Footprints of Worldwide Adaptation in Structured Populations of Drosophila melanogaster Through the Expanded DEST 2.0 Genomic Resource

Joaquin C. B. Nunez; Marta Coronado-Zamora; Mathieu Gautier; Martin Kapun; Sonja Steindl; Lino Ometto; Katja Hoedjes; Julia Beets; R. Axel W. Wiberg; Giovanni R. Mazzeo; David J. Bass; Denys Radionov; Iryna Kozeretska; Mariia Zinchenko; Oleksandra Protsenko; Svitlana V. Serga; Cristina Amor-Jimenez; Sònia Casillas; Alejandro Sánchez-Gracia; Aleksandra Patenkovic; Amanda Glaser-Schmitt; Antonio Barbadilla; Antonio J. Buendia-Ruíz; Astra Clelia Bertelli; Balázs Kiss; Banu Sebnem Önder; Bélen Roldán Matrín; Bregje Wertheim; Candice Deschamps; Carlos E. Arboleda-Bustos; Carlos Tinedo; Christian Feller; Christian Schlötterer; Clancy Lawler; Claudia Fricke; Cristina P. Vieira; Cristina Vieira; Darren Juana Obbard; Dorcas Orengo; Doris Vela; Eduardo Amat; Elgion Loreto; Envel Kerdaffrec; Esra Durmaz Mitchell; Eva Puerma; Fabian Staubach; M. Florencia Camus; Hervé Colinet; Jan Hrcek; Jesper Givskov Sørensen; Jessica Abbott; Joan Torro; John Parsch; Jorge Vieira; Jose Luis Olmo; Khalid Khfif; Krzysztof Wojciechowski; Lilian Madi-Ravazzi; Maaria Kankare; Mads F. Schou; Emmanuel D. Ladoukakis; M. Josefa Gomez-Julian; M. Luisa Espinosa-Jimenez; Maria Pilar Garcia-Guerreiro; Maria-Eleni Parakatselaki; Marija Savic Veselinovic; Marija Tanaskovic; Marina Stamenkovic-Radak; Margot Paris; Marta Pascual; Michael G. Ritchie; Michael Rera; Mihailo Jelić; Mina Hojat Ansari; Mina Rakic; Miriam Merenciano; Natalia Hernandes; Nazar Gora; Nicolas Rode; Omar Rota-Stabelli; Paloma Sepulveda; Patricia Gibert; Pau Carazo; Pinar Kohlmeier; Priscilla A. Erickson; Renaud Vitalis; Jorge Roberto Torres; Sara Guirao-Rico; Sebastian E. Ramos-Onsins; Silvana Castillo; Tânia F. Paulo; Venera Tyukmaeva; Zahara Alonso; Vladimir E. Alatortsev; Elena Pasyukova; Dmitry V. Mukha; Dmitri A. Petrov; Paul Schmidt; Thomas Flatt; Alan O. Bergland; Josefa Gonzalez

doi:10.1101/2024.11.10.622744

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Footprints of Worldwide Adaptation in Structured Populations of Drosophila melanogaster Through the Expanded DEST 2.0 Genomic Resource

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Footprints of Worldwide Adaptation in Structured Populations of Drosophila melanogaster Through the Expanded DEST 2.0 Genomic Resource

Joaquin C. B. Nunez, Marta Coronado-Zamora, Mathieu Gautier, Martin Kapun, Sonja Steindl, Lino Ometto, Katja Hoedjes, Julia Beets, R. Axel W. Wiberg, Giovanni R. Mazzeo, …

Molecular Biology and Evolution, Vol.42(8)

18/08/2025

DOI: https://doi.org/10.1101/2024.11.10.622744

PMID: 40824865

Résumé

Jeu de données

population structure

seasonal selection

local adaptation

ecological genomics

Drosophila melanogaster

vinegar fly

data set

distribution over space and time

spatiotemporal distribution

gene library

gene bank

genetic structure of populations

population genetic structure

size of the population

pesticide resistance

resistance to pesticides

model system

environmental adaptation

ecological adaptation

genetic footprint

DNA barcoding

DNA fingerprint

genetic resources conservation

genetic variation

genetic variability

population genetics

Drosophila

evolution of populations

population evolution

Large scale genomic resources can place genetic variation into an ecologically informed context. To advance our understanding of the population genetics of the fruit fly Drosophila melanogaster , we present an expanded release of the community-generated population genomics resource Drosophila Evolution over Space and Time (DEST 2.0; https://dest.bio). This release includes 530 high-quality pooled libraries from flies collected across six continents over more than a decade (2009-2021), most at multiple time points per year; 211 of these libraries are sequenced and shared here for the first time. We used this enhanced resource to elucidate several aspects of the species' demographic history and identify novel signs of adaptation across spatial and temporal dimensions. We showed that patterns of secondary contact, originally characterized in North America, are replicated in South America and Australia. We also found that the spatial genetic structure of populations is stable over time, but that drift due to seasonal contractions of population size causes populations to diverge over time. We identified signals of adaptation that vary between continents in genomic regions associated with xenobiotic resistance, consistent with independent adaptation to common pesticides. Moreover, by analyzing samples collected during spring and fall across Europe, we provide new evidence for seasonal adaptation related to loci associated with pathogen response. Furthermore, we have also released an updated version of the DEST genome browser. This is a useful tool for studying spatio-temporal patterns of genetic variation in this classic model system.

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Titre: Footprints of Worldwide Adaptation in Structured Populations of Drosophila melanogaster Through the Expanded DEST 2.0 Genomic Resource
Créateurs - sans rôle: Joaquin C. B. Nunez - University of Virginia
Marta Coronado-Zamora - Institut de Biologia Evolutiva
Mathieu Gautier - Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement
Martin Kapun - Natural History Museum Vienna
Sonja Steindl - Natural History Museum Vienna
Lino Ometto - University of Pavia
Katja Hoedjes - Vrije Universiteit Amsterdam
Julia Beets - Vrije Universiteit Amsterdam
R. Axel W. Wiberg - Stockholm University
Giovanni R. Mazzeo - University of Virginia
David J. Bass - University of Virginia
Denys Radionov - Odessa National I.I.Mechnikov University
Iryna Kozeretska - State Institution National Antarctic Scientific Center
Mariia Zinchenko - Lesya Ukrainka Volyn National University
Oleksandra Protsenko - Taras Shevchenko National University of Kyiv
Svitlana V. Serga - Agropolis International
Cristina Amor-Jimenez - Universitat Autònoma de Barcelona
Sònia Casillas - Universitat Autònoma de Barcelona
Alejandro Sánchez-Gracia - Universitat de Barcelona
Aleksandra Patenkovic - Institute for Biological Research “Siniša Stanković”
Amanda Glaser-Schmitt - Ludwig-Maximilians-Universität München
Antonio Barbadilla - Universitat Autònoma de Barcelona
Antonio J. Buendia-Ruíz - Hospital General de Tomelloso
Astra Clelia Bertelli - Natural History Museum Vienna
Balázs Kiss - Hungarian Research Network
Banu Sebnem Önder - Hacettepe University
Bélen Roldán Matrín - Instituto de Enseñanza Secundaria Alonso de Ercilla
Bregje Wertheim - University of Groningen
Candice Deschamps - Centre de Biologie et de Gestion des Populations
Carlos E. Arboleda-Bustos - Universidad Nacional de Colombia
Carlos Tinedo - Universitat de Barcelona
Christian Feller - Zú
Christian Schlötterer - University of Veterinary Medicine Vienna
Clancy Lawler - The University of Melbourne
Claudia Fricke - Martin Luther University Halle-Wittenberg
Cristina P. Vieira - Centre National de la Recherche Scientifique
Cristina Vieira - Centre National de la Recherche Scientifique
Darren Juana Obbard - University of Edinburgh
Dorcas Orengo - Universitat de Barcelona
Doris Vela - Pontificia Universidad Católica del Ecuador
Eduardo Amat - Antioquia Institute of Technology
Elgion Loreto - Universidade Federal de Santa Maria
Envel Kerdaffrec - University of Fribourg
Esra Durmaz Mitchell - University of Fribourg
Eva Puerma - Vall d'Hebron Institute of Oncology
Fabian Staubach - University of Freiburg
M. Florencia Camus - University College London
Hervé Colinet - Ecosystèmes, Biodiversité, Evolution
Jan Hrcek - Czech Academy of Sciences, Biology Centre
Jesper Givskov Sørensen - Aarhus University
Jessica Abbott - Lund University
Joan Torro - Instituto de Enseñanza Secundaria Benjamín Jarnés
John Parsch - Ludwig-Maximilians-Universität München
Jorge Vieira - i3S - Instituto de Investigação e Inovação em Saúde, Universidade do Porto
Jose Luis Olmo - Instituto de Enseñanza Secundaria Azuer
Khalid Khfif - École Nationale de Commerce et de Gestion de Tanger
Krzysztof Wojciechowski - Regional Landscape Parks of Lublin
Lilian Madi-Ravazzi - Universidade Estadual Paulista (Unesp)
Maaria Kankare - University of Jyväskylä
Mads F. Schou - Aarhus University
Emmanuel D. Ladoukakis - Crete University Press
M. Josefa Gomez-Julian - Hospital General de Tomelloso
M. Luisa Espinosa-Jimenez - Hospital General de Tomelloso
Maria Pilar Garcia-Guerreiro - Universitat Autònoma de Barcelona
Maria-Eleni Parakatselaki - Crete University Press
Marija Savic Veselinovic - University of Belgrade
Marija Tanaskovic - Institute for Biological Research Sinisa Stankovic [Belgrade]
Marina Stamenkovic-Radak - University of Belgrade
Margot Paris - University of Fribourg
Marta Pascual - Universitat de Barcelona
Michael G. Ritchie - University of St Andrews
Michael Rera - Institut Jacques Monod
Mihailo Jelić - University of Belgrade
Mina Hojat Ansari - University of Freiburg
Mina Rakic - University of Belgrade
Miriam Merenciano - Institut de Biologia Evolutiva
Natalia Hernandes - The University of Melbourne
Nazar Gora - Lawrence Berkeley National Laboratory
Nicolas Rode - Agropolis International
Omar Rota-Stabelli - University of Trento
Paloma Sepulveda - Instituto de Enseñanza Secundaria Carpetania
Patricia Gibert - Laboratoire de Biométrie et Biologie Evolutive
Pau Carazo - Institute for Biodiversity
Pinar Kohlmeier - Groningen Institute for Evolutionary Life Sciences [Groningen]
Priscilla A. Erickson - University of Virginia
Renaud Vitalis - Centre de Biologie et de Gestion des Populations
Jorge Roberto Torres - Ciencia
Sara Guirao-Rico - Universitat de Barcelona
Sebastian E. Ramos-Onsins - Center for Research in Agricultural Genomics
Silvana Castillo - Instituto de Enseñanza Secundaria Jose de Mora
Tânia F. Paulo - Instituto Gulbenkian de Ciência
Venera Tyukmaeva - University of Liverpool
Zahara Alonso - Centro de Educación Infantil y Primaria Ramón y Cajal
Vladimir E. Alatortsev - Institute of Molecular Genetics
Elena Pasyukova - Institute of Molecular Genetics
Dmitry V. Mukha - Vavilov Institute of General Genetics
Dmitri A. Petrov - Stanford University
Paul Schmidt - University of Pennsylvania
Thomas Flatt - University of Fribourg
Alan O. Bergland - University of Virginia
Josefa Gonzalez - Institut de Biologia Evolutiva
Détails de publication: Molecular Biology and Evolution, Vol.42(8)
Note de subvention: J.C.B.N. was supported by start-up funds from the University of Vermont. M.Kap. and S.S. were supported by the Horizon Europe project FAIRiCUBE (grant #101059238). D.A.P. was supported by the NIH 2R35GM11816506 (MIRA grant). T.F. was supported by the Swiss National Science Foundation (SNSF) grants 31003A-182262, 310030_219283, and FZEB-0-214654. A.O.B. was supported by the National Institutes of Health R35 GM119686 and National Science Foundation CAREER #2145688 grants. J.G. was supported by grant PID2020-115874GB-I00 funded by MICIU/AEI /10.13039/501100011033, grant PID2023-148838NB-I00 funded by MICIU/AEI/10.13039/501100011033 and FEDER/EU, and grant 2021 SGR 00417 funded by the Departament de Recerca i Universitats, Generalitat de Catalunya. A.S.-G. was supported by the Ministerio de Ciencia e Innovación of Spain (MCIN/AEI/10.13039/501100011033; grant PID2020-113168GB-I00) and Comissió Interdepartamental de Recerca I Innovació Tecnològica of Catalonia, Spain (2021SGR00279). A.P. and M.T. were supported by the Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA), grant no. 451-03-66/2024-03/200007. A.B., M.P.G.G., and S.Casi. were supported by Ministerio de Ciencia e Innovación (PID2021-127107NB-I00) and AGAUR Generalitat de Catalunya (SGR 00526). C.S. was supported by the Austrian Science Funds, FWF, 10.55776/P32935, 10.55776/P33734. C.Fr. was supported by the German Research Foundation (DFG, grant # FR2973/11-1). D.O. was supported by the UK Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/T007516/1. D.V. was supported by project QINV0196-IINV529010100 from the Pontificia Universidad Católica del Ecuador; Abbott was supported by VR-2015-04680 and VR-2020-05412. J.P. was supported by the Deutsche Forschungsgemeinschaft (DFG) projects 255619725 and 503272152. M.Kan. was supported by the Academy of Finland project 322980. M.S.V., M.J., and M.Ra. were supported by the Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA), grant no. 451-03-65/2024-03/ 200178. M.S.-R. was supported by the Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA) grant no. 451-03-47/2023-01/200178. M.G.R. was supported by Natural Environment Research Council (NERC), UK award NE/V001566/1. M.Re. was supported by the Bettencourt Schueller Foundation long-term partnership; this work was also partly supported by a CRI Core Research Fellowship. P.A.E. was supported by award #61-1673 from the Jane Coffin Childs Memorial Fund for Medical Research (www.jccfund.org). S.E.R.-O. was supported by PID2020-119255GB-I00 (MICINN, Spain), by the CERCA Programme/Generalitat de Catalunya and acknowledges financial support from the Spanish Ministry of Economy and Competitiveness, through the Severo Ochoa Programme for Centres of Excellence in R&D 2016–2019 and 2020–2023 (SEV-2015-0533, CEX2019-000917) and the European Regional Development Fund (ERDF). N.H. and C.L. were supported by Australian Research Council DP190102512. E.K. was supported by the European Molecular Biology Organization (EMBO) long-term fellowship ALT 248-02018. H.C. was supported by the French National Research Agency (ANR) project Drothermal (ANR-20-CE02-011). DrosEU was funded by a Special Topic Networks (STN) grant from the European Society for Evolutionary Biology (ESEB). J.C.B.N. acknowledges the Henderson–Harris fellowship program at the University of Vermont, also the Vermont Advanced Computing Center (URL: https://www.uvm.edu/vacc) for providing computational resources that contributed to this publication. A.O.B. acknowledges Research Computing at the University of Virginia (URL: https://rc.virginia.edu) for providing computational resources and technical support that have contributed to the results reported within this publication. A.O.B. also acknowledges Kathryn Linehan from UVA's RC for support in updating the SNP calling pipeline that is part of DEST2.0. M.C.-Z. and J.G. acknowledge the Galician Supercomputing Center (CESGA), which provided access to its supercomputing infrastructure, the supercomputer FinisTerrae III and its permanent data storage system, funded by the Spanish Ministry of Science and Innovation, the Galician Government, and the European Regional Development Fund (ERDF). M.G. acknowledges the genotoul bioinformatics platform Toulouse Occitanie (Bioinfo Genotoul, https://doi.org/10.15454/1.5572369328961167E12) for providing computing resources.
Identifiants: 99161482609311
Unité académique: Université de Montpellier
Langue: English
Type de ressource: Journal article
Champs locaux: hal-04779897