Vocal learning–associated convergent evolution in mammalian proteins and regulatory elements
Author:
Wirthlin Morgan E.12ORCID, Schmid Tobias A.3ORCID, Elie Julie E.34ORCID, Zhang Xiaomeng1ORCID, Kowalczyk Amanda12ORCID, Redlich Ruby1ORCID, Shvareva Varvara A.5, Rakuljic Ashley5, Ji Maria B.6ORCID, Bhat Ninad S.5, Kaplow Irene M.17ORCID, Schäffer Daniel E.1ORCID, Lawler Alyssa J.28ORCID, Wang Andrew Z.1ORCID, Phan BaDoi N.12ORCID, Annaldasula Siddharth1, Brown Ashley R.12ORCID, Lu Tianyu1, Lim Byung Kook9ORCID, Azim Eiman10ORCID, , Clark Nathan L.11ORCID, Meyer Wynn K.12ORCID, Pond Sergei L Kosakovsky13ORCID, Chikina Maria7ORCID, Yartsev Michael M.34ORCID, Pfenning Andreas R.12ORCID, Andrews Gregory, Armstrong Joel C., Bianchi Matteo, Birren Bruce W., Bredemeyer Kevin R., Breit Ana M., Christmas Matthew J., Clawson Hiram, Damas Joana, Di Palma Federica, Diekhans Mark, Dong Michael X., Eizirik Eduardo, Fan Kaili, Fanter Cornelia, Foley Nicole M., Forsberg-Nilsson Karin, Garcia Carlos J., Gatesy John, Gazal Steven, Genereux Diane P., Goodman Linda, Grimshaw Jenna, Halsey Michaela K., Harris Andrew J., Hickey Glenn, Hiller Michael, Hindle Allyson G., Hubley Robert M., Hughes Graham M., Johnson Jeremy, Juan David, Kaplow Irene M., Karlsson Elinor K., Keough Kathleen C., Kirilenko Bogdan, Koepfli Klaus-Peter, Korstian Jennifer M., Kowalczyk Amanda, Kozyrev Sergey V., Lawler Alyssa J., Lawless Colleen, Lehmann Thomas, Levesque Danielle L., Lewin Harris A., Li Xue, Lind Abigail, Lindblad-Toh Kerstin, Mackay-Smith Ava, Marinescu Voichita D., Marques-Bonet Tomas, Mason Victor C., Meadows Jennifer R. S., Meyer Wynn K., Moore Jill E., Moreira Lucas R., Moreno-Santillan Diana D., Morrill Kathleen M., Muntané Gerard, Murphy William J., Navarro Arcadi, Nweeia Martin, Ortmann Sylvia, Osmanski Austin, Paten Benedict, Paulat Nicole S., Pfenning Andreas R., Phan BaDoi N., Pollard Katherine S., Pratt Henry E., Ray David A., Reilly Steven K., Rosen Jeb R., Ruf Irina, Ryan Louise, Ryder Oliver A., Sabeti Pardis C., Schäffer Daniel E., Serres Aitor, Shapiro Beth, Smit Arian F. A., Springer Mark, Srinivasan Chaitanya, Steiner Cynthia, Storer Jessica M., Sullivan Kevin A. M., Sullivan Patrick F., Sundström Elisabeth, Supple Megan A., Swofford Ross, Talbot Joy-El, Teeling Emma, Turner-Maier Jason, Valenzuela Alejandro, Wagner Franziska, Wallerman Ola, Wang Chao, Wang Juehan, Weng Zhiping, Wilder Aryn P., Wirthlin Morgan E., Xue James R., Zhang Xiaomeng
Affiliation:
1. Department of Computational Biology, Carnegie Mellon University, Pittsburgh, PA 15213, USA. 2. Neuroscience Institute, Carnegie Mellon University, Pittsburgh, PA 15213, USA. 3. Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, CA 94708, USA. 4. Department of Bioengineering, University of California, Berkeley, Berkeley, CA 94708, USA. 5. Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, CA 94708, USA. 6. Department of Psychology, University of California, Berkeley, Berkeley, CA 94708, USA. 7. Department of Computational and Systems Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213, USA. 8. Department of Biological Sciences, Carnegie Mellon University, Pittsburgh, PA 15213, USA. 9. Neurobiology section, Division of Biological Science, University of California, San Diego, La Jolla, CA 92093, USA. 10. Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, CA 92037, USA. 11. Department of Biological Sciences, University of Pittsburgh, Pittsburgh, PA 15213, USA. 12. Department of Biological Sciences, Lehigh University, Bethlehem, PA 18015, USA. 13. Department of Biology, Temple University, Philadelphia, PA 19122, USA.
Abstract
Vocal production learning (“vocal learning”) is a convergently evolved trait in vertebrates. To identify brain genomic elements associated with mammalian vocal learning, we integrated genomic, anatomical, and neurophysiological data from the Egyptian fruit bat (
Rousettus aegyptiacus
) with analyses of the genomes of 215 placental mammals. First, we identified a set of proteins evolving more slowly in vocal learners. Then, we discovered a vocal motor cortical region in the Egyptian fruit bat, an emergent vocal learner, and leveraged that knowledge to identify active cis-regulatory elements in the motor cortex of vocal learners. Machine learning methods applied to motor cortex open chromatin revealed 50 enhancers robustly associated with vocal learning whose activity tended to be lower in vocal learners. Our research implicates convergent losses of motor cortex regulatory elements in mammalian vocal learning evolution.
Publisher
American Association for the Advancement of Science (AAAS)
Cited by
4 articles.
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