Genomic Analysis of European Drosophila melanogaster Populations Reveals Longitudinal Structure, Continent-Wide Selection, and Previously Unknown DNA Viruses

Author:

Kapun Martin12345ORCID,Barrón Maite G36,Staubach Fabian37,Obbard Darren J38,Wiberg R Axel W3910ORCID,Vieira Jorge31112,Goubert Clément31314,Rota-Stabelli Omar315,Kankare Maaria316ORCID,Bogaerts-Márquez María36,Haudry Annabelle313,Waidele Lena37,Kozeretska Iryna31718,Pasyukova Elena G319,Loeschcke Volker320,Pascual Marta32122,Vieira Cristina P31112,Serga Svitlana317,Montchamp-Moreau Catherine323,Abbott Jessica324,Gibert Patricia313,Porcelli Damiano325,Posnien Nico326ORCID,Sánchez-Gracia Alejandro32122,Grath Sonja327,Sucena Élio32829,Bergland Alan O330,Guerreiro Maria Pilar Garcia331,Onder Banu Sebnem332,Argyridou Eliza327,Guio Lain36,Schou Mads Fristrup32024,Deplancke Bart333,Vieira Cristina313,Ritchie Michael G39ORCID,Zwaan Bas J334ORCID,Tauber Eran33536,Orengo Dorcas J32122,Puerma Eva32122,Aguadé Montserrat32122,Schmidt Paul337ORCID,Parsch John327,Betancourt Andrea J338,Flatt Thomas345ORCID,González Josefa36

Affiliation:

1. Department of Evolutionary Biology and Environmental Sciences, University of Zürich, Zürich, Switzerland

2. Division of Cell and Developmental Biology, Medical University of Vienna, Vienna, Austria

3. The European Drosophila Population Genomics Consortium (DrosEU)

4. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

5. Department of Biology, University of Fribourg, Fribourg, Switzerland

6. Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain

7. Department of Evolutionary Biology and Ecology, University of Freiburg, Freiburg, Germany

8. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United Kingdom

9. Centre for Biological Diversity, School of Biology, University of St. Andrews, St Andrews, Scotland

10. Department of Environmental Sciences, Zoological Institute, University of Basel, Basel, Switzerland

11. Instituto de Biologia Molecular e Celular (IBMC), University of Porto, Porto, Portugal

12. Instituto de Investigação e Inovação em Saúde (I3S), University of Porto, Porto, Portugal

13. Laboratoire de Biométrie et Biologie Evolutive UMR 5558, CNRS, Université Lyon 1, Université de Lyon, Villeurbanne, France

14. Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY

15. Research and Innovation Centre, Fondazione Edmund Mach, San Michele all’ Adige, Italy

16. Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland

17. General and Medical Genetics Department, Taras Shevchenko National University of Kyiv, Kyiv, Ukraine

18. State Institution National Antarctic Scientific Center of Ministry of Education and Science of Ukraine, Kyiv, Ukraine

19. Laboratory of Genome Variation, Institute of Molecular Genetics of RAS, Moscow, Russia

20. Department of Bioscience—Genetics, Ecology and Evolution, Aarhus University, Aarhus C, Denmark

21. Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia, Universitat de Barcelona, Barcelona, Spain

22. Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain

23. Université Paris-Saclay, CNRS, IRD, UMR Évolution, Génomes, Comportement et Écologie, 91198, Gif-sur-Yvette, France

24. Section for Evolutionary Ecology, Department of Biology, Lund University, Lund, Sweden

25. Department of Animal and Plant Sciences, Sheffield, United Kingdom

26. Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie, Universität Göttingen, Göttingen, Germany

27. Division of Evolutionary Biology, Faculty of Biology, Ludwig-Maximilians-Universität München, Planegg, Germany

28. Instituto Gulbenkian de Ciência, Oeiras, Portugal

29. Departamento de Biologia Animal, Faculdade de Ciências da Universidade de Lisboa, Lisboa, Portugal

30. Department of Biology, University of Virginia, Charlottesville, VA

31. Departament de Genètica i Microbiologia, Universitat Autònoma de Barcelona, Barcelona, Spain

32. Department of Biology, Faculty of Science, Hacettepe University, Ankara, Turkey

33. Institute of Bio-engineering, School of Life Sciences, EPFL, Lausanne, Switzerland

34. Laboratory of Genetics, Department of Plant Sciences, Wageningen University, Wageningen, Netherlands

35. Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel

36. Institute of Evolution, University of Haifa, Haifa, Israel

37. Department of Biology, University of Pennsylvania, Philadelphia, PA

38. Department of Evolution, Ecology, and Behaviour, University of Liverpool, Liverpool, United Kingdom

Abstract

AbstractGenetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatiotemporal 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 characterize variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples.

Funder

University of Freiburg Research Innovation Fund 2014

Deutsche Forschungsgemeinschaft

DFG

Academy of Finland

Russian Foundation of Basic Research

Danish Natural Science Research Council

Ministerio de Economia y Competitividad

Centre National de la Recherche Scientifique

Vetenskapsrådet

Emmy Noether Programme of the DFG

National Institute of Health

Scientific and Technological Research Council of Turkey

Agence Nationale de la Recherche Exhyb

Network of Excellence LifeSpan

IDEAL

Israel Science Foundation

Austrian Science Fund

Biotechnology and Biological Sciences Research Council

BBSRC

Swiss National Science Foundation

SNSF

European Commission

Secretaria d’Universitats i Recerca

Ministerio de Economia y Competitividad/FEDER

Ministerio de Ciencia e Innovación/AEI/FEDER

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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