Emx2 underlies the development and evolution of marsupial gliding membranes

Jorge A. Moreno, Olga Dudchenko, Charles Y. Feigin, Sarah A. Mereby, Zhuoxin Chen, Raul Ramos, Axel A. Almet, Harsha Sen, Benjamin J. Brack, Matthew R. Johnson, Sha Li, Wei Wang, Jenna M. Gaska, Alexander Ploss, David Weisz, Arina D. Omer, Weijie Yao, Zane Colaric, Parwinder Kaur, Judy St. Leger, Qing Nie, Alexandria Mena, Joseph P. Flanagan, Greta Keller, Thomas Sanger, Bruce Ostrow, Maksim V. Plikus, Evgeny Z. Kvon, Erez Lieberman Aiden () and Ricardo Mallarino ()
Additional contact information
Jorge A. Moreno: Princeton University
Olga Dudchenko: The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine
Charles Y. Feigin: Princeton University
Sarah A. Mereby: Princeton University
Zhuoxin Chen: University of California, Irvine
Raul Ramos: University of California, Irvine
Axel A. Almet: University of California, Irvine
Harsha Sen: Princeton University
Benjamin J. Brack: Princeton University
Matthew R. Johnson: Princeton University
Sha Li: Princeton University
Wei Wang: Princeton University
Jenna M. Gaska: Princeton University
Alexander Ploss: Princeton University
David Weisz: The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine
Arina D. Omer: The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine
Weijie Yao: The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine
Zane Colaric: The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine
Parwinder Kaur: The University of Western Australia
Judy St. Leger: Cornell University College of Veterinary Medicine
Qing Nie: University of California, Irvine
Alexandria Mena: SeaWorld San Diego
Joseph P. Flanagan: Houston Zoo
Greta Keller: Loyola University
Thomas Sanger: Loyola University
Bruce Ostrow: Grand Valley State University
Maksim V. Plikus: University of California, Irvine
Evgeny Z. Kvon: University of California, Irvine
Erez Lieberman Aiden: The Center for Genome Architecture, Department of Molecular and Human Genetics, Baylor College of Medicine
Ricardo Mallarino: Princeton University

Nature, 2024, vol. 629, issue 8010, 127-135

Abstract: Abstract Phenotypic 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.

Date: 2024
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DOI: 10.1038/s41586-024-07305-3

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