The genomics of ecological flexibility, large brains, and long lives in capuchin monkeys revealed with fecalFACS

Orkin, JD; Montague, MJ; Tejada-Martinez, D; de Manuel, M; Del Campo, J; Cheves Hernandez, S; Di Fiore, A; Fontsere, C; Hodgson, JA; Janiak, MC; Kuderna, LFK; Lizano, E; Martin, MP; Niimura, Y; Perry, GH; Valverde, CS; Tang, J; Warren, WC; de Magalhães, JP; Kawamura, S; Marquès-Bonet, T; Krawetz, R; Melin, AD

Abstract

Ecological flexibility, extended lifespans, and large brains have long intrigued evolutionary biologists, and comparative genomics offers an efficient and effective tool for generating new insights into the evolution of such traits. Studies of capuchin monkeys are particularly well situated to shed light on the selective pressures and genetic underpinnings of local adaptation to diverse habitats, longevity, and brain development. Distributed widely across Central and South America, they are inventive and extractive foragers, known for their sensorimotor intelligence. Capuchins have among the largest relative brain size of any monkey and a lifespan that exceeds 50 y, despite their small (3 to 5 kg) body size. We assemble and annotate a de novo reference genome for Through high-depth sequencing of DNA derived from blood, various tissues, and feces via fluorescence-activated cell sorting (fecalFACS) to isolate monkey epithelial cells, we compared genomes of capuchin populations from tropical dry forests and lowland rainforests and identified population divergence in genes involved in water balance, kidney function, and metabolism. Through a comparative genomics approach spanning a wide diversity of mammals, we identified genes under positive selection associated with longevity and brain development. Additionally, we provide a technological advancement in the use of noninvasive genomics for studies of free-ranging mammals. Our intra- and interspecific comparative study of capuchin genomics provides insights into processes underlying local adaptation to diverse and physiologically challenging environments, as well as the molecular basis of brain evolution and longevity. [Abstract copyright: Copyright © 2021 the Author(s). Published by PNAS.]

Citation

Orkin, J., Montague, M., Tejada-Martinez, D., de Manuel, M., Del Campo, J., Cheves Hernandez, S., …Melin, A. (2021). The genomics of ecological flexibility, large brains, and long lives in capuchin monkeys revealed with fecalFACS. Proceedings of the National Academy of Sciences, 118(7), e2010632118. https://doi.org/10.1073/pnas.2010632118

• Journal Article Type: Article
• Acceptance Date: Nov 12, 2020
• Online Publication Date: Feb 11, 2021
• Publication Date: Feb 16, 2021
• Deposit Date: Feb 26, 2021
• Publicly Available Date: Feb 26, 2021
• Journal: Proceedings of the National Academy of Sciences
• Electronic ISSN: 1091-6490
• Publisher: National Academy of Sciences
• Volume: 118
• Issue: 7
• Pages: e2010632118
• DOI: https://doi.org/10.1073/pnas.2010632118
• Publisher URL: https://doi.org/10.1073/pnas.2010632118
• Related Public URLs: http://www.pnas.org/
• Additional Information: Additional Information : ** From PubMed via Jisc Publications Router **Journal IDs: eissn 1091-6490 **Article IDs: pubmed: 33574059; pii: 2010632118 **History: published 16-02-2021; Funders : Washington University in St. Louis;Canada Research Chairs Program;National Sciences and Engineering Research Council of Canada Discovery Grant;Alberta Children’s Hospital Research Institute;Beatriu de Pinós postdoctoral programme of the Government of Catalonia’s Secretariat for Universities and Research of the Ministry of Economy and Knowledge;Japan Society for the Promotion of Science;Methuselah Foundation;Comisión Nacional de Investigación Científica y Tecnológica Chile;Higher Education Quality Improvement Program (MECESUP);Biotechnology and Biological Sciences Research Council Grant;European Research Council (ERC);MINECO/FEDER, UE;Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya;Natural Environment Research Council (NERC); Projects : European Union’s Horizon 2020;Unidad de Excelencia María de Maeztu; Grant Number: 2017 BP 00265; Grant Number: 15H02421 and 18H04005; Grant Number: 21170433; Grant Number: AUS 2003; Grant Number: BB/R014949/1; Grant Number: 864203; Grant Number: BFU2017-86471-P; Grant Number: GRC 2017 SGR 880; Grant Number: CGL2017-82654-P; Grant Number: NE/T000341/1