ref096","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1083\/jcb.128.4.455","article-title":"Zip1-induced changes in synaptonemal complex structure and polycomplex assembly","volume":"128","author":"M Sym","year":"1995","journal-title":"J Cell Biol"},{"key":"pgen.1011549.ref097","doi-asserted-by":"crossref","first-page":"e2204701119","DOI":"10.1073\/pnas.2204701119","article-title":"Polycomb group (PcG) proteins prevent the assembly of abnormal synaptonemal complex structures during meiosis.","volume":"119","author":"T Feij\u00e3o","year":"2022","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1011549.ref098","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1002\/evl3.192","article-title":"The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics","volume":"4","author":"F Ruzicka","year":"2020","journal-title":"Evol Lett"},{"key":"pgen.1011549.ref099","first-page":"20240438","article-title":"On the resolution of sexual conflict over shared traits","volume":"291","author":"TM Pennell","year":"2024","journal-title":"Proc Biol Sci"},{"key":"pgen.1011549.ref100","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1146\/annurev-ecolsys-120213-091721","article-title":"Constraints Evolve: Context Dependency of Gene Effects Allows Evolution of Pleiotropy.","volume":"46","author":"M Pavli\u010dev","year":"2015","journal-title":"Annu Rev Ecol Evol Syst"},{"key":"pgen.1011549.ref101","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1534\/g3.119.400922","article-title":"Chromosome-Level Assembly of Drosophila bifasciata Reveals Important Karyotypic Transition of the X Chromosome.","volume":"10","author":"R Bracewell","year":"2020","journal-title":"G3"},{"key":"pgen.1011549.ref102","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","article-title":"Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype","volume":"37","author":"D Kim","year":"2019","journal-title":"Nat Biotechnol"},{"key":"pgen.1011549.ref103","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"H Li","year":"2009","journal-title":"Bioinformatics"},{"key":"pgen.1011549.ref104","doi-asserted-by":"crossref","first-page":"e108","DOI":"10.1093\/nar\/gkt214","article-title":"The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote","volume":"41","author":"Y Liao","year":"2013","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011549.ref105","article-title":"Models for transcript quantification from RNA-Seq.","author":"L. Pachter","year":"2011","journal-title":"arXiv [q-bio.GN]"},{"key":"pgen.1011549.ref106","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1038\/nbt.3122","article-title":"StringTie enables improved reconstruction of a transcriptome from RNA-seq reads","volume":"33","author":"M Pertea","year":"2015","journal-title":"Nat Biotechnol"},{"key":"pgen.1011549.ref107","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1186\/1471-2105-12-491","article-title":"MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects","volume":"12","author":"C Holt","year":"2011","journal-title":"BMC Bioinformatics"},{"key":"pgen.1011549.ref108","doi-asserted-by":"crossref","first-page":"9451","DOI":"10.1073\/pnas.1921046117","article-title":"RepeatModeler2 for automated genomic discovery of transposable element families","volume":"117","author":"JM Flynn","year":"2020","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pgen.1011549.ref109","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1186\/1471-2105-5-59","article-title":"Gene finding in novel genomes","volume":"5","author":"I. Korf","year":"2004","journal-title":"BMC Bioinformatics"},{"key":"pgen.1011549.ref110","doi-asserted-by":"crossref","first-page":"24","DOI":"10.1038\/nbt.1754","article-title":"Integrative genomics viewer","volume":"29","author":"JT Robinson","year":"2011","journal-title":"Nat Biotechnol"},{"key":"pgen.1011549.ref111","doi-asserted-by":"crossref","first-page":"e12","DOI":"10.1093\/nar\/gkr995","article-title":"GenomeView: a next-generation genome browser","volume":"40","author":"T Abeel","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011549.ref112","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1016\/j.infsof.2005.09.005","article-title":"Engineering a software tool for gene structure prediction in higher organisms","volume":"47","author":"G Gremme","year":"2005","journal-title":"Inf Softw Technol"},{"key":"pgen.1011549.ref113","doi-asserted-by":"crossref","first-page":"482","DOI":"10.1186\/s12859-017-1930-3","article-title":"GFF3sort: a novel tool to sort GFF3 files for tabix indexing","volume":"18","author":"T Zhu","year":"2017","journal-title":"BMC Bioinformatics"},{"key":"pgen.1011549.ref114","doi-asserted-by":"crossref","first-page":"304","DOI":"10.12688\/f1000research.23297.1","article-title":"GFF Utilities: GffRead and GffCompare.","volume":"9","author":"G Pertea","year":"2020","journal-title":"F1000Res"},{"key":"pgen.1011549.ref115","doi-asserted-by":"crossref","first-page":"1639","DOI":"10.1093\/bioinformatics\/btaa1016","article-title":"Liftoff: accurate mapping of gene annotations","volume":"37","author":"A Shumate","year":"2021","journal-title":"Bioinformatics"},{"key":"pgen.1011549.ref116","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1093\/bioinformatics\/bty191","article-title":"Minimap2: pairwise alignment for nucleotide sequences","volume":"34","author":"H. Li","year":"2018","journal-title":"Bioinformatics"},{"key":"pgen.1011549.ref117","doi-asserted-by":"crossref","first-page":"W276","DOI":"10.1093\/nar\/gkac240","article-title":"Search and sequence analysis tools services from EMBL-EBI in 2022","volume":"50","author":"F Madeira","year":"2022","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011549.ref118","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1007\/978-1-62703-646-7_10","article-title":"Phylogeny-aware alignment with PRANK","volume":"1079","author":"A. L\u00f6ytynoja","year":"2014","journal-title":"Methods Mol Biol"},{"key":"pgen.1011549.ref119","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT multiple sequence alignment software version 7: improvements in performance and usability","volume":"30","author":"K Katoh","year":"2013","journal-title":"Mol Biol Evol"},{"key":"pgen.1011549.ref120","doi-asserted-by":"crossref","first-page":"1792","DOI":"10.1093\/nar\/gkh340","article-title":"MUSCLE: multiple sequence alignment with high accuracy and high throughput","volume":"32","author":"RC Edgar","year":"2004","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011549.ref121","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1093\/molbev\/msaa015","article-title":"IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era","volume":"37","author":"BQ Minh","year":"2020","journal-title":"Mol Biol Evol"},{"key":"pgen.1011549.ref122","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1093\/molbev\/msx281","article-title":"UFBoot2: Improving the Ultrafast Bootstrap Approximation","volume":"35","author":"DT Hoang","year":"2018","journal-title":"Mol Biol Evol"},{"key":"pgen.1011549.ref123","unstructured":"FigTree. [cited 13 Jul 2023]. Available: http:\/\/tree.bio.ed.ac.uk\/software\/figtree\/."},{"key":"pgen.1011549.ref124","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1111\/j.2041-210X.2011.00169.x","article-title":"phytools: an R package for phylogenetic comparative biology (and other things): phytools: R package.","volume":"3","author":"LJ Revell","year":"2012","journal-title":"Methods Ecol Evol."},{"key":"pgen.1011549.ref125","doi-asserted-by":"crossref","first-page":"W7","DOI":"10.1093\/nar\/gkq291","article-title":"TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations","volume":"38","author":"F Abascal","year":"2010","journal-title":"Nucleic Acids Res"},{"key":"pgen.1011549.ref126","doi-asserted-by":"crossref","first-page":"1342","DOI":"10.1093\/molbev\/msv022","article-title":"Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection","volume":"32","author":"MD Smith","year":"2015","journal-title":"Mol Biol Evol"},{"key":"pgen.1011549.ref127","doi-asserted-by":"crossref","first-page":"1586","DOI":"10.1093\/molbev\/msm088","article-title":"PAML 4: phylogenetic analysis by maximum likelihood","volume":"24","author":"Z. Yang","year":"2007","journal-title":"Mol Biol Evol"},{"key":"pgen.1011549.ref128","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1038\/nature06341","article-title":"Evolution of genes and genomes on the Drosophila phylogeny","volume":"450","author":"AG Clark","year":"2007","journal-title":"Nature"},{"key":"pgen.1011549.ref129","doi-asserted-by":"crossref","first-page":"1090","DOI":"10.3390\/genes13061090","article-title":"PaPAML: An improved computational tool to explore selection pressure on protein-coding sequences.","volume":"13","author":"R Steffen","year":"2022","journal-title":"Genes (Basel)."},{"key":"pgen.1011549.ref130","doi-asserted-by":"crossref","DOI":"10.1093\/molbev\/msad041","article-title":"Beginner\u2019s guide on the use of PAML to detect positive selection","volume":"40","author":"S \u00c1lvarez-Carretero","year":"2023","journal-title":"Mol Biol Evol"},{"key":"pgen.1011549.ref131","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1002\/pro.3943","article-title":"UCSF ChimeraX: Structure visualization for researchers, educators, and developers","volume":"30","author":"EF Pettersen","year":"2021","journal-title":"Protein Sci"},{"key":"pgen.1011549.ref132","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1080\/01621459.1974.10482955","article-title":"Robust tests for the equality of variances","volume":"69","author":"MB Brown","year":"1974","journal-title":"J Am Stat Assoc"}],"updated-by":[{"DOI":"10.1371\/journal.pgen.1011549","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,1,24]],"date-time":"2025-01-24T00:00:00Z","timestamp":1737676800000}}],"container-title":["PLOS Genetics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1011549","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,24]],"date-time":"2025-01-24T14:24:43Z","timestamp":1737728683000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pgen.1011549"}},"subtitle":[],"editor":[{"given":"Colin","family":"Meiklejohn","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,1,13]]},"references-count":132,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,1,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pgen.1011549","relation":{},"ISSN":["1553-7404"],"issn-type":[{"value":"1553-7404","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,1,13]]}}}