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

Abstract

Drosophila melanogaster; Dataset; Ecological genomics

Drosophila melanogaster; Conjunt de dades; Genòmica ecològica

Drosophila melanogaster; Conjunto de datos; Genómica ecológica

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 to 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. For example, we showed 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 spatiotemporal patterns of genetic variation in this classic model system.

J.C.B.N. was supported by start-up funds from the University of Vermont. M.Kap. was supported by the Horizon Europe project FAIRiCUBE (grant #101059238). S.S. was 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-CE02-011-01).