Parallel adaptation of rabbit populations to myxoma virus

Joel M. Alves; Miguel Carneiro; Jade Y. Cheng; Ana Lemos de Matos; Masmudur M. Rahman; Liisa Loog; Paula F. Campos; Nathan Wales; Anders Eriksson; Andrea Manica; Tanja Strive; Stephen C. Graham; Sandra Afonso; Diana J. Bell; Laura Belmont; Jonathan P. Day; Susan J. Fuller; Stéphane Marchandeau; William J. Palmer; Guillaume Queney; Alison K. Surridge; Filipe G. Vieira; Grant McFadden; Rasmus Nielsen; M. Thomas P. Gilbert; Pedro J. Esteves; Nuno Ferrand; Francis M. Jiggins

doi:10.1126/science.aau7285

Parallel adaptation of rabbit populations to myxoma virus

Joel M. Alves, Miguel Carneiro, Jade Y. Cheng, Ana Lemos de Matos, Masmudur M. Rahman, Liisa Loog, Paula F. Campos, Nathan Wales, Anders Eriksson, Andrea Manica, Tanja Strive, Stephen C. Graham, Sandra Afonso, Diana J. Bell, Laura Belmont, Jonathan P. Day, Susan J. Fuller, Stéphane Marchandeau, William J. Palmer, Guillaume QueneyAlison K. Surridge, Filipe G. Vieira, Grant McFadden, Rasmus Nielsen, M. Thomas P. Gilbert, Pedro J. Esteves, Nuno Ferrand, Francis M. Jiggins

Science

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Abstract

In the 1950s the myxoma virus was released into European rabbit populations in Australia and Europe, decimating populations and resulting in the rapid evolution of resistance. We investigated the genetic basis of resistance by comparing the exomes of rabbits collected before and after the pandemic. We found a strong pattern of parallel evolution, with selection on standing genetic variation favoring the same alleles in Australia, France, and the United Kingdom. Many of these changes occurred in immunity-related genes, supporting a polygenic basis of resistance. We experimentally validated the role of several genes in viral replication and showed that selection acting on an interferon protein has increased the protein’s antiviral effect.

Original language	English
Pages (from-to)	1319-1326
Number of pages	8
Journal	Science
Volume	363
Issue number	6433
DOIs	https://doi.org/10.1126/science.aau7285
Publication status	Published - 22 Mar 2019

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Alves, J. M., Carneiro, M., Cheng, J. Y., de Matos, A. L., Rahman, M. M., Loog, L., Campos, P. F., Wales, N., Eriksson, A., Manica, A., Strive, T., Graham, S. C., Afonso, S., Bell, D. J., Belmont, L., Day, J. P., Fuller, S. J., Marchandeau, S., Palmer, W. J., ... Jiggins, F. M. (2019). Parallel adaptation of rabbit populations to myxoma virus. Science, 363(6433), 1319-1326. https://doi.org/10.1126/science.aau7285

@article{5f1a633f08cc490782d3550da9b16548,

title = "Parallel adaptation of rabbit populations to myxoma virus",

abstract = "In the 1950s the myxoma virus was released into European rabbit populations in Australia and Europe, decimating populations and resulting in the rapid evolution of resistance. We investigated the genetic basis of resistance by comparing the exomes of rabbits collected before and after the pandemic. We found a strong pattern of parallel evolution, with selection on standing genetic variation favoring the same alleles in Australia, France, and the United Kingdom. Many of these changes occurred in immunity-related genes, supporting a polygenic basis of resistance. We experimentally validated the role of several genes in viral replication and showed that selection acting on an interferon protein has increased the protein{\textquoteright}s antiviral effect.",

author = "Alves, {Joel M.} and Miguel Carneiro and Cheng, {Jade Y.} and {de Matos}, {Ana Lemos} and Rahman, {Masmudur M.} and Liisa Loog and Campos, {Paula F.} and Nathan Wales and Anders Eriksson and Andrea Manica and Tanja Strive and Graham, {Stephen C.} and Sandra Afonso and Bell, {Diana J.} and Laura Belmont and Day, {Jonathan P.} and Fuller, {Susan J.} and St{\'e}phane Marchandeau and Palmer, {William J.} and Guillaume Queney and Surridge, {Alison K.} and Vieira, {Filipe G.} and Grant McFadden and Rasmus Nielsen and Gilbert, {M. Thomas P.} and Esteves, {Pedro J.} and Nuno Ferrand and Jiggins, {Francis M.}",

note = "Funding Information: This work was funded by grants from the Programa Operacional Potencial Humano?Quadro de Refer?ncia Estrat?gica Nacional funds from the European Social Fund and Portuguese Minist?rio da Ci?ncia, Tecnologia e Ensino Superior to M.C. (IF/00283/2014/ CP1256/CT0012), to P.J.E. (IF/00376/2015), and to J.M.A. (SFRH/BD/72381/2010). J.M.A. was supported by a travel grant from the Middleton Fund (Cambridge) to undertake work in the Centre of GeoGenetics (Copenhagen). A.M., F.M.J., and L.L. were supported by the European Research Council (grants 647787-LocalAdaptation, 281668, and 339941-ADAPT, respectively). M.T.P.G. was funded by Lundbeck Foundation grant R52-A5062 (Pathogen Palaeogenomics). The McFadden lab is supported by National Institutes of Health (NIH) grant R01 AI080607. S.C.G. holds a Sir Henry Dale Fellowship, cofunded by the Wellcome Trust and the Royal Society (098406/Z/12/Z). We thank the Australian Museum, American Museum of Natural History, Booth Museum of Natural History, Natural History Museum (London), Museum of Comparative Zoology (Harvard University), Mus?e des Confluences, Mus?um National d?Histoire Naturelle (Paris), Museum Victoria, Queensland Museum, Museum of Zoology (University of Michigan), Smithsonian Institution National Museum of Natural History, and all the curators and museum technicians who generously sampled and provided historical samples; M.-D. Wandhammer from Mus?e Zoologique de la Ville de Strasbourg, who helped to track historical French samples; and the British Association for Shooting and Conservation (BASC), A. Holroyd, S. Whitehead, and all volunteers who contributed with modern rabbit samples. P. Kerr provided rabbit samples from NSW (Australia) from before the emergence of RHDV. P. Elsworth and W. Dobbie contributed Queensland post-RHDV samples. C. Crump provided human cell lines expressing VPS4. R. Fonseca provided valuable advice concerning ancient DNA bioinformatics. Publisher Copyright: {\textcopyright} 2017 The Authors.",

year = "2019",

month = mar,

day = "22",

doi = "10.1126/science.aau7285",

language = "English",

volume = "363",

pages = "1319--1326",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6433",

}

Alves, JM, Carneiro, M, Cheng, JY, de Matos, AL, Rahman, MM, Loog, L, Campos, PF, Wales, N, Eriksson, A, Manica, A, Strive, T, Graham, SC, Afonso, S, Bell, DJ, Belmont, L, Day, JP, Fuller, SJ, Marchandeau, S, Palmer, WJ, Queney, G, Surridge, AK, Vieira, FG, McFadden, G, Nielsen, R, Gilbert, MTP, Esteves, PJ, Ferrand, N & Jiggins, FM 2019, 'Parallel adaptation of rabbit populations to myxoma virus', Science, vol. 363, no. 6433, pp. 1319-1326. https://doi.org/10.1126/science.aau7285

TY - JOUR

T1 - Parallel adaptation of rabbit populations to myxoma virus

AU - Alves, Joel M.

AU - Carneiro, Miguel

AU - Cheng, Jade Y.

AU - de Matos, Ana Lemos

AU - Rahman, Masmudur M.

AU - Loog, Liisa

AU - Campos, Paula F.

AU - Wales, Nathan

AU - Eriksson, Anders

AU - Manica, Andrea

AU - Strive, Tanja

AU - Graham, Stephen C.

AU - Afonso, Sandra

AU - Bell, Diana J.

AU - Belmont, Laura

AU - Day, Jonathan P.

AU - Fuller, Susan J.

AU - Marchandeau, Stéphane

AU - Palmer, William J.

AU - Queney, Guillaume

AU - Surridge, Alison K.

AU - Vieira, Filipe G.

AU - McFadden, Grant

AU - Nielsen, Rasmus

AU - Gilbert, M. Thomas P.

AU - Esteves, Pedro J.

AU - Ferrand, Nuno

AU - Jiggins, Francis M.

N1 - Funding Information: This work was funded by grants from the Programa Operacional Potencial Humano?Quadro de Refer?ncia Estrat?gica Nacional funds from the European Social Fund and Portuguese Minist?rio da Ci?ncia, Tecnologia e Ensino Superior to M.C. (IF/00283/2014/ CP1256/CT0012), to P.J.E. (IF/00376/2015), and to J.M.A. (SFRH/BD/72381/2010). J.M.A. was supported by a travel grant from the Middleton Fund (Cambridge) to undertake work in the Centre of GeoGenetics (Copenhagen). A.M., F.M.J., and L.L. were supported by the European Research Council (grants 647787-LocalAdaptation, 281668, and 339941-ADAPT, respectively). M.T.P.G. was funded by Lundbeck Foundation grant R52-A5062 (Pathogen Palaeogenomics). The McFadden lab is supported by National Institutes of Health (NIH) grant R01 AI080607. S.C.G. holds a Sir Henry Dale Fellowship, cofunded by the Wellcome Trust and the Royal Society (098406/Z/12/Z). We thank the Australian Museum, American Museum of Natural History, Booth Museum of Natural History, Natural History Museum (London), Museum of Comparative Zoology (Harvard University), Mus?e des Confluences, Mus?um National d?Histoire Naturelle (Paris), Museum Victoria, Queensland Museum, Museum of Zoology (University of Michigan), Smithsonian Institution National Museum of Natural History, and all the curators and museum technicians who generously sampled and provided historical samples; M.-D. Wandhammer from Mus?e Zoologique de la Ville de Strasbourg, who helped to track historical French samples; and the British Association for Shooting and Conservation (BASC), A. Holroyd, S. Whitehead, and all volunteers who contributed with modern rabbit samples. P. Kerr provided rabbit samples from NSW (Australia) from before the emergence of RHDV. P. Elsworth and W. Dobbie contributed Queensland post-RHDV samples. C. Crump provided human cell lines expressing VPS4. R. Fonseca provided valuable advice concerning ancient DNA bioinformatics. Publisher Copyright: © 2017 The Authors.

PY - 2019/3/22

Y1 - 2019/3/22

N2 - In the 1950s the myxoma virus was released into European rabbit populations in Australia and Europe, decimating populations and resulting in the rapid evolution of resistance. We investigated the genetic basis of resistance by comparing the exomes of rabbits collected before and after the pandemic. We found a strong pattern of parallel evolution, with selection on standing genetic variation favoring the same alleles in Australia, France, and the United Kingdom. Many of these changes occurred in immunity-related genes, supporting a polygenic basis of resistance. We experimentally validated the role of several genes in viral replication and showed that selection acting on an interferon protein has increased the protein’s antiviral effect.

AB - In the 1950s the myxoma virus was released into European rabbit populations in Australia and Europe, decimating populations and resulting in the rapid evolution of resistance. We investigated the genetic basis of resistance by comparing the exomes of rabbits collected before and after the pandemic. We found a strong pattern of parallel evolution, with selection on standing genetic variation favoring the same alleles in Australia, France, and the United Kingdom. Many of these changes occurred in immunity-related genes, supporting a polygenic basis of resistance. We experimentally validated the role of several genes in viral replication and showed that selection acting on an interferon protein has increased the protein’s antiviral effect.

UR - http://www.scopus.com/inward/record.url?scp=85061759943&partnerID=8YFLogxK

U2 - 10.1126/science.aau7285

DO - 10.1126/science.aau7285

M3 - Article

C2 - 30765607

AN - SCOPUS:85061759943

SN - 0036-8075

VL - 363

SP - 1319

EP - 1326

JO - Science

JF - Science

IS - 6433

ER -

Parallel adaptation of rabbit populations to myxoma virus

Abstract

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