Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids
International audience Domestic dogs (Canis lupus familiaris) are the most variable-sized mammalian species on Earth, displaying a 40-fold size difference between breeds. Although dogs of variable size are found in the archeological record, the most dramatic shifts in body size are the result of sel...
Published in: | Current Biology |
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Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , |
Other Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
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HAL CCSD
2022
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Subjects: | |
Online Access: | https://hal.science/hal-03555249 https://hal.science/hal-03555249/document https://hal.science/hal-03555249/file/Plassais_Current%20Biology_2022.pdf https://doi.org/10.1016/j.cub.2021.12.036 |
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Inserm: HAL (Institut national de la santé et de la recherche médicale) |
op_collection_id |
ftinserm |
language |
English |
topic |
IGF1 ancient DNA antisense lncRNA body size canid evolution canine dog domestication long non-coding RNA wolf [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics |
spellingShingle |
IGF1 ancient DNA antisense lncRNA body size canid evolution canine dog domestication long non-coding RNA wolf [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics Plassais, Jocelyn Vonholdt, Bridgett M Parker, Heidi G Carmagnini, Alberto Dubos, Nicolas Papa, Ilenia Bevant, Kevin Derrien, Thomas Hennelly, Lauren M Whitaker, D Thad Harris, Alex C Hogan, Andrew N Huson, Heather J Zaibert, Victor F Linderholm, Anna Haile, James Fest, Thierry Habib, Bilal Sacks, Benjamin N Benecke, Norbert Outram, Alan K Sablin, Mikhail V Germonpré, Mietje Larson, Greger Frantz, Laurent Ostrander, Elaine A Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids |
topic_facet |
IGF1 ancient DNA antisense lncRNA body size canid evolution canine dog domestication long non-coding RNA wolf [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics |
description |
International audience Domestic dogs (Canis lupus familiaris) are the most variable-sized mammalian species on Earth, displaying a 40-fold size difference between breeds. Although dogs of variable size are found in the archeological record, 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. Analyses of over 200 domestic breeds have identified approximately 20 body size genes regulating insulin processing, fatty acid metabolism, TGFβ signaling, and skeletal formation. Of these, insulin-like growth factor 1 (IGF1) predominates, controlling approximately 15% of body size variation between breeds. The identification of a functional mutation associated with IGF1 has thus far proven elusive. 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. |
author2 |
National Human Genome Research Institute (NHGRI) Princeton University Queen Mary University of London (QMUL) Territoires, Environnement, Télédétection et Information Spatiale (UMR TETIS) Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-AgroParisTech-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) Microenvironment and B-cells: Immunopathology,Cell Differentiation, and Cancer (MOBIDIC) Université de Rennes (UR)-Etablissement français du sang Rennes (EFS Bretagne)-Institut National de la Santé et de la Recherche Médicale (INSERM) Microenvironment, Cell Differentiation, Immunology and Cancer (MICMAC) Université de Rennes (UR)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ) Hôpital Sud CHU Rennes Centre Hospitalier Universitaire de Rennes CHU Rennes = Rennes University Hospital Ponchaillou Chemistry, Oncogenesis, Stress and Signaling (COSS) Université de Rennes (UR)-CRLCC Eugène Marquis (CRLCC) UNICANCER-UNICANCER-Institut National de la Santé et de la Recherche Médicale (INSERM) CRLCC Eugène Marquis (CRLCC) UNICANCER Institut de Génétique et Développement de Rennes (IGDR) Université de Rennes (UR)-Centre National de la Recherche Scientifique (CNRS)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ) University of California Davis (UC Davis) University of California (UC) Cornell University New York Al-Farabi Kazakh National University Almaty (KazNU) Stockholm University University of Oxford German Archaeological Institute (DAI) University of Exeter Zoological Institute of Russian Academy of Sciences Russian Academy of Sciences Moscow (RAS) Institut Royal des Sciences Naturelles de Belgique = Royal Belgian Institute of Natural Sciences (IRSNB / RBINS) Ludwig Maximilian University Munich = Ludwig Maximilians Universität München (LMU) Intramural Program of the National Human Genome Research Institute (J.P., H.G.P., A.N.H., and E.A.O.). J.P. is also funded by Region Bretagne and Ligue Contre le Cancer. B.M.v.H. is funded by Princeton University. L.F., J.H., and G.L. were supported by the ERC (grant ERC-2013-StG-337574-UNDEAD and ERC-2019-StG-853272-PALAEOFARM) and Natural Environment Research Council grants (NE/K005243/1 and NE/K003259/1). L.F. and A.C. were supported by the Wellcome Trust (210119/Z/18/Z). B.H.’s research was funded by DST, the Government of India, and Maharashtra Forest Department. |
format |
Article in Journal/Newspaper |
author |
Plassais, Jocelyn Vonholdt, Bridgett M Parker, Heidi G Carmagnini, Alberto Dubos, Nicolas Papa, Ilenia Bevant, Kevin Derrien, Thomas Hennelly, Lauren M Whitaker, D Thad Harris, Alex C Hogan, Andrew N Huson, Heather J Zaibert, Victor F Linderholm, Anna Haile, James Fest, Thierry Habib, Bilal Sacks, Benjamin N Benecke, Norbert Outram, Alan K Sablin, Mikhail V Germonpré, Mietje Larson, Greger Frantz, Laurent Ostrander, Elaine A |
author_facet |
Plassais, Jocelyn Vonholdt, Bridgett M Parker, Heidi G Carmagnini, Alberto Dubos, Nicolas Papa, Ilenia Bevant, Kevin Derrien, Thomas Hennelly, Lauren M Whitaker, D Thad Harris, Alex C Hogan, Andrew N Huson, Heather J Zaibert, Victor F Linderholm, Anna Haile, James Fest, Thierry Habib, Bilal Sacks, Benjamin N Benecke, Norbert Outram, Alan K Sablin, Mikhail V Germonpré, Mietje Larson, Greger Frantz, Laurent Ostrander, Elaine A |
author_sort |
Plassais, Jocelyn |
title |
Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids |
title_short |
Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids |
title_full |
Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids |
title_fullStr |
Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids |
title_full_unstemmed |
Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids |
title_sort |
natural and human-driven selection of a single non-coding body size variant in ancient and modern canids |
publisher |
HAL CCSD |
publishDate |
2022 |
url |
https://hal.science/hal-03555249 https://hal.science/hal-03555249/document https://hal.science/hal-03555249/file/Plassais_Current%20Biology_2022.pdf https://doi.org/10.1016/j.cub.2021.12.036 |
genre |
Canis lupus |
genre_facet |
Canis lupus |
op_source |
ISSN: 0960-9822 EISSN: 1879-0445 Current Biology - CB https://hal.science/hal-03555249 Current Biology - CB, 2022, 32 (4), pp.889-897.e9. ⟨10.1016/j.cub.2021.12.036⟩ |
op_relation |
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op_rights |
http://creativecommons.org/licenses/by-nc-nd/ info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.1016/j.cub.2021.12.036 |
container_title |
Current Biology |
container_volume |
32 |
container_issue |
4 |
container_start_page |
889 |
op_container_end_page |
897.e9 |
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spelling |
ftinserm:oai:HAL:hal-03555249v1 2024-06-23T07:52:00+00:00 Natural and human-driven selection of a single non-coding body size variant in ancient and modern canids Plassais, Jocelyn Vonholdt, Bridgett M Parker, Heidi G Carmagnini, Alberto Dubos, Nicolas Papa, Ilenia Bevant, Kevin Derrien, Thomas Hennelly, Lauren M Whitaker, D Thad Harris, Alex C Hogan, Andrew N Huson, Heather J Zaibert, Victor F Linderholm, Anna Haile, James Fest, Thierry Habib, Bilal Sacks, Benjamin N Benecke, Norbert Outram, Alan K Sablin, Mikhail V Germonpré, Mietje Larson, Greger Frantz, Laurent Ostrander, Elaine A National Human Genome Research Institute (NHGRI) Princeton University Queen Mary University of London (QMUL) Territoires, Environnement, Télédétection et Information Spatiale (UMR TETIS) Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-AgroParisTech-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) Microenvironment and B-cells: Immunopathology,Cell Differentiation, and Cancer (MOBIDIC) Université de Rennes (UR)-Etablissement français du sang Rennes (EFS Bretagne)-Institut National de la Santé et de la Recherche Médicale (INSERM) Microenvironment, Cell Differentiation, Immunology and Cancer (MICMAC) Université de Rennes (UR)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ) Hôpital Sud CHU Rennes Centre Hospitalier Universitaire de Rennes CHU Rennes = Rennes University Hospital Ponchaillou Chemistry, Oncogenesis, Stress and Signaling (COSS) Université de Rennes (UR)-CRLCC Eugène Marquis (CRLCC) UNICANCER-UNICANCER-Institut National de la Santé et de la Recherche Médicale (INSERM) CRLCC Eugène Marquis (CRLCC) UNICANCER Institut de Génétique et Développement de Rennes (IGDR) Université de Rennes (UR)-Centre National de la Recherche Scientifique (CNRS)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ) University of California Davis (UC Davis) University of California (UC) Cornell University New York Al-Farabi Kazakh National University Almaty (KazNU) Stockholm University University of Oxford German Archaeological Institute (DAI) University of Exeter Zoological Institute of Russian Academy of Sciences Russian Academy of Sciences Moscow (RAS) Institut Royal des Sciences Naturelles de Belgique = Royal Belgian Institute of Natural Sciences (IRSNB / RBINS) Ludwig Maximilian University Munich = Ludwig Maximilians Universität München (LMU) Intramural Program of the National Human Genome Research Institute (J.P., H.G.P., A.N.H., and E.A.O.). J.P. is also funded by Region Bretagne and Ligue Contre le Cancer. B.M.v.H. is funded by Princeton University. L.F., J.H., and G.L. were supported by the ERC (grant ERC-2013-StG-337574-UNDEAD and ERC-2019-StG-853272-PALAEOFARM) and Natural Environment Research Council grants (NE/K005243/1 and NE/K003259/1). L.F. and A.C. were supported by the Wellcome Trust (210119/Z/18/Z). B.H.’s research was funded by DST, the Government of India, and Maharashtra Forest Department. 2022-02 https://hal.science/hal-03555249 https://hal.science/hal-03555249/document https://hal.science/hal-03555249/file/Plassais_Current%20Biology_2022.pdf https://doi.org/10.1016/j.cub.2021.12.036 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.cub.2021.12.036 info:eu-repo/semantics/altIdentifier/pmid/35090588 hal-03555249 https://hal.science/hal-03555249 https://hal.science/hal-03555249/document https://hal.science/hal-03555249/file/Plassais_Current%20Biology_2022.pdf doi:10.1016/j.cub.2021.12.036 PUBMED: 35090588 PUBMEDCENTRAL: PMC8891063 WOS: 000772929200006 http://creativecommons.org/licenses/by-nc-nd/ info:eu-repo/semantics/OpenAccess ISSN: 0960-9822 EISSN: 1879-0445 Current Biology - CB https://hal.science/hal-03555249 Current Biology - CB, 2022, 32 (4), pp.889-897.e9. ⟨10.1016/j.cub.2021.12.036⟩ IGF1 ancient DNA antisense lncRNA body size canid evolution canine dog domestication long non-coding RNA wolf [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDV.GEN.GA]Life Sciences [q-bio]/Genetics/Animal genetics info:eu-repo/semantics/article Journal articles 2022 ftinserm https://doi.org/10.1016/j.cub.2021.12.036 2024-06-10T23:58:34Z International audience Domestic dogs (Canis lupus familiaris) are the most variable-sized mammalian species on Earth, displaying a 40-fold size difference between breeds. Although dogs of variable size are found in the archeological record, 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. Analyses of over 200 domestic breeds have identified approximately 20 body size genes regulating insulin processing, fatty acid metabolism, TGFβ signaling, and skeletal formation. Of these, insulin-like growth factor 1 (IGF1) predominates, controlling approximately 15% of body size variation between breeds. The identification of a functional mutation associated with IGF1 has thus far proven elusive. 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. Article in Journal/Newspaper Canis lupus Inserm: HAL (Institut national de la santé et de la recherche médicale) Current Biology 32 4 889 897.e9 |