Global urban environmental change drives adaptation in white clover

James S. Santangelo, Rob W. Ness, Beata Cohan, Connor R. Fitzpatrick, Simon G. Innes, Sophie Koch, Lindsay S. Miles, Samreen Munim, Pedro R. Peres-Neto, Cindy Prashad, Alex T. Tong, Windsor E. Aguirre, Philips O. Akinwole, Marina Alberti, Jackie Álvarez, Jill T. Anderson, Joseph J. Anderson, Yoshino Ando, Nigel R. Andrew, Fabio AngeolettoDaniel N. Anstett, Julia Anstett, Felipe Aoki-Gonçalves, A. Z.Andis Arietta, Mary T.K. Arroyo, Emily J. Austen, Fernanda Baena-Díaz, Cory A. Barker, Howard A. Baylis, Julia M. Beliz, Alfonso Benitez-Mora, David Bickford, Gabriela Biedebach, Gwylim S. Blackburn, Mannfred M.A. Boehm, Stephen P. Bonser, Dries Bonte, Jesse R. Bragger, Cristina Branquinho, Kristien I. Brans, Jorge C. Bresciano, Peta D. Brom, Anna Bucharova, Briana Burt, James F. Cahill, Katelyn D. Campbell, Elizabeth J. Carlen, Diego Carmona, Maria Clara Castellanos, Giada Centenaro, Izan Chalen, Jaime A. Chaves, Mariana Chávez-Pesqueira, Xiao Yong Chen, Angela M. Chilton, Kristina M. Chomiak, Diego F. Cisneros-Heredia, Ibrahim K. Cisse, Aimée T. Classen, Mattheau S. Comerford, Camila Cordoba Fradinger, Hannah Corney, Andrew J. Crawford, Kerri M. Crawford, Maxime Dahirel, Santiago David, Robert De Haan, Nicholas J. Deacon, Clare Dean, Ek Del-Val, Eleftherios K. Deligiannis, Derek Denney, Margarete A. Dettlaff, Michelle F. DiLeo, Yuan Yuan Ding, Moisés E. Domínguez-López, Davide M. Dominoni, Savannah L. Draud, Karen Dyson, Jacintha Ellers, Carlos I. Espinosa, Liliana Essi, Mohsen Falahati-Anbaran, Jéssica C.F. Falcão, Hayden T. Fargo, Mark D.E. Fellowes, Raina M. Fitzpatrick, Leah E. Flaherty, Pádraic J. Flood, María F. Flores, Juan Fornoni, Amy G. Foster, Christopher J. Frost, Tracy L. Fuentes, Justin R. Fulkerson, Edeline Gagnon, Frauke Garbsch, Colin J. Garroway, Aleeza C. Gerstein, Mischa M. Giasson, E. Binney Girdler, Spyros Gkelis, William Godsoe, Anneke M. Golemiec, Mireille Golemiec, César González-Lagos, Amanda J. Gorton, Kiyoko M. Gotanda, Gustaf Granath, Stephan Greiner, Joanna S. Griffiths, Filipa Grilo, Pedro E. Gundel, Benjamin Hamilton, Joyce M. Hardin, Tianhua He, Stephen B. Heard, André F. Henriques, Melissa Hernández-Poveda, Molly C. Hetherington-Rauth, Sarah J. Hill, Dieter F. Hochuli, Kathryn A. Hodgins, Glen R. Hood, Gareth R. Hopkins, Katherine A. Hovanes, Ava R. Howard, Sierra C. Hubbard, Carlos N. Ibarra-Cerdeña, Carlos Iñiguez-Armijos, Paola Jara-Arancio, Benjamin J.M. Jarrett, Manon Jeannot, Vania Jiménez-Lobato, Mae Johnson, Oscar Johnson, Philip P. Johnson, Reagan Johnson, Matthew P. Josephson, Meen Chel Jung, Michael G. Just, Aapo Kahilainen, Otto S. Kailing, Eunice Kariñho-Betancourt, Regina Karousou, Lauren A. Kirn, Anna Kirschbaum, Anna Liisa Laine, Jalene M. LaMontagne, Christian Lampei, Carlos Lara, Erica L. Larson, Adrián Lázaro-Lobo, Jennifer H. Le, Deleon S. Leandro, Christopher Lee, Yunting Lei, Carolina A. León, Manuel E. Lequerica Tamara, Danica C. Levesque, Wan Jin Liao, Megan Ljubotina, Hannah Locke, Martin T. Lockett, Tiffany C. Longo, Jeremy T. Lundholm, Thomas MacGillavry, Christopher R. Mackin, Alex R. Mahmoud, Isaac A. Manju, Janine Mariën, D. Nayeli Martínez, Marina Martínez-Bartolomé, Emily K. Meineke, Wendy Mendoza-Arroyo, Thomas J.S. Merritt, Lila Elizabeth L. Merritt, Giuditta Migiani, Emily S. Minor, Nora Mitchell, Mitra Mohammadi Bazargani, Angela T. Moles, Julia D. Monk, Christopher M. Moore, Paula A. Morales-Morales, Brook T. Moyers, Miriam Muñoz-Rojas, Jason Munshi-South, Shannon M. Murphy, Maureen M. Murúa, Melisa Neila, Ourania Nikolaidis, Iva Njunjić, Peter Nosko, Juan Núñez-Farfán, Takayuki Ohgushi, Kenneth M. Olsen, Øystein H. Opedal, Cristina Ornelas, Amy L. Parachnowitsch, Aaron S. Paratore, Angela M. Parody-Merino, Juraj Paule, Octávio S. Paulo, João Carlos Pena, Vera W. Pfeiffer, Pedro Pinho, Anthony Piot, Ilga M. Porth, Nicholas Poulos, Adriana Puentes, Jiao Qu, Estela Quintero-Vallejo, Steve M. Raciti, Joost A.M. Raeymaekers, Krista M. Raveala, Diana J. Rennison, Milton C. Ribeiro, Jonathan L. Richardson, Gonzalo Rivas-Torres, Benjamin J. Rivera, Adam B. Roddy, Erika Rodriguez-Muñoz, José Raúl Román, Laura S. Rossi, Jennifer K. Rowntree, Travis J. Ryan, Santiago Salinas, Nathan J. Sanders, Luis Y. Santiago-Rosario, Amy M. Savage, J. F. Scheepens, Menno Schilthuizen, Adam C. Schneider, Tiffany Scholier, Jared L. Scott, Summer A. Shaheed, Richard P. Shefferson, Caralee A. Shepard, Jacqui A. Shykoff, Georgianna Silveira, Alexis D. Smith, Lizet Solis-Gabriel, Antonella Soro, Katie V. Spellman, Kaitlin Stack Whitney, Indra Starke-Ottich, Jörg G. Stephan, Jessica D. Stephens, Justyna Szulc, Marta Szulkin, Ayco J.M. Tack, Ítalo Tamburrino, Tayler D. Tate, Emmanuel Tergemina, Panagiotis Theodorou, Ken A. Thompson, Caragh G. Threlfall, Robin M. Tinghitella, Lilibeth Toledo-Chelala, Xin Tong, Léa Uroy, Shunsuke Utsumi, Martijn L. Vandegehuchte, Acer VanWallendael, Paula M. Vidal, Susana M. Wadgymar, Ai Ying Wang, Nian Wang, Montana L. Warbrick, Kenneth D. Whitney, Miriam Wiesmeier, J. Tristian Wiles, Jianqiang Wu, Zoe A. Xirocostas, Zhaogui Yan, Jiahe Yao, Jeremy B. Yoder, Owen Yoshida, Jingxiong Zhang, Zhigang Zhao, Carly D. Ziter, Matthew P. Zuellig, Rebecca A. Zufall, Juan E. Zurita, Sharon E. Zytynska, Marc T.J. Johnson

    Research output: Contribution to JournalArticleAcademicpeer-review

    Abstract

    Urbanization transforms environments in ways that alter biological evolution. We examined whether urban environmental change drives parallel evolution by sampling 110,019 white clover plants from 6169 populations in 160 cities globally. Plants were assayed for a Mendelian antiherbivore defense that also affects tolerance to abiotic stressors. Urban-rural gradients were associated with the evolution of clines in defense in 47% of cities throughout the world. Variation in the strength of clines was explained by environmental changes in drought stress and vegetation cover that varied among cities. Sequencing 2074 genomes from 26 cities revealed that the evolution of urban-rural clines was best explained by adaptive evolution, but the degree of parallel adaptation varied among cities. Our results demonstrate that urbanization leads to adaptation at a global scale.

    Original languageEnglish
    Pages (from-to)1275-1281
    Number of pages7
    JournalScience (New York, N.Y.)
    Volume375
    Issue number6586
    Early online date17 Mar 2022
    DOIs
    Publication statusPublished - 18 Mar 2022

    Funding

    The Global Urban Evolution project was primarily funded by an NSERC Discovery Grant, Canada Research Chair and NSERC Steacie Fellowship to M.T.J.J. J.S.S. received funding from an NSERC Canadian Graduate Scholarship and C.R.F. is funded by an NSERC Postdoctoral Fellowship. P.R.P.-N., R.W.N., and J.C.C. were supported by NSERC Discovery grants. M.A. was funded by NSF RCN DEB-1840663. F.A. received funding from CAPES. M.T.K.A. was funded by CONICYT PIA APOYO CCTE AFB170008. J.R.B, T.C.L., and S.A.S were supported by Monmouth University School of Science Summer Research Program. E.G. was funded by Département de Biologie, Université de Moncton. C.G.-L. received funding from the Center of Applied Ecology and Sustainability (CAPES), and ANID PIA/BASAL FB0002. S.G. was funded by the Max Planck Society. P.J.-A. was funded by ANID PIA/BASAL FB210006. I.N. and M.S. were supported by Leiden Municipality. K.M.O. was funded by US NSF awards IOS-1557770 and DEB-1601641. J.C.P. thanks FAPESP process 2018/00107-3 and M.C.R. thanks CNPq and FAPESP.

    FundersFunder number
    Center of Applied Ecology and Sustainability
    Département de Biologie, Université de Moncton
    Leiden Municipality
    National Science FoundationDEB-1601641, IOS-1557770, RCN DEB-1840663
    Natural Sciences and Engineering Research Council of Canada
    Fundação de Amparo à Pesquisa do Estado de São Paulo2018/00107-3
    Comisión Nacional de Investigación Científica y TecnológicaAFB170008
    Conselho Nacional de Desenvolvimento Científico e Tecnológico
    Max-Planck-GesellschaftPIA/BASAL FB210006
    Agencia Nacional de Investigación y DesarrolloPIA/BASAL FB0002

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