Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids
Plassais J. vonHoldt B.M. Parker H.G. Carmagnini A. Dubos N. Papa I. Bevant K. Derrien T. Hennelly L.M. Whitaker D.T. Harris A.C. Hogan A.N. Huson H.J. Zaibert V.F. Linderholm A. Haile J. Fest T. Habib B. Sacks B.N. Benecke N. Outram A.K. Sablin M.V. Germonpré M. Larson G. Frantz L. Ostrander E.A.
28 February 2022Cell Press
Current Biology
2022#32Issue 4889 - 897.e9 pp.
Domestic dogs (Canis lupus familiaris) are the most variable-sized mammalian species on Earth, displaying a 40-fold size difference between breeds.1 Although dogs of variable size are found in the archeological record,2–4 the most dramatic shifts in body size are the result of selection over the last two centuries, as dog breeders selected and propagated phenotypic extremes within closed breeding populations.5 Analyses of over 200 domestic breeds have identified approximately 20 body size genes regulating insulin processing, fatty acid metabolism, TGFβ signaling, and skeletal formation.6–10 Of these, insulin-like growth factor 1 (IGF1) predominates, controlling approximately 15% of body size variation between breeds.8 The identification of a functional mutation associated with IGF1 has thus far proven elusive.6,10,11 Here, to identify and elucidate the role of an ancestral IGF1 allele in the propagation of modern canids, we analyzed 1,431 genome sequences from 13 species, including both ancient and modern canids, thus allowing us to define the evolutionary history of both ancestral and derived alleles at this locus. We identified a single variant in an antisense long non-coding RNA (IGF1-AS) that interacts with the IGF1 gene, creating a duplex. While the derived mutation predominates in both modern gray wolves and large domestic breeds, the ancestral allele, which predisposes to small size, was common in small-sized breeds and smaller wild canids. Our analyses demonstrate that this major regulator of canid body size nearly vanished in Pleistocene wolves, before its recent resurgence resulting from human-imposed selection for small-sized breed dogs.
ancient DNA , antisense lncRNA , body size , canid evolution , canine , dog , domestication , IGF1 , long non-coding RNA , wolf
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Cancer Genetics and Comparative Genomics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, MD, United States
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ, United States
School of Biological and Chemical Sciences, Queen Mary University of London, UK, London, United Kingdom
INRAE UMR TETIS, Maison de la Télédétection, Montpellier, France
INSERM, UMR1236-MICMAC, University of Rennes 1, Hematology Department CHU Rennes, Rennes, France
INSERM, UMR1242-COSS, University of Rennes 1, Centre de lutte contre le Cancer Eugène Marquis, CHU Rennes, Rennes, France
CNRS, IGDR-UMR6290, University of Rennes 1, Rennes, France
Mammalian Ecology and Conservation Unit, Veterinary Genetics Laboratory, Department of Population Health and Reproduction, School of Veterinary Medicine, University of California, Davis, Davis, CA, United States
Department of Animal Science, Cornell University, Ithaca, NY, United States
Institute of Archaeology and Steppe Civilizations, Al-Farabi Kazakh National University, Almaty, Kazakhstan
Centre for Paleogenomics, Department of Geological Sciences, Stockholm University, Stockholm, Sweden
The Paleogenomics and Bio-Archaeology Research Network, Research Laboratory for Archaeology and History of Art, University of Oxford, UK, Oxford, United Kingdom
Department of Animal Ecology and Conservation Biology, Wildlife Institute of India, Dehradun, India
Scientific Department of the Head Office, German Archaeological Institute, Berlin, Germany
Department of Archaeology, University of Exeter, Laver Building, UK, Exeter, United Kingdom
Zoological Institute of the Russian Academy of Sciences, Saint Petersburg, Russian Federation
Royal Belgian Institute of Natural Sciences, Brussels, Belgium
Paleogenetics Group, Department of Veterinary Sciences, Ludwig Maximilian University, Munich, Germany
Cancer Genetics and Comparative Genomics Branch
Department of Ecology and Evolutionary Biology
School of Biological and Chemical Sciences
INRAE UMR TETIS
INSERM
INSERM
CNRS
Mammalian Ecology and Conservation Unit
Department of Animal Science
Institute of Archaeology and Steppe Civilizations
Centre for Paleogenomics
The Paleogenomics and Bio-Archaeology Research Network
Department of Animal Ecology and Conservation Biology
Scientific Department of the Head Office
Department of Archaeology
Zoological Institute of the Russian Academy of Sciences
Royal Belgian Institute of Natural Sciences
Paleogenetics Group
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