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

Science. 2019 Mar 22;363(6433):1319-1326. doi: 10.1126/science.aau7285. Epub 2019 Feb 14.

Authors

Joel M Alves^{1

2

3}, Miguel Carneiro^{4

5}, Jade Y Cheng^{6

7}, Ana Lemos de Matos⁸, Masmudur M Rahman⁸, Liisa Loog^{3

9}, Paula F Campos^{7

10}, Nathan Wales^{7

11

12}, Anders Eriksson¹³, Andrea Manica¹⁴, Tanja Strive^{15

16}, Stephen C Graham¹⁷, Sandra Afonso², Diana J Bell¹⁸, Laura Belmont⁸, Jonathan P Day¹⁹, Susan J Fuller²⁰, Stéphane Marchandeau²¹, William J Palmer²², Guillaume Queney²³, Alison K Surridge¹⁸, Filipe G Vieira⁷, Grant McFadden⁸, Rasmus Nielsen^{6

7}, M Thomas P Gilbert^{7

24}, Pedro J Esteves^{2

25}, Nuno Ferrand^{2

5

26}, Francis M Jiggins¹

Affiliations

¹ Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UK. joel.alves@arch.ox.ac.uk miguel.carneiro@cibio.up.pt fmj1001@cam.ac.uk.
² CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, 4485-661 Vairão, Portugal.
³ Palaeogenomics and Bio-Archaeology Research Network Research Laboratory for Archaeology and History of Art, University of Oxford, Dyson Perrins Building, South Parks Road, Oxford OX1 3QY, UK.
⁴ CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Laboratório Associado, Universidade do Porto, 4485-661 Vairão, Portugal. joel.alves@arch.ox.ac.uk miguel.carneiro@cibio.up.pt fmj1001@cam.ac.uk.
⁵ Departamento de Biologia, Faculdade de Ciências da Universidade do Porto, 4169-007 Porto, Portugal.
⁶ Departments of Integrative Biology and Statistics, University of California, Berkeley, Berkeley, CA 94720, USA.
⁷ Centre for GeoGenetics, Natural History Museum of Denmark, University of Copenhagen, Copenhagen 1350, Denmark.
⁸ The Biodesign Institute, Center for Immunotherapy, Vaccines, and Virotherapy, Arizona State University, Tempe, AZ 85287-5401, USA.
⁹ Manchester Institute of Biotechnology, School of Earth and Environmental Sciences, University of Manchester, Manchester M1 7DN, UK.
¹⁰ CIIMAR, Interdisciplinary Centre of Marine and Environmental Research, University of Porto, Avenida General Norton de Matos, S/N, 4450-208 Matosinhos, Portugal.
¹¹ Department of Plant and Microbial Biology, University of California, 111 Koshland Hall, Berkeley, CA 94720, USA.
¹² Department of Archaeology, University of York, King's Manor, York YO1 7EP, UK.
¹³ Department of Medical and Molecular Genetics, King's College London, London SE1 9RT, UK.
¹⁴ Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK.
¹⁵ Health and Biosecurity, Commonwealth Scientific and Industrial Research Organisation, Canberra, ACT 2601, Australia.
¹⁶ Centre for Invasive Species Solutions, University of Canberra, Bruce, ACT 2601, Australia.
¹⁷ Department of Pathology, University of Cambridge, Cambridge CB2 1QP, UK.
¹⁸ Centre for Ecology, Evolution and Conservation, School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK.
¹⁹ Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UK.
²⁰ School of Earth, Environmental and Biological Sciences, Science and Engineering Faculty, Queensland University of Technology, Brisbane, Australia.
²¹ Office National de la Chasse et de la Faune Sauvage, Nantes, France.
²² The Genome Center and Department of Plant Sciences, University of California, Davis, CA 95616, USA.
²³ ANTAGENE, Wildlife Genetics Laboratory, La Tour de Salvagny (Lyon), France.
²⁴ Norwegian University of Science and Technology, University Museum, 7491 Trondheim, Norway.
²⁵ Instituto de Investigação e Formação Avançada em Ciências e Tecnologias da Saúde (CESPU), Gandra, Portugal.
²⁶ Department of Zoology, Faculty of Sciences, University of Johannesburg, Auckland Park 2006, South Africa.

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.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Adaptation, Biological / genetics*
Alleles
Animals
Australia
Evolution, Molecular
France
Gene Frequency
Genetic Variation
Immunity, Innate / genetics*
Interferon alpha-2 / genetics
Interferon alpha-2 / immunology
Myxoma virus / immunology*
Myxomatosis, Infectious / genetics
Myxomatosis, Infectious / immunology*
Polymorphism, Single Nucleotide
Population
Rabbits / genetics*
Rabbits / immunology
Rabbits / virology*
United Kingdom

Substances

Interferon alpha-2

Abstract

Publication types

MeSH terms

Substances

Grants and funding