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Genomic analysis of European Drosophila melanogaster populations reveals longitudinal structure, continent-wide selection, and previously unknown DNA viruses

View ORCID ProfileMartin Kapun, View ORCID ProfileMaite G. Barrón, View ORCID ProfileFabian Staubach, View ORCID ProfileDarren J. Obbard, View ORCID ProfileR. Axel W. Wiberg, View ORCID ProfileJorge Vieira, View ORCID ProfileClément Goubert, View ORCID ProfileOmar Rota-Stabelli, View ORCID ProfileMaaria Kankare, View ORCID ProfileMaría Bogaerts-Márquez, View ORCID ProfileAnnabelle Haudry, View ORCID ProfileLena Waidele, View ORCID ProfileIryna Kozeretska, View ORCID ProfileElena G. Pasyukova, View ORCID ProfileVolker Loeschcke, View ORCID ProfileMarta Pascual, View ORCID ProfileCristina P. Vieira, View ORCID ProfileSvitlana Serga, View ORCID ProfileCatherine Montchamp-Moreau, View ORCID ProfileJessica Abbott, View ORCID ProfilePatricia Gibert, View ORCID ProfileDamiano Porcelli, View ORCID ProfileNico Posnien, View ORCID ProfileAlejandro Sánchez-Gracia, View ORCID ProfileSonja Grath, View ORCID ProfileÉlio Sucena, View ORCID ProfileAlan O. Bergland, Maria Pilar Garcia Guerreiro, View ORCID ProfileBanu Sebnem Onder, View ORCID ProfileEliza Argyridou, View ORCID ProfileLain Guio, View ORCID ProfileMads Fristrup Schou, View ORCID ProfileBart Deplancke, View ORCID ProfileCristina Vieira, View ORCID ProfileMichael G. Ritchie, View ORCID ProfileBas J. Zwaan, View ORCID ProfileEran Tauber, View ORCID ProfileDorcas J. Orengo, View ORCID ProfileEva Puerma, View ORCID ProfileMontserrat Aguadé, View ORCID ProfilePaul S. Schmidt, View ORCID ProfileJohn Parsch, View ORCID ProfileAndrea J. Betancourt, View ORCID ProfileThomas Flatt, View ORCID ProfileJosefa González
doi: https://doi.org/10.1101/313759
Martin Kapun
1The European Drosophila Population Genomics Consortium (DrosEU)
2Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland
3Department of Biology, University of Fribourg, CH-1700 Fribourg, Switzerland
4Department of Evolutionary Biology and Environmental Sciences, University of Zürich, CH-8057 Zürich, Switzerland; Division of Cell and Developmental Biology, Medical University of Vienna, AT-1090 Vienna, Austria
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  • ORCID record for Martin Kapun
  • For correspondence: martin.kapun@uzh.ch thomas.flatt@unifr.ch josefa.gonzalez@ibe.upf-csic.es
Maite G. Barrón
1The European Drosophila Population Genomics Consortium (DrosEU)
5Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain
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  • ORCID record for Maite G. Barrón
Fabian Staubach
1The European Drosophila Population Genomics Consortium (DrosEU)
6Department of Evolutionary Biology and Ecology, University of Freiburg, 79104 Freiburg, German
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  • ORCID record for Fabian Staubach
Darren J. Obbard
1The European Drosophila Population Genomics Consortium (DrosEU)
7Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom
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R. Axel W. Wiberg
1The European Drosophila Population Genomics Consortium (DrosEU)
8Centre for Biological Diversity, School of Biology, University of St. Andrews, St Andrews, United Kingdom
9Department of Environmental Sciences, Zoological Institute, University of Basel, Basel, CH-4051, Switzerland
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  • ORCID record for R. Axel W. Wiberg
Jorge Vieira
1The European Drosophila Population Genomics Consortium (DrosEU)
10Instituto de Biologia Molecular e Celular (IBMC) University of Porto, Porto, Portugal
11Instituto de Investigação e Inovação em Saúde (I3S), University of Porto, Porto, Portugal
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Clément Goubert
1The European Drosophila Population Genomics Consortium (DrosEU)
12Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, University Lyon 1, Lyon, France
13Department of Molecular Biology and Genetics, 107 Biotechnology Building, Cornell University, Ithaca, New York 14853, USA
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  • ORCID record for Clément Goubert
Omar Rota-Stabelli
1The European Drosophila Population Genomics Consortium (DrosEU)
14Research and Innovation Centre, Fondazione Edmund Mach, San Michele all’ Adige, Italy
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  • ORCID record for Omar Rota-Stabelli
Maaria Kankare
1The European Drosophila Population Genomics Consortium (DrosEU)
15Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland
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María Bogaerts-Márquez
1The European Drosophila Population Genomics Consortium (DrosEU)
5Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain
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  • ORCID record for María Bogaerts-Márquez
Annabelle Haudry
1The European Drosophila Population Genomics Consortium (DrosEU)
12Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, University Lyon 1, Lyon, France
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Lena Waidele
1The European Drosophila Population Genomics Consortium (DrosEU)
6Department of Evolutionary Biology and Ecology, University of Freiburg, 79104 Freiburg, German
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  • ORCID record for Lena Waidele
Iryna Kozeretska
1The European Drosophila Population Genomics Consortium (DrosEU)
16General and Medical Genetics Department, Taras Shevchenko National University of Kyiv, Kyiv, Ukraine
17State Institution National Antarctic Center of Ministry of Education and Science of Ukraine, 16 Taras Shevchenko Blvd., 01601, Kyiv, Ukraine
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Elena G. Pasyukova
1The European Drosophila Population Genomics Consortium (DrosEU)
18Laboratory of Genome Variation, Institute of Molecular Genetics of RAS, Moscow, Russia
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  • ORCID record for Elena G. Pasyukova
Volker Loeschcke
1The European Drosophila Population Genomics Consortium (DrosEU)
19Department of Bioscience - Genetics, Ecology and Evolution, Aarhus University, Aarhus C, Denmark
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  • ORCID record for Volker Loeschcke
Marta Pascual
1The European Drosophila Population Genomics Consortium (DrosEU)
20Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
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  • ORCID record for Marta Pascual
Cristina P. Vieira
1The European Drosophila Population Genomics Consortium (DrosEU)
10Instituto de Biologia Molecular e Celular (IBMC) University of Porto, Porto, Portugal
11Instituto de Investigação e Inovação em Saúde (I3S), University of Porto, Porto, Portugal
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  • ORCID record for Cristina P. Vieira
Svitlana Serga
1The European Drosophila Population Genomics Consortium (DrosEU)
16General and Medical Genetics Department, Taras Shevchenko National University of Kyiv, Kyiv, Ukraine
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Catherine Montchamp-Moreau
1The European Drosophila Population Genomics Consortium (DrosEU)
21Laboratoire Evolution, Génomes, Comportement et Ecologie (EGCE) UMR 9191 CNRS - UMR247 IRD - Université Paris Sud - Université Paris Saclay. 91198 Gif sur Yvette Cedex, France
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Jessica Abbott
1The European Drosophila Population Genomics Consortium (DrosEU)
22Department of Biology, Section for Evolutionary Ecology, Lund, Sweden
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  • ORCID record for Jessica Abbott
Patricia Gibert
1The European Drosophila Population Genomics Consortium (DrosEU)
12Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, University Lyon 1, Lyon, France
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Damiano Porcelli
1The European Drosophila Population Genomics Consortium (DrosEU)
23Department of Animal and Plant Sciences, Sheffield, United Kingdom
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Nico Posnien
1The European Drosophila Population Genomics Consortium (DrosEU)
24Universität Göttingen, Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Göttingen, Germany
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Alejandro Sánchez-Gracia
1The European Drosophila Population Genomics Consortium (DrosEU)
20Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
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Sonja Grath
1The European Drosophila Population Genomics Consortium (DrosEU)
25Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg, Germany
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Élio Sucena
1The European Drosophila Population Genomics Consortium (DrosEU)
26Instituto Gulbenkian de Ciência, Oeiras, Portugal
27Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Lisboa, Portugal
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Alan O. Bergland
1The European Drosophila Population Genomics Consortium (DrosEU)
28Department of Biology, University of Virginia, Charlottesville, VA, USA
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Maria Pilar Garcia Guerreiro
1The European Drosophila Population Genomics Consortium (DrosEU)
29Departament de Genètica i Microbiologia, Universitat Autònoma de Barcelona, Barcelona, Spain
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Banu Sebnem Onder
1The European Drosophila Population Genomics Consortium (DrosEU)
30Department of Biology, Faculty of Science, Hacettepe University, Ankara, Turkey
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Eliza Argyridou
1The European Drosophila Population Genomics Consortium (DrosEU)
25Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg, Germany
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Lain Guio
1The European Drosophila Population Genomics Consortium (DrosEU)
5Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain
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Mads Fristrup Schou
1The European Drosophila Population Genomics Consortium (DrosEU)
19Department of Bioscience - Genetics, Ecology and Evolution, Aarhus University, Aarhus C, Denmark
22Department of Biology, Section for Evolutionary Ecology, Lund, Sweden
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Bart Deplancke
1The European Drosophila Population Genomics Consortium (DrosEU)
31Laboratory of Systems Biology and Genetics, EPFL-SV-IBI-UPDEPLA, CH-1015 Lausanne, Switzerland
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  • ORCID record for Bart Deplancke
Cristina Vieira
1The European Drosophila Population Genomics Consortium (DrosEU)
12Laboratoire de Biométrie et Biologie Evolutive, UMR CNRS 5558, University Lyon 1, Lyon, France
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Michael G. Ritchie
1The European Drosophila Population Genomics Consortium (DrosEU)
8Centre for Biological Diversity, School of Biology, University of St. Andrews, St Andrews, United Kingdom
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  • ORCID record for Michael G. Ritchie
Bas J. Zwaan
1The European Drosophila Population Genomics Consortium (DrosEU)
32Laboratory of Genetics, Department of Plant Sciences, Wageningen University, Wageningen, Netherlands
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Eran Tauber
1The European Drosophila Population Genomics Consortium (DrosEU)
33Department of Evolutionary and Environmental Biology and Institute of Evolution, University of Haifa, Haifa, Israel
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Dorcas J. Orengo
1The European Drosophila Population Genomics Consortium (DrosEU)
20Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
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Eva Puerma
1The European Drosophila Population Genomics Consortium (DrosEU)
20Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
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Montserrat Aguadé
1The European Drosophila Population Genomics Consortium (DrosEU)
20Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain
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Paul S. Schmidt
1The European Drosophila Population Genomics Consortium (DrosEU)
34Department of Biology, University of Pennsylvania, Philadelphia, USA
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John Parsch
1The European Drosophila Population Genomics Consortium (DrosEU)
25Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg, Germany
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Andrea J. Betancourt
1The European Drosophila Population Genomics Consortium (DrosEU)
35Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom
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Thomas Flatt
1The European Drosophila Population Genomics Consortium (DrosEU)
2Department of Ecology and Evolution, University of Lausanne, CH-1015 Lausanne, Switzerland
3Department of Biology, University of Fribourg, CH-1700 Fribourg, Switzerland
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  • For correspondence: martin.kapun@uzh.ch thomas.flatt@unifr.ch josefa.gonzalez@ibe.upf-csic.es
Josefa González
1The European Drosophila Population Genomics Consortium (DrosEU)
5Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain
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  • ORCID record for Josefa González
  • For correspondence: martin.kapun@uzh.ch thomas.flatt@unifr.ch josefa.gonzalez@ibe.upf-csic.es
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Abstract

Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatio-temporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster. Our analyses uncover longitudinal population structure, provide evidence for continent-wide selective sweeps, identify candidate genes for local climate adaptation, and document clines in chromosomal inversion and transposable element frequencies. We also characterise variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples.

Footnotes

  • ↵§ Members of the Drosophila Real Time Evolution (Dros-RTEC) Consortium

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Genomic analysis of European Drosophila melanogaster populations reveals longitudinal structure, continent-wide selection, and previously unknown DNA viruses
Martin Kapun, Maite G. Barrón, Fabian Staubach, Darren J. Obbard, R. Axel W. Wiberg, Jorge Vieira, Clément Goubert, Omar Rota-Stabelli, Maaria Kankare, María Bogaerts-Márquez, Annabelle Haudry, Lena Waidele, Iryna Kozeretska, Elena G. Pasyukova, Volker Loeschcke, Marta Pascual, Cristina P. Vieira, Svitlana Serga, Catherine Montchamp-Moreau, Jessica Abbott, Patricia Gibert, Damiano Porcelli, Nico Posnien, Alejandro Sánchez-Gracia, Sonja Grath, Élio Sucena, Alan O. Bergland, Maria Pilar Garcia Guerreiro, Banu Sebnem Onder, Eliza Argyridou, Lain Guio, Mads Fristrup Schou, Bart Deplancke, Cristina Vieira, Michael G. Ritchie, Bas J. Zwaan, Eran Tauber, Dorcas J. Orengo, Eva Puerma, Montserrat Aguadé, Paul S. Schmidt, John Parsch, Andrea J. Betancourt, Thomas Flatt, Josefa González
bioRxiv 313759; doi: https://doi.org/10.1101/313759
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Genomic analysis of European Drosophila melanogaster populations reveals longitudinal structure, continent-wide selection, and previously unknown DNA viruses
Martin Kapun, Maite G. Barrón, Fabian Staubach, Darren J. Obbard, R. Axel W. Wiberg, Jorge Vieira, Clément Goubert, Omar Rota-Stabelli, Maaria Kankare, María Bogaerts-Márquez, Annabelle Haudry, Lena Waidele, Iryna Kozeretska, Elena G. Pasyukova, Volker Loeschcke, Marta Pascual, Cristina P. Vieira, Svitlana Serga, Catherine Montchamp-Moreau, Jessica Abbott, Patricia Gibert, Damiano Porcelli, Nico Posnien, Alejandro Sánchez-Gracia, Sonja Grath, Élio Sucena, Alan O. Bergland, Maria Pilar Garcia Guerreiro, Banu Sebnem Onder, Eliza Argyridou, Lain Guio, Mads Fristrup Schou, Bart Deplancke, Cristina Vieira, Michael G. Ritchie, Bas J. Zwaan, Eran Tauber, Dorcas J. Orengo, Eva Puerma, Montserrat Aguadé, Paul S. Schmidt, John Parsch, Andrea J. Betancourt, Thomas Flatt, Josefa González
bioRxiv 313759; doi: https://doi.org/10.1101/313759

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