Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird

International audience Over evolutionary time, pathogen challenge shapes the immune phenotype of the host to better respond to an incipient threat. The extent and direction of this selection pressure depends on the local pathogen composition, which is in turn determined by biotic and abiotic feature...

Full description

Bibliographic Details
Published in:Molecular Biology and Evolution
Main Authors: Levy, Hila, Fiddaman, Steven, Vianna, Juliana, Noll, Daly, Clucas, Gemma, Sidhu, Jasmine, Polito, Michael, Bost, Charles, Phillips, Richard, Crofts, Sarah, Miller, Gary, Pistorius, Pierre, Bonadonna, Francesco, Le Bohec, Céline, Barbosa, Andrés, Trathan, Phil, Raya Rey, Andrea, Frantz, Laurent, Hart, Tom, Smith, Adrian
Other Authors: Department of Zoology Oxford, University of Oxford Oxford, Department of Zoology, Peter Medawar Building for Pathogen Research UK, Departamento de Ecosistemas y Medio Ambiente Chile, Pontificia Universidad Católica de Chile (UC), Atkinson Center for a Sustainable Future and Cornell Lab of Ornithology USA, Cornell University New York, Department of Oceanography and Coastal Sciences, Louisiana State University (LSU), Centre d'Études Biologiques de Chizé - UMR 7372 (CEBC), Université de La Rochelle (ULR)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), British Antarctic Survey (BAS), Natural Environment Research Council (NERC), Falklands Conservation, Carnegie Mellon University Pittsburgh (CMU), National Research Foundation Centre of Excellence at the Percy FitzPatrick Institute, Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Université Paul-Valéry - Montpellier 3 (UPVM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut de Recherche pour le Développement (IRD France-Sud ), Département Ecologie, Physiologie et Ethologie (DEPE-IPHC), Institut Pluridisciplinaire Hubert Curien (IPHC), Université de Strasbourg (UNISTRA)-Institut National de Physique Nucléaire et de Physique des Particules du CNRS (IN2P3)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Institut National de Physique Nucléaire et de Physique des Particules du CNRS (IN2P3)-Centre National de la Recherche Scientifique (CNRS), Departamento de Ecología Evolutiva (Museo Nacional de Ciencias Naturales), Museo Nacional de Ciencias Naturales (MNCN), Centro Austral de Investigaciones Científicas Ushuaia (CADIC), Consejo Nacional de Investigaciones Científicas y Técnicas Buenos Aires (CONICET), School of Biological and Chemical Sciences, Queen Mary University of London (QMUL)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2020
Subjects:
Online Access:https://hal.archives-ouvertes.fr/hal-02988644
https://hal.archives-ouvertes.fr/hal-02988644/document
https://hal.archives-ouvertes.fr/hal-02988644/file/Levy%202020%20HAL.pdf
https://doi.org/10.1093/molbev/msaa040
id ftccsdartic:oai:HAL:hal-02988644v1
record_format openpolar
institution Open Polar
collection Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe)
op_collection_id ftccsdartic
language English
topic Gentoo penguin
Antarctica and Southern Ocean
immunogenetics
positive selection
Toll-like receptors
pathogen-mediated selection
[SDV.BA]Life Sciences [q-bio]/Animal biology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
[SDV.NEU.PC]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Psychology and behavior
spellingShingle Gentoo penguin
Antarctica and Southern Ocean
immunogenetics
positive selection
Toll-like receptors
pathogen-mediated selection
[SDV.BA]Life Sciences [q-bio]/Animal biology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
[SDV.NEU.PC]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Psychology and behavior
Levy, Hila
Fiddaman, Steven
Vianna, Juliana
Noll, Daly
Clucas, Gemma
Sidhu, Jasmine
Polito, Michael
Bost, Charles
Phillips, Richard
Crofts, Sarah
Miller, Gary
Pistorius, Pierre
Bonadonna, Francesco
Le Bohec, Céline
Barbosa, Andrés
Trathan, Phil
Raya Rey, Andrea
Frantz, Laurent
Hart, Tom
Smith, Adrian
Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird
topic_facet Gentoo penguin
Antarctica and Southern Ocean
immunogenetics
positive selection
Toll-like receptors
pathogen-mediated selection
[SDV.BA]Life Sciences [q-bio]/Animal biology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
[SDV.NEU.PC]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Psychology and behavior
description International audience Over evolutionary time, pathogen challenge shapes the immune phenotype of the host to better respond to an incipient threat. The extent and direction of this selection pressure depends on the local pathogen composition, which is in turn determined by biotic and abiotic features of the environment. However, little is known about adaptation to local pathogen threats in wild animals. The Gentoo penguin (Pygoscelis papua) is a species complex that lends itself to the study of immune adaptation because of its circumpolar distribution over a large latitudinal range, with little or no admixture between different clades. In this study, we examine the diversity in a key family of innate immune genes - the Toll-like receptors (TLRs) - across the range of the Gentoo. The three TLRs that we investigated present varying levels of diversity, with TLR4 and TLR5 greatly exceeding the diversity of TLR7. We present evidence of positive selection in TLR4 and TLR5, which points to pathogen-driven adaptation to the local pathogen milieu. Finally, we demonstrate that two positively selected co-segregating sites in TLR5 are sufficient to alter the responsiveness of the receptor to its bacterial ligand, flagellin. Taken together, these results suggest that Gentoo penguins have experienced distinct pathogen-driven selection pressures in different environments, which may be important given the role of the Gentoo as a sentinel species in some of the world's most rapidly changing environments.
author2 Department of Zoology Oxford
University of Oxford Oxford
Department of Zoology, Peter Medawar Building for Pathogen Research UK
Departamento de Ecosistemas y Medio Ambiente Chile
Pontificia Universidad Católica de Chile (UC)
Atkinson Center for a Sustainable Future and Cornell Lab of Ornithology USA
Cornell University New York
Department of Oceanography and Coastal Sciences
Louisiana State University (LSU)
Centre d'Études Biologiques de Chizé - UMR 7372 (CEBC)
Université de La Rochelle (ULR)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)
British Antarctic Survey (BAS)
Natural Environment Research Council (NERC)
Falklands Conservation
Carnegie Mellon University Pittsburgh (CMU)
National Research Foundation Centre of Excellence at the Percy FitzPatrick Institute
Centre d’Ecologie Fonctionnelle et Evolutive (CEFE)
Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-École pratique des hautes études (EPHE)
Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Université Paul-Valéry - Montpellier 3 (UPVM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)
Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut de Recherche pour le Développement (IRD France-Sud )
Département Ecologie, Physiologie et Ethologie (DEPE-IPHC)
Institut Pluridisciplinaire Hubert Curien (IPHC)
Université de Strasbourg (UNISTRA)-Institut National de Physique Nucléaire et de Physique des Particules du CNRS (IN2P3)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Institut National de Physique Nucléaire et de Physique des Particules du CNRS (IN2P3)-Centre National de la Recherche Scientifique (CNRS)
Departamento de Ecología Evolutiva (Museo Nacional de Ciencias Naturales)
Museo Nacional de Ciencias Naturales (MNCN)
Centro Austral de Investigaciones Científicas Ushuaia (CADIC)
Consejo Nacional de Investigaciones Científicas y Técnicas Buenos Aires (CONICET)
School of Biological and Chemical Sciences
Queen Mary University of London (QMUL)
format Article in Journal/Newspaper
author Levy, Hila
Fiddaman, Steven
Vianna, Juliana
Noll, Daly
Clucas, Gemma
Sidhu, Jasmine
Polito, Michael
Bost, Charles
Phillips, Richard
Crofts, Sarah
Miller, Gary
Pistorius, Pierre
Bonadonna, Francesco
Le Bohec, Céline
Barbosa, Andrés
Trathan, Phil
Raya Rey, Andrea
Frantz, Laurent
Hart, Tom
Smith, Adrian
author_facet Levy, Hila
Fiddaman, Steven
Vianna, Juliana
Noll, Daly
Clucas, Gemma
Sidhu, Jasmine
Polito, Michael
Bost, Charles
Phillips, Richard
Crofts, Sarah
Miller, Gary
Pistorius, Pierre
Bonadonna, Francesco
Le Bohec, Céline
Barbosa, Andrés
Trathan, Phil
Raya Rey, Andrea
Frantz, Laurent
Hart, Tom
Smith, Adrian
author_sort Levy, Hila
title Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird
title_short Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird
title_full Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird
title_fullStr Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird
title_full_unstemmed Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird
title_sort evidence of pathogen-induced immunogenetic selection across the large geographic range of a wild seabird
publisher HAL CCSD
publishDate 2020
url https://hal.archives-ouvertes.fr/hal-02988644
https://hal.archives-ouvertes.fr/hal-02988644/document
https://hal.archives-ouvertes.fr/hal-02988644/file/Levy%202020%20HAL.pdf
https://doi.org/10.1093/molbev/msaa040
geographic Southern Ocean
geographic_facet Southern Ocean
genre Antarc*
Antarctica
Gentoo penguin
Pygoscelis papua
Southern Ocean
genre_facet Antarc*
Antarctica
Gentoo penguin
Pygoscelis papua
Southern Ocean
op_source ISSN: 0737-4038
EISSN: 1537-1719
Molecular Biology and Evolution
https://hal.archives-ouvertes.fr/hal-02988644
Molecular Biology and Evolution, Oxford University Press (OUP), 2020, 37 (6), pp.1708-1726. ⟨10.1093/molbev/msaa040⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1093/molbev/msaa040
hal-02988644
https://hal.archives-ouvertes.fr/hal-02988644
https://hal.archives-ouvertes.fr/hal-02988644/document
https://hal.archives-ouvertes.fr/hal-02988644/file/Levy%202020%20HAL.pdf
doi:10.1093/molbev/msaa040
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1093/molbev/msaa040
container_title Molecular Biology and Evolution
container_volume 37
container_issue 6
container_start_page 1708
op_container_end_page 1726
_version_ 1766266256736911360
spelling ftccsdartic:oai:HAL:hal-02988644v1 2023-05-15T13:58:09+02:00 Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird Levy, Hila Fiddaman, Steven Vianna, Juliana Noll, Daly Clucas, Gemma Sidhu, Jasmine Polito, Michael Bost, Charles Phillips, Richard Crofts, Sarah Miller, Gary Pistorius, Pierre Bonadonna, Francesco Le Bohec, Céline Barbosa, Andrés Trathan, Phil Raya Rey, Andrea Frantz, Laurent Hart, Tom Smith, Adrian Department of Zoology Oxford University of Oxford Oxford Department of Zoology, Peter Medawar Building for Pathogen Research UK Departamento de Ecosistemas y Medio Ambiente Chile Pontificia Universidad Católica de Chile (UC) Atkinson Center for a Sustainable Future and Cornell Lab of Ornithology USA Cornell University New York Department of Oceanography and Coastal Sciences Louisiana State University (LSU) Centre d'Études Biologiques de Chizé - UMR 7372 (CEBC) Université de La Rochelle (ULR)-Centre National de la Recherche Scientifique (CNRS)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE) British Antarctic Survey (BAS) Natural Environment Research Council (NERC) Falklands Conservation Carnegie Mellon University Pittsburgh (CMU) National Research Foundation Centre of Excellence at the Percy FitzPatrick Institute Centre d’Ecologie Fonctionnelle et Evolutive (CEFE) Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-École pratique des hautes études (EPHE) Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Université Paul-Valéry - Montpellier 3 (UPVM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro) Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut de Recherche pour le Développement (IRD France-Sud ) Département Ecologie, Physiologie et Ethologie (DEPE-IPHC) Institut Pluridisciplinaire Hubert Curien (IPHC) Université de Strasbourg (UNISTRA)-Institut National de Physique Nucléaire et de Physique des Particules du CNRS (IN2P3)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA)-Institut National de Physique Nucléaire et de Physique des Particules du CNRS (IN2P3)-Centre National de la Recherche Scientifique (CNRS) Departamento de Ecología Evolutiva (Museo Nacional de Ciencias Naturales) Museo Nacional de Ciencias Naturales (MNCN) Centro Austral de Investigaciones Científicas Ushuaia (CADIC) Consejo Nacional de Investigaciones Científicas y Técnicas Buenos Aires (CONICET) School of Biological and Chemical Sciences Queen Mary University of London (QMUL) 2020-06-01 https://hal.archives-ouvertes.fr/hal-02988644 https://hal.archives-ouvertes.fr/hal-02988644/document https://hal.archives-ouvertes.fr/hal-02988644/file/Levy%202020%20HAL.pdf https://doi.org/10.1093/molbev/msaa040 en eng HAL CCSD Oxford University Press (OUP) info:eu-repo/semantics/altIdentifier/doi/10.1093/molbev/msaa040 hal-02988644 https://hal.archives-ouvertes.fr/hal-02988644 https://hal.archives-ouvertes.fr/hal-02988644/document https://hal.archives-ouvertes.fr/hal-02988644/file/Levy%202020%20HAL.pdf doi:10.1093/molbev/msaa040 info:eu-repo/semantics/OpenAccess ISSN: 0737-4038 EISSN: 1537-1719 Molecular Biology and Evolution https://hal.archives-ouvertes.fr/hal-02988644 Molecular Biology and Evolution, Oxford University Press (OUP), 2020, 37 (6), pp.1708-1726. ⟨10.1093/molbev/msaa040⟩ Gentoo penguin Antarctica and Southern Ocean immunogenetics positive selection Toll-like receptors pathogen-mediated selection [SDV.BA]Life Sciences [q-bio]/Animal biology [SDE.BE]Environmental Sciences/Biodiversity and Ecology [SDV.NEU.PC]Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC]/Psychology and behavior info:eu-repo/semantics/article Journal articles 2020 ftccsdartic https://doi.org/10.1093/molbev/msaa040 2021-11-21T00:32:09Z International audience Over evolutionary time, pathogen challenge shapes the immune phenotype of the host to better respond to an incipient threat. The extent and direction of this selection pressure depends on the local pathogen composition, which is in turn determined by biotic and abiotic features of the environment. However, little is known about adaptation to local pathogen threats in wild animals. The Gentoo penguin (Pygoscelis papua) is a species complex that lends itself to the study of immune adaptation because of its circumpolar distribution over a large latitudinal range, with little or no admixture between different clades. In this study, we examine the diversity in a key family of innate immune genes - the Toll-like receptors (TLRs) - across the range of the Gentoo. The three TLRs that we investigated present varying levels of diversity, with TLR4 and TLR5 greatly exceeding the diversity of TLR7. We present evidence of positive selection in TLR4 and TLR5, which points to pathogen-driven adaptation to the local pathogen milieu. Finally, we demonstrate that two positively selected co-segregating sites in TLR5 are sufficient to alter the responsiveness of the receptor to its bacterial ligand, flagellin. Taken together, these results suggest that Gentoo penguins have experienced distinct pathogen-driven selection pressures in different environments, which may be important given the role of the Gentoo as a sentinel species in some of the world's most rapidly changing environments. Article in Journal/Newspaper Antarc* Antarctica Gentoo penguin Pygoscelis papua Southern Ocean Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Southern Ocean Molecular Biology and Evolution 37 6 1708 1726