Dataset Information

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

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.

SUBMITTER: Wirthlin ME

PROVIDER: S-EPMC11313673 | biostudies-literature | 2024 Mar

REPOSITORIES: biostudies-literature

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

Wirthlin Morgan E ME Schmid Tobias A TA Elie Julie E JE Zhang Xiaomeng X Kowalczyk Amanda A Redlich Ruby R Shvareva Varvara A VA Rakuljic Ashley A Ji Maria B MB Bhat Ninad S NS Kaplow Irene M IM Schäffer Daniel E DE Lawler Alyssa J AJ Wang Andrew Z AZ Phan BaDoi N BN Annaldasula Siddharth S Brown Ashley R AR Lu Tianyu T Lim Byung Kook BK Azim Eiman E Clark Nathan L NL Meyer Wynn K WK Pond Sergei L Kosakovsky SLK Chikina Maria M Yartsev Michael M MM Pfenning Andreas R AR Andrews Gregory G Armstrong Joel C JC Bianchi Matteo M Birren Bruce W BW Bredemeyer Kevin R KR Breit Ana M AM Christmas Matthew J MJ Clawson Hiram H Damas Joana J Di Palma Federica F Diekhans Mark M Dong Michael X MX Eizirik Eduardo E Fan Kaili K Fanter Cornelia C Foley Nicole M NM Forsberg-Nilsson Karin K Garcia Carlos J CJ Gatesy John J Gazal Steven S Genereux Diane P DP Goodman Linda L Grimshaw Jenna J Halsey Michaela K MK Harris Andrew J AJ Hickey Glenn G Hiller Michael M Hindle Allyson G AG Hubley Robert M RM Hughes Graham M GM Johnson Jeremy J Juan David D Kaplow Irene M IM Karlsson Elinor K EK Keough Kathleen C KC Kirilenko Bogdan B Koepfli Klaus-Peter KP Korstian Jennifer M JM Kowalczyk Amanda A Kozyrev Sergey V SV Lawler Alyssa J AJ Lawless Colleen C Lehmann Thomas T Levesque Danielle L DL Lewin Harris A HA Li Xue X Lind Abigail A Lindblad-Toh Kerstin K Mackay-Smith Ava A Marinescu Voichita D VD Marques-Bonet Tomas T Mason Victor C VC Meadows Jennifer R S JRS Meyer Wynn K WK Moore Jill E JE Moreira Lucas R LR Moreno-Santillan Diana D DD Morrill Kathleen M KM Muntané Gerard G Murphy William J WJ Navarro Arcadi A Nweeia Martin M Ortmann Sylvia S Osmanski Austin A Paten Benedict B Paulat Nicole S NS Pfenning Andreas R AR Phan BaDoi N BN Pollard Katherine S KS Pratt Henry E HE Ray David A DA Reilly Steven K SK Rosen Jeb R JR Ruf Irina I Ryan Louise L Ryder Oliver A OA Sabeti Pardis C PC Schäffer Daniel E DE Serres Aitor A Shapiro Beth B Smit Arian F A AFA Springer Mark M Srinivasan Chaitanya C Steiner Cynthia C Storer Jessica M JM Sullivan Kevin A M KAM Sullivan Patrick F PF Sundström Elisabeth E Supple Megan A MA Swofford Ross R Talbot Joy-El JE Teeling Emma E Turner-Maier Jason J Valenzuela Alejandro A Wagner Franziska F Wallerman Ola O Wang Chao C Wang Juehan J Weng Zhiping Z Wilder Aryn P AP Wirthlin Morgan E ME Xue James R JR Zhang Xiaomeng X

Science (New York, N.Y.) 20240329 6690

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 (<i>Rousettus aegyptiacus</i>) 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 ba ...[more]

PMID: 38422184

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Project description:BackgroundEvolutionary relations of similar segments shared by different protein folds remain controversial, even though many examples of such segments have been found. To date, several methods such as those based on the results of structure comparisons, sequence-based classifications, and sequence-based profile-profile comparisons have been applied to identify such protein segments that possess local similarities in both sequence and structure across protein folds. However, to capture more precise sequence-structure relations, no method reported to date combines structure-based profiles, and sequence-based profiles based on evolutionary information. The former are generally regarded as representing the amino acid preferences at each position of a specific conformation of protein segment. They might reflect the nature of ancient short peptide ancestors, using the results of structural classifications of protein segments.ResultsThis report describes the development and use of "Cross Profile Analysis" to compare sequence-based profiles and structure-based profiles based on amino acid occurrences at each position within a protein segment cluster. Using systematic cross profile analysis, we found structural clusters of 9-residue and 15-residue segments showing remarkably strong correlation with particular sequence profiles. These correlations reflect structural similarities among constituent segments of both sequence-based and structure-based profiles. We also report previously undetectable sequence-structure patterns that transcend protein family and fold boundaries, and present results of the conformational analysis of the deduced peptide of a segment cluster. These results suggest the existence of ancient short-peptide ancestors.ConclusionsCross profile analysis reveals the polyphyletic and convergent evolution of β-hairpin-like structures, which were verified both experimentally and computationally. The results presented here give us new insights into the evolution of short protein segments.

Project description:Uncoupling protein 1 (UCP1) permits non-shivering thermogenesis (NST) when highly expressed in brown adipose tissue (BAT) mitochondria. Exclusive to placental mammals, BAT has commonly been regarded to be advantageous for thermoregulation in hibernators, small-bodied species, and the neonates of larger species. While numerous regulatory control motifs associated with UCP1 transcription have been proposed for murid rodents, it remains unclear whether these are conserved across the eutherian mammal phylogeny and hence essential for UCP1 expression. To address this shortcoming, we conducted a broad comparative survey of putative UCP1 transcriptional regulatory elements in 139 mammals (135 eutherians). We find no evidence for presence of a UCP1 enhancer in monotremes and marsupials, supporting the hypothesis that this control region evolved in a stem eutherian ancestor. We additionally reveal that several putative promoter elements (e.g., CRE-4, CCAAT) identified in murid rodents are not conserved among BAT-expressing eutherians, and together with the putative regulatory region (PRR) and CpG island do not appear to be crucial for UCP1 expression. The specificity and importance of the upTRE, dnTRE, URE1, CRE-2, RARE-2, NBRE, BRE-1, and BRE-2 enhancer elements first described from rats and mice are moreover uncertain as these motifs differ substantially-but generally remain highly conserved-in other BAT-expressing eutherians. Other UCP1 enhancer motifs (CRE-3, PPRE, and RARE-3) as well as the TATA box are also highly conserved in nearly all eutherian lineages with an intact UCP1. While these transcriptional regulatory motifs are generally also maintained in species where this gene is pseudogenized, the loss or degeneration of key basal promoter (e.g., TATA box) and enhancer elements in other UCP1-lacking lineages make it unlikely that the enhancer region is pleiotropic (i.e., co-regulates additional genes). Importantly, differential losses of (or mutations within) putative regulatory elements among the eutherian lineages with an intact UCP1 suggests that the transcriptional control of gene expression is not highly conserved in this mammalian clade.

Dataset Information

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

Publications

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

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