Emx2 underlies the development and evolution of marsupial gliding membranes

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dc.citation.firstpage127en_US
dc.citation.journalTitleNatureen_US
dc.citation.lastpage135en_US
dc.citation.volumeNumber629en_US
dc.contributor.authorMoreno, Jorge A.en_US
dc.contributor.authorDudchenko, Olgaen_US
dc.contributor.authorFeigin, Charles Y.en_US
dc.contributor.authorMereby, Sarah A.en_US
dc.contributor.authorChen, Zhuoxinen_US
dc.contributor.authorRamos, Raulen_US
dc.contributor.authorAlmet, Axel A.en_US
dc.contributor.authorSen, Harshaen_US
dc.contributor.authorBrack, Benjamin J.en_US
dc.contributor.authorJohnson, Matthew R.en_US
dc.contributor.authorLi, Shaen_US
dc.contributor.authorWang, Weien_US
dc.contributor.authorGaska, Jenna M.en_US
dc.contributor.authorPloss, Alexanderen_US
dc.contributor.authorWeisz, Daviden_US
dc.contributor.authorOmer, Arina D.en_US
dc.contributor.authorYao, Weijieen_US
dc.contributor.authorColaric, Zaneen_US
dc.contributor.authorKaur, Parwinderen_US
dc.contributor.authorLeger, Judy Sten_US
dc.contributor.authorNie, Qingen_US
dc.contributor.authorMena, Alexandriaen_US
dc.contributor.authorFlanagan, Joseph P.en_US
dc.contributor.authorKeller, Gretaen_US
dc.contributor.authorSanger, Thomasen_US
dc.contributor.authorOstrow, Bruceen_US
dc.contributor.authorPlikus, Maksim V.en_US
dc.contributor.authorKvon, Evgeny Z.en_US
dc.contributor.authorAiden, Erez Liebermanen_US
dc.contributor.authorMallarino, Ricardoen_US
dc.contributor.orgCenter for Theoretical Biological Physicsen_US
dc.date.accessioned2024-07-25T20:55:18Zen_US
dc.date.available2024-07-25T20:55:18Zen_US
dc.date.issued2024en_US
dc.description.abstractPhenotypic variation among species is a product of evolutionary changes to developmental programs1,2. However, how these changes generate novel morphological traits remains largely unclear. Here we studied the genomic and developmental basis of the mammalian gliding membrane, or patagium—an adaptative trait that has repeatedly evolved in different lineages, including in closely related marsupial species. Through comparative genomic analysis of 15 marsupial genomes, both from gliding and non-gliding species, we find that the Emx2 locus experienced lineage-specific patterns of accelerated cis-regulatory evolution in gliding species. By combining epigenomics, transcriptomics and in-pouch marsupial transgenics, we show that Emx2 is a critical upstream regulator of patagium development. Moreover, we identify different cis-regulatory elements that may be responsible for driving increased Emx2 expression levels in gliding species. Lastly, using mouse functional experiments, we find evidence that Emx2 expression patterns in gliders may have been modified from a pre-existing program found in all mammals. Together, our results suggest that patagia repeatedly originated through a process of convergent genomic evolution, whereby regulation of Emx2 was altered by distinct cis-regulatory elements in independently evolved species. Thus, different regulatory elements targeting the same key developmental gene may constitute an effective strategy by which natural selection has harnessed regulatory evolution in marsupial genomes to generate phenotypic novelty.en_US
dc.identifier.citationMoreno, J. A., Dudchenko, O., Feigin, C. Y., Mereby, S. A., Chen, Z., Ramos, R., Almet, A. A., Sen, H., Brack, B. J., Johnson, M. R., Li, S., Wang, W., Gaska, J. M., Ploss, A., Weisz, D., Omer, A. D., Yao, W., Colaric, Z., Kaur, P., … Mallarino, R. (2024). Emx2 underlies the development and evolution of marsupial gliding membranes. Nature, 629(8010), 127–135. https://doi.org/10.1038/s41586-024-07305-3en_US
dc.identifier.digitals41586-024-07305-3en_US
dc.identifier.doihttps://doi.org/10.1038/s41586-024-07305-3en_US
dc.identifier.urihttps://hdl.handle.net/1911/117523en_US
dc.language.isoengen_US
dc.publisherSpringer Natureen_US
dc.rightsExcept where otherwise noted, this work is licensed under a Creative Commons Attribution (CC BY) license.  Permission to reuse, publish, or reproduce the work beyond the terms of the license or beyond the bounds of fair use or other exemptions to copyright law must be obtained from the copyright holder.en_US
dc.rights.urihttps://creativecommons.org/licenses/by/4.0/en_US
dc.titleEmx2 underlies the development and evolution of marsupial gliding membranesen_US
dc.typeJournal articleen_US
dc.type.dcmiTexten_US
dc.type.publicationpublisher versionen_US
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