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

Nunez, Joaquin C B and Coronado-Zamora, Marta and Gautier, Mathieu and Kapun, Martin and Steindl, Sonja and Ometto, Lino and Hoedjes, Katja and Beets, Julia and Wiberg, R Axel W and Mazzeo, Giovanni R and Bass, David J and Radionov, Denys and Kozeretska, Iryna and Zinchenko, Mariia and Protsenko, Oleksandra and Serga, Svitlana V and Amor-Jimenez, Cristina and Casillas, Sònia and Sánchez-Gracia, Alejandro and Patenkovic, Aleksandra and Glaser-Schmitt, Amanda and Barbadilla, Antonio and Buendia-Ruíz, Antonio J and Bertelli, Astra Clelia and Kiss, Balázs and Önder, Banu Sebnem and Matrín, Bélen Roldán and Wertheim, Bregje and Deschamps, Candice and Arboleda-Bustos, Carlos E and Tinedo, Carlos and Feller, Christian and Schlötterer, Christian and Lawler, Clancy and Fricke, Claudia and Vieira, Cristina P. and Vieira, Cristina and Obbard, Darren J. and Orengo, Dorcas Juana and Vela, Doris and Amat, Eduardo and Loreto, Elgion and Kerdaffrec, Envel and Durmaz Mitchell, Esra and Puerma, Eva and Staubach, Fabian and Camus, M. Florencia and Colinet, Hervé and Hrcek, Jan and Sørensen, Jesper Givskov and Abbott, Jessica and Torro, Joan and Parsch, John and Vieira, Jorge and Olmo, Jose Luis and Khfif, Khalid and Wojciechowski, Krzysztof and Madi-Ravazzi, Lilian and Kankare, Maaria and Schou, Mads F and Ladoukakis, Emmanuel D. and Gómez-Julián, M. Josefa and Espinosa-Jimenez, M. Luisa and Garcia Guerreiro, Maria Pilar and Parakatselaki, Maria-Eleni and Veselinovic, Marija Savic and Tanaskovic, Marija and Stamenkovic-Radak, Marina and Paris, Margot and Pascual, Marta and Ritchie, Michael G. and Rera, Michel and Jelić, Mihailo and Hojat Ansari, Mina and Rakic, Mina and Merenciano, Miriam and Hernandes, Natalia and Gora, Nazar and Rode, Nicolas and Rota-Stabelli, Omar and Sepulveda, Paloma and Gibert, Patricia and Carazo, Pau and Kohlmeier, Pinar and Erickson, Priscilla A. and Vitalis, Renaud and Torres, Jorge Roberto and Guirao-Rico, Sara and Ramos-Onsins, Sebastian E. and Castillo, Silvana and Paulo, Tânia F and Tyukmaeva, Venera and Alonso, Zahara and Alatortsev, Vladimir E. and Pasyukova, Elena and Mukha, Dmitry V. and Petrov, Dmitri A. and Schmidt, Paul and Flatt, Thomas and Bergland, Alan O. and Gonzalez, Josefa (2025) Footprints of Worldwide Adaptation in Structured Populations of Drosophila melanogaster Through the Expanded DEST 2.0 Genomic Resource. MOLECULAR BIOLOGY AND EVOLUTION, 42 (8). pp. 1-28. ISSN 0737-4038

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Abstract

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.

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