Continent-wide differentiation of fitness traits and patterns of climate adaptation among European populations of Drosophila melanogaster

Esra Durmaz Mitchell; Envel Kerdaffrec; Ewan Harney; Tânia F. Paulo; Marija Savic Veselinovic; Marija Tanaskovic; Venera Tyukmaeva; Teresa Abaurrea Fernandez de Arcaya; Cansu Aksoy; Eliza Argyridou; Tiphaine P. M. Bailly; Dogus Can; Ezgi Cobanoglu; Nicola Cook; Seda Coşkun; Slobodan Davidovic; Ekin Demir; Tânia Dias; Somayeh Rasouli-Dogaheh; Pedro Duque; Katarina Eric; Pavle Eric; Priscilla Erickson; Filip Filipovski; Bettina Fishman; Amanda Glaser-Schmitt; August Goldfischer; Llewellyn Green; Sonia Janillon; Mihailo Jelic; Hristina Kostic; Lucas E. Kreiman; Natacha Kremer; Manolis Lyrakis; Oleksandr M. Maistrenko; Sapho-Lou Marti; Megan Mc Gunnigle; Miriam Merenciano; Mário S. Mira; Vincent Montbel; Laurence Mouton; Dmitry V. Mukha; Siddharth Murali; Aleksandra Patenkovic; Oleksandra Protsenko; Florencia A. Putero; Micael Reis; Natalia V. Roshina; Olga Y. Rybina; Mads F. Schou; Thibault Schowing; Senel Selin Senkal; Svitlana Serga; Virginie Trieu; Alexander V. Symonenko; Mikhail V. Trostnikov; Evgenia A. Tsybul'Ko; Joost van den Heuvel; David van Waarde; Ekaterina R. Veselkina; Cristina P. Vieira; Xiaocui Wang; Jelle Zandveld; Jessica Abbott; Jean-Christophe Billeter; Hervé Colinet; Mehregan Ebrahimi; Patricia Gibert; Jan Hrcek; Maaria Kankare; Iryna Kozeretska; Volker Loeschcke; Julián Mensch; Banu Sebnem Onder; John Parsch; Elena G. Pasyukova; Marina Stamenkovic-Radak; Eran Tauber; Cristina Vieira; Christian Wegener; Katja M. Hoedjes; Bas J. Zwaan; Andrea J. Betancourt; Claudia Fricke; Sonja Grath; Nico Posnien; Jorge Vieira; Martin Kapun; Christian Schlötterer; Paul Schmidt; Élio Sucena; Josefa González; Alan Bergland; Michael Ritchie; Thomas Flatt

doi:10.1093/evlett/qraf014

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Continent-wide differentiation of fitness traits and patterns of climate adaptation among European populations of Drosophila melanogaster

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Continent-wide differentiation of fitness traits and patterns of climate adaptation among European populations of Drosophila melanogaster

Esra Durmaz Mitchell, Envel Kerdaffrec, Ewan Harney, Tânia F. Paulo, Marija Savic Veselinovic, Marija Tanaskovic, Venera Tyukmaeva, Teresa Abaurrea Fernandez de Arcaya, Cansu Aksoy, Eliza Argyridou, …

Evolution Letters, Vol.9(4)

08/2025

DOI: https://doi.org/10.1093/evlett/qraf014

PMID: 40980703

Résumé

phenotypic variation

Europe

D. melanogaster

adaptation

population differentiation

fitness traits

A particularly well-studied evolutionary model is the vinegar fly Drosophila melanogaster, a cosmopolitan insect of ancestral southern-central African origin. Recent work suggests that it expanded out of Africa ∼9,000 years ago, and spread from the Middle East into Europe ∼1,800 years ago. During its global expansion, this human commensal adapted to novel climate zones and habitats. Despite much work on phenotypic differentiation and adaptation on several continents (especially North America and Australia), typically in the context of latitudinal clines, little is known about phenotypic divergence among European populations. Here, we sought to provide a continent-wide study of phenotypic differentiation among European populations of D. melanogaster. In a consortium-wide phenomics effort, we assayed 16 fitness-related traits on a panel of 173 isofemale lines from 9 European populations, with the majority of traits measured by several groups using semi-standardized protocols. For most fitness-related traits, we found significant differentiation among populations on a continental scale. Despite inevitable differences in assay conditions among labs, the reproducibility and hence robustness of our measurements were overall remarkably good. Several fitness components (e.g., viability, development time) exhibited significant latitudinal or longitudinal clines, and populations differed markedly in multivariate trait structure. Notably, populations experiencing higher humidity/rainfall and lower maximum temperature showed higher viability, fertility, starvation resistance, and lifespan at the expense of lower heat-shock survival, suggesting a pattern of local adaptation. Our results indicate that derived populations of this tropical fly have been shaped by pervasive spatially varying multivariate selection and adaptation to different climates on the European continent.

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Titre: Continent-wide differentiation of fitness traits and patterns of climate adaptation among European populations of Drosophila melanogaster
Créateurs - sans rôle: Esra Durmaz Mitchell - University of Fribourg
Envel Kerdaffrec - University of Fribourg
Ewan Harney - Institut de Biologia Evolutiva
Tânia F. Paulo - Instituto Gulbenkian de Ciência
Marija Savic Veselinovic - University of Belgrade
Marija Tanaskovic - Institute for Biological Research “Siniša Stanković”
Venera Tyukmaeva - University of Liverpool
Teresa Abaurrea Fernandez de Arcaya - University of St Andrews
Cansu Aksoy - Hacettepe University
Eliza Argyridou - Ludwig-Maximilians-Universität München
Tiphaine P. M. Bailly - University of Groningen
Dogus Can - Hacettepe University
Ezgi Cobanoglu - Hacettepe University
Nicola Cook - University of St Andrews
Seda Coşkun - Hacettepe University
Slobodan Davidovic - Institute for Biological Research “Siniša Stanković”
Ekin Demir - Hacettepe University
Tânia Dias - Instituto de Biologia Molecular e Celular
Somayeh Rasouli-Dogaheh - Czech Academy of Sciences
Pedro Duque - Instituto de Biologia Molecular e Celular
Katarina Eric - Institute for Biological Research “Siniša Stanković”
Pavle Eric - Institute for Biological Research “Siniša Stanković”
Priscilla Erickson - University of Richmond
Filip Filipovski - University of Belgrade
Bettina Fishman - University of Haifa
Amanda Glaser-Schmitt - Ludwig-Maximilians-Universität München
August Goldfischer - University of Pennsylvania
Llewellyn Green - Institut de Biologia Evolutiva
Sonia Janillon - Centre National de la Recherche Scientifique
Mihailo Jelic - University of Belgrade
Hristina Kostic - University of Lausanne
Lucas E. Kreiman - Consejo Nacional de Investigaciones Científicas y Técnicas
Natacha Kremer - Centre National de la Recherche Scientifique
Manolis Lyrakis - University of Veterinary Medicine
Oleksandr M. Maistrenko - Royal Netherlands Institute for Sea Research
Sapho-Lou Marti - Ecosystèmes, Biodiversité, Evolution
Megan Mc Gunnigle - University of St Andrews
Miriam Merenciano - Institut de Biologia Evolutiva
Mário S. Mira - University of Groningen
Vincent Montbel - Czech Academy of Sciences
Laurence Mouton - Centre National de la Recherche Scientifique
Dmitry V. Mukha - Vavilov Institute of General Genetics
Siddharth Murali - University of Göttingen
Aleksandra Patenkovic - Institute for Biological Research “Siniša Stanković”
Oleksandra Protsenko - Ministry of Education and Science
Florencia A. Putero - Consejo Nacional de Investigaciones Científicas y Técnicas
Micael Reis - Centre National de la Recherche Scientifique
Natalia V. Roshina - Institute of Molecular Genetics
Olga Y. Rybina - Institute of Molecular Genetics
Mads F. Schou - Aarhus University
Thibault Schowing - University of Fribourg
Senel Selin Senkal - Hacettepe University
Svitlana Serga - Centre de Coopération Internationale en Recherche Agronomique pour le Développement
Virginie Trieu - University of Fribourg
Alexander V. Symonenko - Institute of Molecular Genetics
Mikhail V. Trostnikov - Institute of Molecular Genetics
Evgenia A. Tsybul'Ko - Institute of Molecular Genetics
Joost van den Heuvel - Wageningen University and Research [Wageningen]
David van Waarde - Wageningen University and Research [Wageningen]
Ekaterina R. Veselkina - Institute of Molecular Genetics
Cristina P. Vieira - Instituto de Biologia Molecular e Celular
Xiaocui Wang - University of Groningen
Jelle Zandveld - Utrecht University
Jessica Abbott - Lund University
Jean-Christophe Billeter - Groningen Institute for Evolutionary Life Sciences [Groningen]
Hervé Colinet - Centre National de la Recherche Scientifique
Mehregan Ebrahimi - Flinders University
Patricia Gibert - Laboratoire de Biométrie et Biologie Evolutive
Jan Hrcek - Czech Academy of Sciences
Maaria Kankare - University of Jyväskylä
Iryna Kozeretska - Ministry of Education and Science
Volker Loeschcke - Aarhus University
Julián Mensch - Consejo Nacional de Investigaciones Científicas y Técnicas
Banu Sebnem Onder - Hacettepe University
John Parsch - Ludwig-Maximilians-Universität München
Elena G. Pasyukova - Institute of Molecular Genetics
Marina Stamenkovic-Radak - University of Belgrade
Eran Tauber - University of Haifa
Cristina Vieira - Instituto de Biologia Molecular e Celular
Christian Wegener - University of Würzburg
Katja M. Hoedjes - University of Lausanne
Bas J. Zwaan - Wageningen University and Research [Wageningen]
Andrea J. Betancourt - University of Liverpool
Claudia Fricke - Martin Luther University Halle-Wittenberg
Sonja Grath - Ludwig-Maximilians-Universität München
Nico Posnien - University of Göttingen
Jorge Vieira - Instituto de Biologia Molecular e Celular
Martin Kapun - Medical University of Vienna
Christian Schlötterer - Institut für Populationsgenetik [Vienna]
Paul Schmidt - University of Pennsylvania
Élio Sucena - Instituto Gulbenkian de Ciência
Josefa González - Institut Botànic de Barcelona
Alan Bergland - University of Virginia
Michael Ritchie - University of St Andrews
Thomas Flatt - University of Fribourg
Détails de publication: Evolution Letters, Vol.9(4)
Note de subvention: This research was supported by a Special Topics Network (STN) grant from the European Society of Evolutionary Biology (ESEB) to the DrosEU consortium as well as by individual grants and fellowships (grantees in alphabetical order): J.A.: Swedish Research Council (VR) grants 2015-04680 and 2020-05412; A.J.B.: European Research Council (ERC CoG TE_INVASION); S.D.: Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA) grant 451-03-66/2024-03/200007; K.E.: Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA) grant 451-03-66/2024-03/200007; P.E.: Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA) grant 451-03-66/2024-03/200007; P.E.: Jane Coffin Childs Memorial Fund for Medical Research 61-1673: T.F.: Swiss National Science Foundation (SNSF) grants 31003A-182262, 310030_219283, FZEB-0-214654; C.F.: Deutsche Forschungsgemeinschaft (DFG) grants 2973/5-1 and 2973/11; J.G.: Ministerio de Ciencia, Innovación y Universidades/Agencia Estatal de Investigación (MICIU/AEI/10.13039/501100011033/) grant PID2020-115874GB-I00; Ministerio de Ciencia, Innovación y Universidades/Agencia Estatal de Investigación (MICIU/AEI/10.13039/501100011033 and FEDER, UE) grant PID2023-148838NB-I00; Departament de Recerca i Universitats Generalitat de Catalunya grant 2021 SGR 00417; S.G.: Deutsche Forschungsgemeinschaft (DFG) grants 271330745 and 514085304; K.M.H.: Marie Skłodowska-Curie Individual Fellowship (H2020-MSCA-IF-2015) 701949; J.H.: Czech Ministry of Education, grant; European Research Council (ERC CZ LL2001); M.J.: Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA) grant 451-03-65/2024-03/200178; M.K.: Academy of Finland grant 322980; E.K.: European Molecular Biology Organization (EMBO) ALTF 248-2018; M.S.M.: ALW Open Programme grant 101185; J.P.: Deutsche Forschungsgemeinschaft (DFG) grants 255619725 (GR 4495/2-2) and 503272152 (GR 4495/4-1); E.G.P.: Russian state budget, assignment NRC “KI”; A.P.: Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA) grant 451-03-66/2024-03/200007; N.P.: Deutsche Forschungsgemeinschaft (DFG) grants PO 1648/7-1, PO 1648/3-1, PO 1648/3-2; M.S.V.: Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA) grant 451-03-65/2024-03/200178; C.S.: Austrian Science Fund (FWF) grants 10.55776/P32935, 10.55776/W1225, 10.55776/P33734; P.S.: National Institutes of Health (NIH) R01GM137430; M.S.-R.: Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA) grant 451-03-47/2023-01/200178; M.T.: Ministry of Science, Technological Development and Innovation of the Republic of Serbia (NITRA) grant 451-03-66/2024-03/200007; E.T.: Israel Science Foundation (ISF) 2121/23; C.V.: Agence Nationale de la Recherche (ANR) grant Longevity ANR-20-CE02-0015, J.V.: Fundação para a Ciência e a Tecnologia (FCT) UIDB/04293/2020; C.W.: Deutsche Forschungsgemeinschaft (DFG) grant WE 2652/7-1.
Identifiants: 99137487509311
Unité académique: Université de Montpellier
Langue: English
Type de ressource: Journal article
Champs locaux: hal-05151686