TY - JOUR
T1 - The genomics of ecological flexibility, large brains, and long lives in capuchin monkeys revealed with fecalFACS
AU - Orkin, Joseph D.
AU - Montague, Michael J.
AU - Tejada-Martinez, Daniela
AU - de Manuel, Marc
AU - del Campo, Javier
AU - Hernandez, Saul Cheves
AU - Fiore, Anthony Di
AU - Fontsere, Claudia
AU - Hodgson, Jason A.
AU - Janiak, Mareike C.
AU - Kuderna, Lukas F.K.
AU - Lizano, Esther
AU - Martin, Maria Pia
AU - Niimura, Yoshihito
AU - Perry, George H.
AU - Valverde, Carmen Soto
AU - Tang, Jia
AU - Warren, Wesley C.
AU - de Magalhães, João Pedro
AU - Kawamura, Shoji
AU - Marquès-Bonet, Tomàs
AU - Krawetz, Roman
AU - Melin, Amanda D.
N1 - Funding Information:
2017 SGR 880). C.F. is supported by the “La Caixa” doctoral fellowship program. E.L. is supported by CGL2017-82654-P (MINECO/FEDER, UE). M.C.J. is supported by funding from the Natural Environment Research Council
Funding Information:
ACKNOWLEDGMENTS. We thank R. Blanco Segura and M. M. Chavarria and staff from the Área de Conservación Guanacaste and Ministerio de Ambi-ente y Energía; Jose Alfredo Hernández Ugalde and Angela González Grau from CONAGEBIO in Costa Rica; the administration, volunteers, and veterinarians from Kids Saving the Rainforest, for their help, especially Jennifer Rice and Chip Braman; Kelly Kries, Gwen Duytschaever, Eva Garrett, Jene Weatherhead, Laurie Kennedy, and Yiping Liu for their assistance in the laboratory; Aoife Doherty and Mengjia Li for exploratory analyses of selection in aging-related genes; Patrick Minx and Kim Kyung for assistance with bioinformatics; Eva Wikberg, Fernando Campos, Kathy Jack, Linda Fedigan, and many students, research assistants, and volunteers for their contributions to the PACE database and Santa Rosa project; Jessica Lynch and Hazel Byrne for sharing comparative data; R. Gregory in the Centre for Genomic Research and I. C. Smith in the Advanced Research Computing at the University of Liverpool for the access to the computing resources; and Dr. J. C. Opazo for insightful discussions. Funding was provided by Washington University in St. Louis, the Canada Research Chairs Program, and a National Sciences and Engineering Research Council of Canada Discovery Grant (to A.D.M.); the Alberta Children’s Hospital Research Institute (A.D.M., J.D.O., and M.C.J.); the Beatriu de Pinós postdoctoral programme of the Government of Catalonia’s Secretariat for Universities and Research of the Ministry of Economy and Knowledge 2017 BP 00265 (to J.D.O.); and the Japan Society for the Promotion of Science 15H02421 and 18H04005 (to S.K.). This work was partly funded by a Methuselah Foundation grant (to J.P.d.M.); and the Comisión Nacional de Investigación Científica y Tecnológica Chile through the doctoral studentship number 21170433 and the scholarship from the Higher Education Quality Improvement Program (MECESUP) AUS 2003 (to D.T.-M.). GenAge is funded by a Biotechnology and Biological Sciences Research Council Grant BB/R014949/1 (to J.P.d.M.). T.M.-B. is supported by funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (grant agreement No. 864203), BFU2017-86471-P (MINECO/FEDER, UE), “Unidad de Exce-lencia María de Maeztu”, funded by the Agencia Estatal de Investigación (CEX2018-000792-M), Howard Hughes International Early Career, Obra Social “La Caixa” and Secretaria d’Universitats i Recerca and CERCA Programme del Departament d’Economia i Coneixement de la Generalitat de Catalunya (GRC
Publisher Copyright:
© 2021 National Academy of Sciences. All rights reserved.
PY - 2021/2/16
Y1 - 2021/2/16
N2 - 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 Cebus imitator. 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.
AB - 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 Cebus imitator. 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.
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U2 - 10.1073/pnas.2010632118
DO - 10.1073/pnas.2010632118
M3 - Article
C2 - 33574059
AN - SCOPUS:85101035581
SN - 0027-8424
VL - 118
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 7
M1 - e2010632118
ER -