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

Abstract 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 depend on the local pathogen composition, which is in turn determined by biotic and abiotic features of the enviro...

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Published in:Molecular Biology and Evolution
Main Authors: Levy, Hila, Fiddaman, Steven R, Vianna, Juliana A, Noll, Daly, Clucas, Gemma V, Sidhu, Jasmine K H, Polito, Michael J, Bost, Charles A, Phillips, Richard A, Crofts, Sarah, Miller, Gary D, Pistorius, Pierre, Bonnadonna, Francesco, Le Bohec, Céline, Barbosa, Andrés, Trathan, Phil, Raya Rey, Andrea, Frantz, Laurent A F, Hart, Tom, Smith, Adrian L
Other Authors: Yeager, Meredith, Oxford Clarendon Fund, Biotechnology and Biological Sciences Research Council, BBSRC, CONICYT PIA, Spanish Ministry of Science, Institut Polaire Français Paul-Emile Victor, Laboratoire International Associé 647 “BioSensib”, CSM/CNRS-University of Strasbourg
Format: Article in Journal/Newspaper
Language:English
Published: Oxford University Press (OUP) 2020
Subjects:
Online Access:http://dx.doi.org/10.1093/molbev/msaa040
http://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msaa040/32931989/msaa040.pdf
http://academic.oup.com/mbe/article-pdf/37/6/1708/33317007/msaa040.pdf
id croxfordunivpr:10.1093/molbev/msaa040
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spelling croxfordunivpr:10.1093/molbev/msaa040 2024-06-09T07:46:06+00:00 Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird Levy, Hila Fiddaman, Steven R Vianna, Juliana A Noll, Daly Clucas, Gemma V Sidhu, Jasmine K H Polito, Michael J Bost, Charles A Phillips, Richard A Crofts, Sarah Miller, Gary D Pistorius, Pierre Bonnadonna, Francesco Le Bohec, Céline Barbosa, Andrés Trathan, Phil Raya Rey, Andrea Frantz, Laurent A F Hart, Tom Smith, Adrian L Yeager, Meredith Oxford Clarendon Fund Biotechnology and Biological Sciences Research Council BBSRC CONICYT PIA Spanish Ministry of Science Institut Polaire Français Paul-Emile Victor Laboratoire International Associé 647 “BioSensib” CSM/CNRS-University of Strasbourg 2020 http://dx.doi.org/10.1093/molbev/msaa040 http://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msaa040/32931989/msaa040.pdf http://academic.oup.com/mbe/article-pdf/37/6/1708/33317007/msaa040.pdf en eng Oxford University Press (OUP) http://creativecommons.org/licenses/by/4.0/ Molecular Biology and Evolution volume 37, issue 6, page 1708-1726 ISSN 0737-4038 1537-1719 journal-article 2020 croxfordunivpr https://doi.org/10.1093/molbev/msaa040 2024-05-10T13:14:33Z Abstract 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 depend 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 penguin. 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 cosegregating 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 penguin as a sentinel species in some of the world’s most rapidly changing environments. Article in Journal/Newspaper Gentoo penguin Pygoscelis papua Oxford University Press Molecular Biology and Evolution 37 6 1708 1726
institution Open Polar
collection Oxford University Press
op_collection_id croxfordunivpr
language English
description Abstract 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 depend 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 penguin. 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 cosegregating 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 penguin as a sentinel species in some of the world’s most rapidly changing environments.
author2 Yeager, Meredith
Oxford Clarendon Fund
Biotechnology and Biological Sciences Research Council
BBSRC
CONICYT PIA
Spanish Ministry of Science
Institut Polaire Français Paul-Emile Victor
Laboratoire International Associé 647 “BioSensib”
CSM/CNRS-University of Strasbourg
format Article in Journal/Newspaper
author Levy, Hila
Fiddaman, Steven R
Vianna, Juliana A
Noll, Daly
Clucas, Gemma V
Sidhu, Jasmine K H
Polito, Michael J
Bost, Charles A
Phillips, Richard A
Crofts, Sarah
Miller, Gary D
Pistorius, Pierre
Bonnadonna, Francesco
Le Bohec, Céline
Barbosa, Andrés
Trathan, Phil
Raya Rey, Andrea
Frantz, Laurent A F
Hart, Tom
Smith, Adrian L
spellingShingle Levy, Hila
Fiddaman, Steven R
Vianna, Juliana A
Noll, Daly
Clucas, Gemma V
Sidhu, Jasmine K H
Polito, Michael J
Bost, Charles A
Phillips, Richard A
Crofts, Sarah
Miller, Gary D
Pistorius, Pierre
Bonnadonna, Francesco
Le Bohec, Céline
Barbosa, Andrés
Trathan, Phil
Raya Rey, Andrea
Frantz, Laurent A F
Hart, Tom
Smith, Adrian L
Evidence of Pathogen-Induced Immunogenetic Selection across the Large Geographic Range of a Wild Seabird
author_facet Levy, Hila
Fiddaman, Steven R
Vianna, Juliana A
Noll, Daly
Clucas, Gemma V
Sidhu, Jasmine K H
Polito, Michael J
Bost, Charles A
Phillips, Richard A
Crofts, Sarah
Miller, Gary D
Pistorius, Pierre
Bonnadonna, Francesco
Le Bohec, Céline
Barbosa, Andrés
Trathan, Phil
Raya Rey, Andrea
Frantz, Laurent A F
Hart, Tom
Smith, Adrian L
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 Oxford University Press (OUP)
publishDate 2020
url http://dx.doi.org/10.1093/molbev/msaa040
http://academic.oup.com/mbe/advance-article-pdf/doi/10.1093/molbev/msaa040/32931989/msaa040.pdf
http://academic.oup.com/mbe/article-pdf/37/6/1708/33317007/msaa040.pdf
genre Gentoo penguin
Pygoscelis papua
genre_facet Gentoo penguin
Pygoscelis papua
op_source Molecular Biology and Evolution
volume 37, issue 6, page 1708-1726
ISSN 0737-4038 1537-1719
op_rights http://creativecommons.org/licenses/by/4.0/
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
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