{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T00:15:12Z","timestamp":1788394512543,"version":"build-2803163510"},"reference-count":80,"publisher":"Oxford University Press (OUP)","issue":"9","license":[{"start":{"date-parts":[[2025,9,4]],"date-time":"2025-09-04T00:00:00Z","timestamp":1756944000000},"content-version":"vor","delay-in-days":3,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100008982","name":"National Science Foundation","doi-asserted-by":"publisher","award":["IOS2211833"],"award-info":[{"award-number":["IOS2211833"]}],"id":[{"id":"10.13039\/501100008982","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["R35GM14196"],"award-info":[{"award-number":["R35GM14196"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000199","name":"USDA","doi-asserted-by":"publisher","award":["2018-08230"],"award-info":[{"award-number":["2018-08230"]}],"id":[{"id":"10.13039\/100000199","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2025,9,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>A major hurdle in understanding the molecular changes responsible for metazoan diversity is the characterization of cis-regulatory elements (CREs) for gene regulatory networks (GRNs). CRE changes are suspected to be commonplace in trait evolution, since such changes circumvent the deleterious effects of pleiotropy. A growing list of genes, though, is known to be regulated by redundant CREs. Such redundant CRE architectures complicate the characterization of GRN evolution, as they compound the effort to characterize each locus, and raise the questions of how and whether genes with redundant architectures evolve expression. Here, we used the evolution of sexually dimorphic abdomen pigmentation of Drosophila (D.) melanogaster as a model to study the function and evolution of CREs. Numerous sequences were evaluated that were previously predicted as potential abdomen CREs. Most of these predictions were validated, including two, four, and ten that, respectively, reside in the homothorax, grainy head, and Eip74EF transcription factor loci. The homothorax CREs were found to be partially redundant for this gene's pigmentation function, and pupal-stage Homothorax expression and the CRE activities were conserved among Drosophila species with the derived dimorphic and ancestral monomorphic phenotypes. Similarly, the Eip74EF CREs were conserved in the monomorphic D. willistoni. Thus, this gene's extensive CRE spatiotemporal redundancy has been conserved for over 30 million years, predating the dimorphic trait. Pigmentation evolution has been connected elsewhere to changes in nonredundant CREs. When these traits evolve, GRN changes may be biased towards the genes with singular nonredundant CREs, while the expression of redundantly regulated genes remains conserved.<\/jats:p>","DOI":"10.1093\/molbev\/msaf213","type":"journal-article","created":{"date-parts":[[2025,9,4]],"date-time":"2025-09-04T14:36:43Z","timestamp":1756996603000},"source":"Crossref","is-referenced-by-count":2,"title":["Redundant and Singular Regulatory Elements Underlie the Rapidly Evolving Pigmentation of <i>Drosophila<\/i>"],"prefix":"10.1093","volume":"42","author":[{"ORCID":"https:\/\/orcid.org\/0009-0000-3333-0207","authenticated-orcid":false,"given":"Logan A","family":"Brubaker","sequence":"first","affiliation":[{"name":"Department of Biology, University of Dayton , Dayton, OH 45469 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-3786-2285","authenticated-orcid":false,"given":"Hayley","family":"Long","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Dayton , Dayton, OH 45469 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0003-5099-818X","authenticated-orcid":false,"given":"Allison","family":"Pavlus","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Dayton , Dayton, OH 45469 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0009-3947-4776","authenticated-orcid":false,"given":"Melissa E","family":"Williams","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Dayton , Dayton, OH 45469 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-3804-6597","authenticated-orcid":false,"given":"Devon M","family":"Seibert","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Dayton , Dayton, OH 45469 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-9624-9958","authenticated-orcid":false,"given":"Ashley V","family":"Williams","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Dayton , Dayton, OH 45469 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4149-2705","authenticated-orcid":false,"given":"Marc S","family":"Halfon","sequence":"additional","affiliation":[{"name":"Program in Genetics, Genomics, and Bioinformatics, University at Buffalo-State University of New York , Buffalo, NY ,","place":["USA"]},{"name":"Department of Biochemistry, University at Buffalo-State University of New York , Buffalo, NY ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5731-5570","authenticated-orcid":false,"given":"Mark","family":"Rebeiz","sequence":"additional","affiliation":[{"name":"Department of Biological Sciences, University of Pittsburgh , Pittsburgh, PA 15260, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1363-0637","authenticated-orcid":false,"given":"Thomas M","family":"Williams","sequence":"additional","affiliation":[{"name":"Department of Biology, University of Dayton , Dayton, OH 45469 ,","place":["USA"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2025,9,4]]},"reference":[{"issue":"3","key":"2025092506423924300_msaf213-B1","doi-asserted-by":"publisher","first-page":"jkac010","DOI":"10.1093\/g3journal\/jkac010","article-title":"The role of the epidermis enhancer element in positive and negative transcriptional regulation of ebony in Drosophila melanogaster","volume":"12","author":"Akiyama","year":"2022","journal-title":"G3 (Bethesda)"},{"issue":"1","key":"2025092506423924300_msaf213-B2","doi-asserted-by":"publisher","first-page":"122","DOI":"10.1016\/j.ydbio.2011.07.018","article-title":"TALE-class homeodomain transcription factors, homothorax and extradenticle, control dendritic and axonal targeting of olfactory projection neurons in the Drosophila brain","volume":"358","author":"Ando","year":"2011","journal-title":"Dev Biol."},{"key":"2025092506423924300_msaf213-B3","volume-title":"Drosophila: a laboratory handbook","author":"Ashburner","year":"2011","edition":"2nd ed"},{"key":"2025092506423924300_msaf213-B4","doi-asserted-by":"publisher","first-page":"2685","DOI":"10.1242\/dev.127.12.2685","article-title":"Function and regulation of homothorax in the wing imaginai disc of Drosophila","volume":"127","author":"Azpiazu","year":"2000","journal-title":"Development"},{"key":"2025092506423924300_msaf213-B5","doi-asserted-by":"publisher","first-page":"3312","DOI":"10.1073\/pnas.0611511104","article-title":"An optimized transgenesis system for Drosophila using germ-line-specific \u03a6C31 integrases","volume":"104","author":"Bischof","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2025092506423924300_msaf213-B6","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1038\/nature12962","article-title":"Diversity and dynamics of the Drosophila transcriptome","volume":"512","author":"Brown","year":"2014","journal-title":"Nature"},{"key":"2025092506423924300_msaf213-B7","doi-asserted-by":"publisher","first-page":"3971","DOI":"10.1242\/dev.127.18.3971","article-title":"Generation of medial and lateral dorsal body domains by the pannier gene of Drosophila","volume":"127","author":"Calleja","year":"2000","journal-title":"Development"},{"key":"2025092506423924300_msaf213-B8","doi-asserted-by":"publisher","first-page":"e1005136","DOI":"10.1371\/journal.pgen.1005136","article-title":"The evolutionary origination and diversification of a dimorphic gene regulatory network through parallel innovations in cis and trans","volume":"11","author":"Camino","year":"2015","journal-title":"PLoS Genet"},{"key":"2025092506423924300_msaf213-B9","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1016\/j.cell.2008.06.030","article-title":"Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution","volume":"134","author":"Carroll","year":"2008","journal-title":"Cell"},{"key":"2025092506423924300_msaf213-B10","doi-asserted-by":"publisher","first-page":"302","DOI":"10.1126\/science.1182213","article-title":"Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer","volume":"327","author":"Chan","year":"2010","journal-title":"Science"},{"key":"2025092506423924300_msaf213-B11","doi-asserted-by":"publisher","first-page":"pdb.prot080762","DOI":"10.1101\/pdb.prot080762","article-title":"Generation of transgenic Drosophila expressing shRNAs in the miR-1 backbone","volume":"2014","author":"Chang","year":"2014","journal-title":"Cold Spring Harb Protoc"},{"key":"2025092506423924300_msaf213-B12","doi-asserted-by":"publisher","first-page":"D486","DOI":"10.1093\/nar\/gkl827","article-title":"FlyBase: genomes by the dozen","volume":"35","author":"Crosby","year":"2007","journal-title":"Nucleic Acids Res."},{"key":"2025092506423924300_msaf213-B13","doi-asserted-by":"publisher","first-page":"e1007573","DOI":"10.1371\/journal.pgen.1007573","article-title":"Bric \u00e0 brac (bab), a central player in the gene regulatory network that mediates thermal plasticity of pigmentation in Drosophila melanogaster","volume":"14","author":"De Castro","year":"2018","journal-title":"PLoS Genet"},{"key":"2025092506423924300_msaf213-B14","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1038\/nature06341","article-title":"Evolution of genes and genomes on the Drosophila phylogeny","volume":"450","author":"Drosophila 12 Genomes Consortium","year":"2007","journal-title":"Nature"},{"key":"2025092506423924300_msaf213-B15","doi-asserted-by":"publisher","first-page":"490","DOI":"10.1038\/nature09158","article-title":"Phenotypic robustness conferred by apparently redundant transcriptional enhancers","volume":"466","author":"Frankel","year":"2010","journal-title":"Nature"},{"key":"2025092506423924300_msaf213-B16","doi-asserted-by":"publisher","first-page":"20975","DOI":"10.1073\/pnas.1207715109","article-title":"Conserved regulatory architecture underlies parallel genetic changes and convergent phenotypic evolution","volume":"109","author":"Frankel","year":"2012","journal-title":"Proc Natl Acad Sci U S A."},{"key":"2025092506423924300_msaf213-B17","doi-asserted-by":"publisher","first-page":"W273","DOI":"10.1093\/nar\/gkh458","article-title":"VISTA: computational tools for comparative genomics","volume":"32","author":"Frazer","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"2025092506423924300_msaf213-B18","doi-asserted-by":"publisher","first-page":"e30","DOI":"10.1371\/journal.pgen.0030030","article-title":"Phenotypic plasticity in Drosophila pigmentation caused by temperature sensitivity of a chromatin regulator network","volume":"3","author":"Gibert","year":"2007","journal-title":"PLoS Genet"},{"key":"2025092506423924300_msaf213-B19","doi-asserted-by":"publisher","first-page":"iyac035","DOI":"10.1093\/genetics\/iyac035","article-title":"FlyBase: a guided tour of highlighted features","volume":"220","author":"Gramates","year":"2022","journal-title":"Genetics"},{"key":"2025092506423924300_msaf213-B20","doi-asserted-by":"publisher","first-page":"1775","DOI":"10.1093\/genetics\/166.4.1775","article-title":"Construction of transgenic Drosophila by using the site-speci\ufb01c integrase from phage \u03d5C3","volume":"166","author":"Groth","year":"2004","journal-title":"Genetics"},{"key":"2025092506423924300_msaf213-B21","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1016\/j.ydbio.2018.07.001","article-title":"Augmentation of a wound response element accompanies the origin of a Hox-regulated Drosophila abdominal pigmentation trait","volume":"441","author":"Grover","year":"2018","journal-title":"Dev Biol."},{"key":"2025092506423924300_msaf213-B22","doi-asserted-by":"publisher","first-page":"11435","DOI":"10.1073\/pnas.1006689107","article-title":"Vectors and parameters that enhance the efficacy of RNAi-mediated gene disruption in transgenic Drosophila","volume":"107","author":"Haley","year":"2010","journal-title":"Proc Natl Acad Sci U S A."},{"key":"2025092506423924300_msaf213-B23","doi-asserted-by":"publisher","first-page":"482","DOI":"10.1016\/j.ydbio.2008.06.015","article-title":"A simplified miRNA-based gene silencing method for Drosophila melanogaster","volume":"321","author":"Haley","year":"2008","journal-title":"Dev Biol."},{"key":"2025092506423924300_msaf213-B24","doi-asserted-by":"publisher","first-page":"149","DOI":"10.1016\/j.tig.2019.12.005","article-title":"Silencers, enhancers, and the multifunctional regulatory genome","volume":"36","author":"Halfon","year":"2020","journal-title":"Trends Genet."},{"key":"2025092506423924300_msaf213-B25","doi-asserted-by":"publisher","first-page":"983","DOI":"10.1242\/dev.058370","article-title":"Concentric zones, cell migration and neuronal circuits in the Drosophila visual center","volume":"138","author":"Hasegawa","year":"2011","journal-title":"Development"},{"key":"2025092506423924300_msaf213-B26","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1242\/dev.02746","article-title":"Comparative analysis of Hox downstream genes in Drosophila","volume":"134","author":"Hueber","year":"2007","journal-title":"Development"},{"key":"2025092506423924300_msaf213-B27","doi-asserted-by":"publisher","first-page":"80","DOI":"10.3389\/fevo.2020.00080","article-title":"Gene regulatory network homoplasy underlies recurrent sexually dimorphic fruit fly pigmentation","volume":"8","author":"Hughes","year":"2020","journal-title":"Front Ecol Evol."},{"key":"2025092506423924300_msaf213-B28","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1002\/jez.b.23068","article-title":"Widespread cis- and trans-regulatory evolution underlies the origin, diversification, and loss of a sexually dimorphic fruit fly pigmentation trait","volume":"340","author":"Hughes","year":"2023","journal-title":"J Exp Zool Pt B"},{"key":"2025092506423924300_msaf213-B29","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1016\/j.cell.2008.01.014","article-title":"The evolution of gene regulation underlies a morphological difference between two Drosophila sister species","volume":"132","author":"Jeong","year":"2008","journal-title":"Cell"},{"key":"2025092506423924300_msaf213-B30","doi-asserted-by":"publisher","first-page":"1387","DOI":"10.1016\/j.cell.2006.04.043","article-title":"Regulation of body pigmentation by the abdominal-B Hox protein and its gain and loss in Drosophila evolution","volume":"125","author":"Jeong","year":"2006","journal-title":"Cell"},{"key":"2025092506423924300_msaf213-B31","doi-asserted-by":"publisher","first-page":"e1005279","DOI":"10.1371\/journal.pgen.1005279","article-title":"Genetic changes to a transcriptional silencer element confers phenotypic diversity within and between Drosophila species","volume":"11","author":"Johnson","year":"2015","journal-title":"PLoS Genet"},{"key":"2025092506423924300_msaf213-B32","doi-asserted-by":"publisher","first-page":"e1007375","DOI":"10.1371\/journal.pgen.1007375","article-title":"Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution","volume":"14","author":"Kittelmann","year":"2018","journal-title":"PLoS Genet"},{"key":"2025092506423924300_msaf213-B33","doi-asserted-by":"publisher","first-page":"553","DOI":"10.1038\/35046017","article-title":"Genetic control and evolution of sexually dimorphic characters in Drosophila","volume":"408","author":"Kopp","year":"2000","journal-title":"Nature"},{"key":"2025092506423924300_msaf213-B34","doi-asserted-by":"publisher","first-page":"7524","DOI":"10.1073\/pnas.1509022112","article-title":"Gain of cis-regulatory activities underlies novel domains of wingless gene expression in Drosophila","volume":"112","author":"Koshikawa","year":"2015","journal-title":"Proc Natl Acad Sci U S A."},{"issue":"D1","key":"2025092506423924300_msaf213-B35","doi-asserted-by":"publisher","first-page":"D155","DOI":"10.1093\/nar\/gky1141","article-title":"miRBase: from microRNA sequences to function","volume":"47","author":"Kozomara","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"2025092506423924300_msaf213-B36","doi-asserted-by":"publisher","first-page":"1463","DOI":"10.1038\/s41588-018-0221-x","article-title":"Dynamic 3D chromatin architecture contributes to enhancer specificity and limb morphogenesis","volume":"50","author":"Kragesteen","year":"2018","journal-title":"Nat Genet"},{"key":"2025092506423924300_msaf213-B37","doi-asserted-by":"publisher","first-page":"1037","DOI":"10.1242\/dev.125.6.1037","article-title":"dorsotonals\/homothorax, the Drosophila homologue of meis1, interacts with extradenticle in patterning of the embryonic PNS","volume":"125","author":"Kurant","year":"1998","journal-title":"Development"},{"key":"2025092506423924300_msaf213-B38","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1016\/j.cell.2016.09.028","article-title":"Progressive loss of function in a limb enhancer during snake evolution","volume":"167","author":"Kvon","year":"2016","journal-title":"Cell"},{"key":"2025092506423924300_msaf213-B39","doi-asserted-by":"publisher","first-page":"324","DOI":"10.1038\/s41576-020-00311-x","article-title":"Enhancer redundancy in development and disease","volume":"22","author":"Kvon","year":"2021","journal-title":"Nat Rev Genet"},{"key":"2025092506423924300_msaf213-B40","doi-asserted-by":"publisher","first-page":"1262","DOI":"10.1016\/j.cell.2020.02.031","article-title":"Comprehensive in vivo interrogation reveals phenotypic impact of human enhancer variants","volume":"180","author":"Kvon","year":"2020","journal-title":"Cell"},{"key":"2025092506423924300_msaf213-B41","doi-asserted-by":"publisher","first-page":"978","DOI":"10.1093\/hmg\/ddm370","article-title":"Point mutations in a distant sonic hedgehog cis-regulator generate a variable regulatory output responsible for preaxial polydactyly","volume":"17","author":"Lettice","year":"2008","journal-title":"Hum Mol Genet."},{"key":"2025092506423924300_msaf213-B42","doi-asserted-by":"publisher","first-page":"7548","DOI":"10.1073\/pnas.112212199","article-title":"Disruption of a long-range cis-acting regulator for shh causes preaxial polydactyly","volume":"99","author":"Lettice","year":"2002","journal-title":"Proc Natl Acad Sci U S A."},{"key":"2025092506423924300_msaf213-B43","doi-asserted-by":"publisher","first-page":"2157","DOI":"10.1016\/j.cub.2019.05.074","article-title":"Changes throughout a genetic network mask the contribution of hox gene evolution","volume":"29","author":"Liu","year":"2019","journal-title":"Curr Biol."},{"key":"2025092506423924300_msaf213-B44","doi-asserted-by":"publisher","first-page":"1035","DOI":"10.1016\/j.tree.2024.07.005","article-title":"Beyond modular enhancers: new questions in cis-regulatory evolution","volume":"39","author":"McDonald","year":"2024","journal-title":"Trends Ecol Evol."},{"key":"2025092506423924300_msaf213-B45","doi-asserted-by":"publisher","first-page":"W20","DOI":"10.1093\/nar\/gkh435","article-title":"BLAST: at the core of a powerful and diverse set of sequence analysis tools","volume":"32","author":"McGinnis","year":"2004","journal-title":"Nucleic Acids Res."},{"key":"2025092506423924300_msaf213-B46","doi-asserted-by":"publisher","first-page":"587","DOI":"10.1038\/nature05988","article-title":"Morphological evolution through multiple cis-regulatory mutations at a single gene","volume":"448","author":"McGregor","year":"2007","journal-title":"Nature"},{"key":"2025092506423924300_msaf213-B47","doi-asserted-by":"publisher","first-page":"e1010722","DOI":"10.1371\/journal.pgen.1010722","article-title":"Changes in locus wide repression underlie the evolution of Drosophila abdominal pigmentation","volume":"19","author":"M\u00e9ndez-Gonz\u00e1lez","year":"2023","journal-title":"PLoS Genet"},{"key":"2025092506423924300_msaf213-B48","doi-asserted-by":"publisher","first-page":"1089","DOI":"10.1534\/genetics.109.103630","article-title":"A Drosophila resource of transgenic RNAi lines for neurogenetics","volume":"182","author":"Ni","year":"2009","journal-title":"Genetics"},{"key":"2025092506423924300_msaf213-B49","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1038\/nmeth1146","article-title":"Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster","volume":"5","author":"Ni","year":"2008","journal-title":"Nat Methods"},{"key":"2025092506423924300_msaf213-B50","doi-asserted-by":"publisher","first-page":"405","DOI":"10.1038\/nmeth.1592","article-title":"A genome-scale shRNA resource for transgenic RNAi in Drosophila","volume":"8","author":"Ni","year":"2011","journal-title":"Nat Methods"},{"key":"2025092506423924300_msaf213-B51","doi-asserted-by":"publisher","first-page":"3021","DOI":"10.1016\/j.celrep.2018.02.073","article-title":"Comprehensive analysis of a cis-regulatory region reveals pleiotropy in enhancer function","volume":"22","author":"Noon","year":"2018","journal-title":"Cell Rep."},{"key":"2025092506423924300_msaf213-B52","doi-asserted-by":"publisher","first-page":"442","DOI":"10.1006\/mpev.2001.1053","article-title":"Phylogeny of the subgenus sophophora (Diptera: Drosophilidae) based on combined analysis of nuclear and mitochondrial sequences","volume":"22","author":"O\u2019Grady","year":"2002","journal-title":"Mol Phylogenet Evol."},{"key":"2025092506423924300_msaf213-B53","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1038\/nature25461","article-title":"Enhancer redundancy provides phenotypic robustness in mammalian development","volume":"554","author":"Osterwalder","year":"2018","journal-title":"Nature"},{"key":"2025092506423924300_msaf213-B54","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1038\/s41586-020-2879-3","article-title":"Neuronal diversity and convergence in a visual system developmental atlas","volume":"589","author":"\u00d6zel","year":"2021","journal-title":"Nature"},{"key":"2025092506423924300_msaf213-B55","doi-asserted-by":"publisher","first-page":"435","DOI":"10.1101\/gad.12.3.435","article-title":"The Homothorax homeoprotein activates the nuclear localization of another homeoprotein, extradenticle, and suppresses eye development in Drosophila","volume":"12","author":"Pai","year":"1998","journal-title":"Genes Dev."},{"key":"2025092506423924300_msaf213-B56","doi-asserted-by":"publisher","first-page":"jkae097","DOI":"10.1093\/g3journal\/jkae097","article-title":"A genetic screen of transcription factors in the Drosophila melanogaster abdomen identifies novel pigmentation genes","volume":"14","author":"Petrosky","year":"2024","journal-title":"G3 (Bethesda)"},{"key":"2025092506423924300_msaf213-B57","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/molbev\/msae250","article-title":"Saltational episodes of reticulate evolution in the Drosophila saltans species group","volume":"41","author":"Prediger","year":"2024","journal-title":"Mol Biol Evol."},{"key":"2025092506423924300_msaf213-B58","doi-asserted-by":"publisher","first-page":"8605","DOI":"10.1073\/pnas.0700488104","article-title":"Emerging principles of regulatory evolution","volume":"104","author":"Prud\u2019homme","year":"2007","journal-title":"Proc Natl Acad Sci USA."},{"key":"2025092506423924300_msaf213-B59","doi-asserted-by":"publisher","first-page":"1050","DOI":"10.1038\/nature04597","article-title":"Repeated morphological evolution through cis-regulatory changes in a pleiotropic gene","volume":"440","author":"Prud\u2019homme","year":"2006","journal-title":"Nature"},{"key":"2025092506423924300_msaf213-B60","doi-asserted-by":"publisher","first-page":"1663","DOI":"10.1126\/science.1178357","article-title":"Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population","volume":"326","author":"Rebeiz","year":"2009","journal-title":"Science"},{"key":"2025092506423924300_msaf213-B61","doi-asserted-by":"publisher","first-page":"431","DOI":"10.1016\/j.ydbio.2004.04.011","article-title":"GenePalette: a universal software tool for genome sequence visualization and analysis","volume":"271","author":"Rebeiz","year":"2004","journal-title":"Dev Biol."},{"key":"2025092506423924300_msaf213-B62","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.cois.2016.10.002","article-title":"Using Drosophila pigmentation traits to study the mechanisms of cis-regulatory evolution","volume":"19","author":"Rebeiz","year":"2017","journal-title":"Curr Opin Insect Sci."},{"key":"2025092506423924300_msaf213-B63","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1101\/gr.3059305","article-title":"Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution","volume":"15","author":"Richards","year":"2005","journal-title":"Genome Res"},{"key":"2025092506423924300_msaf213-B64","doi-asserted-by":"publisher","first-page":"e32273","DOI":"10.7554\/eLife.32273","article-title":"Cis-regulatory evolution integrated the Bric-\u00e0-brac transcription factors into a novel fruit fly gene regulatory network","volume":"7","author":"Roeske","year":"2018","journal-title":"eLife"},{"key":"2025092506423924300_msaf213-B65","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1016\/j.ydbio.2013.11.013","article-title":"A survey of the trans-regulatory landscape for Drosophila melanogaster abdominal pigmentation","volume":"385","author":"Rogers","year":"2014","journal-title":"Dev Biol."},{"key":"2025092506423924300_msaf213-B66","doi-asserted-by":"publisher","first-page":"e1003740","DOI":"10.1371\/journal.pgen.1003740","article-title":"Recurrent modification of a conserved cis-regulatory element underlies fruit fly pigmentation diversity","volume":"9","author":"Rogers","year":"2013","journal-title":"PLoS Genet"},{"key":"2025092506423924300_msaf213-B67","doi-asserted-by":"publisher","first-page":"3395","DOI":"10.3791\/3395","article-title":"Quantitative comparison of Cis-Regulatory Element (CRE) activities in transgenic Drosophila melanogaster","volume":"58","author":"Rogers","year":"2011","journal-title":"J Vis Exp."},{"key":"2025092506423924300_msaf213-B68","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1093\/molbev\/msae004","article-title":"The density of regulatory information is a major determinant of evolutionary constraint on noncoding DNA in Drosophila","volume":"41","author":"Sabar\u00eds","year":"2024","journal-title":"Mol Biol Evol."},{"key":"2025092506423924300_msaf213-B69","doi-asserted-by":"publisher","first-page":"442","DOI":"10.1111\/ede.12053","article-title":"The evolution of bab paralog expression and abdominal pigmentation among Sophophora fruit fly species","volume":"15","author":"Salomone","year":"2013","journal-title":"Evol Dev."},{"issue":"7","key":"2025092506423924300_msaf213-B70","doi-asserted-by":"publisher","first-page":"dev158550","DOI":"10.1242\/dev.158550","article-title":"Disrupting the three-dimensional regulatory topology of the Pitx1 locus results in overtly normal development","volume":"145","author":"Sarro","year":"2018","journal-title":"Development"},{"key":"2025092506423924300_msaf213-B71","doi-asserted-by":"publisher","first-page":"47","DOI":"10.4161\/fly.22353","article-title":"Genomic resources for multiple species in the Drosophila ananassae species group","volume":"7","author":"Signor","year":"2013","journal-title":"Fly (Austin)."},{"key":"2025092506423924300_msaf213-B72","doi-asserted-by":"publisher","first-page":"158","DOI":"10.1016\/j.ydbio.2017.06.033","article-title":"Automated tools for comparative sequence analysis of genic regions using the GenePalette application","volume":"429","author":"Smith","year":"2017","journal-title":"Dev Biol."},{"key":"2025092506423924300_msaf213-B73","doi-asserted-by":"publisher","first-page":"e38555","DOI":"10.7554\/eLife.38555","article-title":"A novel enhancer near the pitx1 gene influences development and evolution of pelvic appendages in vertebrates","volume":"7","author":"Thompson","year":"2018","journal-title":"Elife"},{"key":"2025092506423924300_msaf213-B74","doi-asserted-by":"publisher","first-page":"520","DOI":"10.1186\/1471-2105-7-520","article-title":"An accurate and interpretable model for siRNA efficacy prediction","volume":"7","author":"Vert","year":"2006","journal-title":"BMC Bioinformatics"},{"key":"2025092506423924300_msaf213-B75","doi-asserted-by":"publisher","first-page":"5201","DOI":"10.3390\/cancers13205201","article-title":"No need to stick together to be connected: multiple types of enhancers' networking","volume":"13","author":"Vitale","year":"2021","journal-title":"Cancers (Basel)."},{"key":"2025092506423924300_msaf213-B76","doi-asserted-by":"publisher","first-page":"e59351","DOI":"10.7554\/eLife.59351","article-title":"Shadow enhancers can suppress input transcription factor noise through distinct regulatory logic","volume":"9","author":"Waymack","year":"2020","journal-title":"Elife"},{"key":"2025092506423924300_msaf213-B77","doi-asserted-by":"publisher","first-page":"e1010653","DOI":"10.1371\/journal.pgen.1010653","article-title":"A novel role for trithorax in the gene regulatory network for a rapidly evolving fruit fly pigmentation trait","volume":"19","author":"Weinstein","year":"2023","journal-title":"PLoS Genet"},{"key":"2025092506423924300_msaf213-B78","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.1038\/nature08896","article-title":"Generation of a novel wing colour pattern by the wingless morphogen","volume":"464","author":"Werner","year":"2010","journal-title":"Nature"},{"key":"2025092506423924300_msaf213-B79","doi-asserted-by":"publisher","first-page":"610","DOI":"10.1016\/j.cell.2008.06.052","article-title":"The regulation and evolution of a genetic switch controlling sexually dimorphic traits in Drosophila","volume":"134","author":"Williams","year":"2008","journal-title":"Cell"},{"key":"2025092506423924300_msaf213-B80","doi-asserted-by":"publisher","first-page":"1740","DOI":"10.1016\/j.celrep.2015.08.021","article-title":"Kr\u00fcppel expression levels are maintained through compensatory evolution of shadow enhancers","volume":"12","author":"Wunderlich","year":"2015","journal-title":"Cell Rep."}],"container-title":["Molecular Biology and Evolution"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/mbe\/advance-article-pdf\/doi\/10.1093\/molbev\/msaf213\/64210706\/msaf213.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/mbe\/article-pdf\/42\/9\/msaf213\/64210706\/msaf213.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/mbe\/article-pdf\/42\/9\/msaf213\/64210706\/msaf213.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,9,25]],"date-time":"2025-09-25T10:42:48Z","timestamp":1758796968000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/mbe\/article\/doi\/10.1093\/molbev\/msaf213\/8248050"}},"subtitle":[],"editor":[{"given":"John","family":"True","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2025,9,1]]},"references-count":80,"journal-issue":{"issue":"9","published-print":{"date-parts":[[2025,9,1]]}},"URL":"https:\/\/doi.org\/10.1093\/molbev\/msaf213","relation":{},"ISSN":["0737-4038","1537-1719"],"issn-type":[{"value":"0737-4038","type":"print"},{"value":"1537-1719","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2025,9]]},"published":{"date-parts":[[2025,9,1]]},"article-number":"msaf213"}}