Vocal learning-associated convergent evolution in mammalian proteins and regulatory elements

• Published in: Science (American Association for the Advancement of Science) 2024-03, Vol.383 (6690), p.eabn3263
• Main Authors: Wirthlin, Morgan E, Schmid, Tobias A, Elie, Julie E, Zhang, Xiaomeng, Kowalczyk, Amanda, Redlich, Ruby, Shvareva, Varvara A, Rakuljic, Ashley, Ji, Maria B, Bhat, Ninad S, Kaplow, Irene M, Schäffer, Daniel E, Lawler, Alyssa J, Wang, Andrew Z, Phan, BaDoi N, Annaldasula, Siddharth, Brown, Ashley R, Lu, Tianyu, Lim, Byung Kook, Azim, Eiman, Clark, Nathan L, Meyer, Wynn K, Pond, Sergei L Kosakovsky, Chikina, Maria, Yartsev, Michael M, Pfenning, Andreas R, 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, Karlsson, Elinor K, Keough, Kathleen C, Kirilenko, Bogdan, Koepfli, Klaus-Peter, Korstian, Jennifer M, Kozyrev, Sergey V, 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, 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, Pollard, Katherine S, Pratt, Henry E, Ray, David A, Reilly, Steven K, Rosen, Jeb R, Ruf, Irina
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; Animals; Artificial intelligence; Autism; Bats; Brain; Chiroptera - genetics; Chiroptera - physiology; Chromatin; Chromatin - metabolism; Coding; Consortia; Convergence; Cortex (motor); Enhancer Elements, Genetic; Epigenesis, Genetic; Eutheria - genetics; Eutheria - physiology; Evolution; Evolution, Molecular; Evolutionary genetics; Gene expression; Gene Expression Regulation; Genes; Genome; Genomes; Human behavior; Larynx; Larynx - physiology; Learning algorithms; Learning behavior; Machine Learning; Mammals; Motor Cortex - cytology; Motor Cortex - physiology; Motor neurons; Motor Neurons - physiology; Neural networks; Neurons; Non-coding RNA; Nucleotides; Proteins; Proteins - genetics; Proteins - metabolism; Regulatory sequences; Social behavior; Social environment; Songbirds; Speech; Vertebrates; Vocalization behavior; Vocalization, Animal - physiology
• ISSN: 0036-8075; 1095-9203; 1095-9203
• DOI: 10.1126/science.abn3263

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 ( ) 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.