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 language | English |
|---|---|
| Pages (from-to) | 1-118 |
| Number of pages | 118 |
| Journal | Science (New York, N.Y.) |
| Volume | 375 |
| Issue number | 6586 |
| DOIs | |
| Publication status | Published - 18 Mar 2022 |
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Global urban environmental change drives adaptation in white clover. / Santangelo, James S.; Ness, Rob W.; Cohan, Beata; Fitzpatrick, Connor R.; Innes, Simon G.; Koch, Sophie; Miles, Lindsay S.; Munim, Samreen; Peres-Neto, Pedro R.; Prashad, Cindy; Tong, Alex T.; Aguirre, Windsor E.; Akinwole, Philips O.; Alberti, Marina; Álvarez, Jackie; Anderson, Jill T.; Anderson, Joseph J.; Ando, Yoshino; Andrew, Nigel R.; Angeoletto, Fabio; Anstett, Daniel N.; Anstett, Julia; Aoki-Gonçalves, Felipe; Arietta, A. Z.Andis; Arroyo, Mary T.K.; Austen, Emily J.; Baena-Díaz, Fernanda; Barker, Cory A.; Baylis, Howard A.; Beliz, Julia M.; Benitez-Mora, Alfonso; Bickford, David; Biedebach, Gabriela; Blackburn, Gwylim S.; Boehm, Mannfred M.A.; Bonser, Stephen P.; Bonte, Dries; Bragger, Jesse R.; Branquinho, Cristina; Brans, Kristien I.; Bresciano, Jorge C.; Brom, Peta D.; Bucharova, Anna; Burt, Briana; Cahill, James F.; Campbell, Katelyn D.; Carlen, Elizabeth J.; Carmona, Diego; Castellanos, Maria Clara; Centenaro, Giada; Chalen, Izan; Chaves, Jaime A.; Chávez-Pesqueira, Mariana; Chen, Xiao Yong; Chilton, Angela M.; Chomiak, Kristina M.; Cisneros-Heredia, Diego F.; Cisse, Ibrahim K.; Classen, Aimée T.; Comerford, Mattheau S.; Fradinger, Camila Cordoba; Corney, Hannah; Crawford, Andrew J.; Crawford, Kerri M.; Dahirel, Maxime; David, Santiago; De Haan, Robert; Deacon, Nicholas J.; Dean, Clare; Del-Val, Ek; Deligiannis, Eleftherios K.; Denney, Derek; Dettlaff, Margarete A.; DiLeo, Michelle F.; Ding, Yuan Yuan; Domínguez-López, Moisés E.; Dominoni, Davide M.; Draud, Savannah L.; Dyson, Karen; Ellers, Jacintha; Espinosa, Carlos I.; Essi, Liliana; Falahati-Anbaran, Mohsen; Falcão, Jéssica C.F.; Fargo, Hayden T.; Fellowes, Mark D.E.; Fitzpatrick, Raina M.; Flaherty, Leah E.; Flood, Pádraic J.; Flores, María F.; Fornoni, Juan; Foster, Amy G.; Frost, Christopher J.; Fuentes, Tracy L.; Fulkerson, Justin R.; Gagnon, Edeline; Garbsch, Frauke; Garroway, Colin J.; Gerstein, Aleeza C.; Giasson, Mischa M.; Girdler, E. Binney; Gkelis, Spyros; Godsoe, William; Golemiec, Anneke M.; Golemiec, Mireille; González-Lagos, César; Gorton, Amanda J.; Gotanda, Kiyoko M.; Granath, Gustaf; Greiner, Stephan; Griffiths, Joanna S.; Grilo, Filipa; Gundel, Pedro E.; Hamilton, Benjamin; Hardin, Joyce M.; He, Tianhua; Heard, Stephen B.; Henriques, André F.; Hernández-Poveda, Melissa; Hetherington-Rauth, Molly C.; Hill, Sarah J.; Hochuli, Dieter F.; Hodgins, Kathryn A.; Hood, Glen R.; Hopkins, Gareth R.; Hovanes, Katherine A.; Howard, Ava R.; Hubbard, Sierra C.; Ibarra-Cerdeña, Carlos N.; Iñiguez-Armijos, Carlos; Jara-Arancio, Paola; Jarrett, Benjamin J.M.; Jeannot, Manon; Jiménez-Lobato, Vania; Johnson, Mae; Johnson, Oscar; Johnson, Philip P.; Johnson, Reagan; Josephson, Matthew P.; Jung, Meen Chel; Just, Michael G.; Kahilainen, Aapo; Kailing, Otto S.; Kariñho-Betancourt, Eunice; Karousou, Regina; Kirn, Lauren A.; Kirschbaum, Anna; Laine, Anna Liisa; LaMontagne, Jalene M.; Lampei, Christian; Lara, Carlos; Larson, Erica L.; Lázaro-Lobo, Adrián; Le, Jennifer H.; Leandro, Deleon S.; Lee, Christopher; Lei, Yunting; León, Carolina A.; Lequerica Tamara, Manuel E.; Levesque, Danica C.; Liao, Wan Jin; Ljubotina, Megan; Locke, Hannah; Lockett, Martin T.; Longo, Tiffany C.; Lundholm, Jeremy T.; MacGillavry, Thomas; Mackin, Christopher R.; Mahmoud, Alex R.; Manju, Isaac A.; Mariën, Janine; Martínez, D. Nayeli; Martínez-Bartolomé, Marina; Meineke, Emily K.; Mendoza-Arroyo, Wendy; Merritt, Thomas J.S.; Merritt, Lila Elizabeth L.; Migiani, Giuditta; Minor, Emily S.; Mitchell, Nora; Mohammadi Bazargani, Mitra; Moles, Angela T.; Monk, Julia D.; Moore, Christopher M.; Morales-Morales, Paula A.; Moyers, Brook T.; Muñoz-Rojas, Miriam; Munshi-South, Jason; Murphy, Shannon M.; Murúa, Maureen M.; Neila, Melisa; Nikolaidis, Ourania; Njunjić, Iva; Nosko, Peter; Núñez-Farfán, Juan; Ohgushi, Takayuki; Olsen, Kenneth M.; Opedal, Øystein H.; Ornelas, Cristina; Parachnowitsch, Amy L.; Paratore, Aaron S.; Parody-Merino, Angela M.; Paule, Juraj; Paulo, Octávio S.; Pena, João Carlos; Pfeiffer, Vera W.; Pinho, Pedro; Piot, Anthony; Porth, Ilga M.; Poulos, Nicholas; Puentes, Adriana; Qu, Jiao; Quintero-Vallejo, Estela; Raciti, Steve M.; Raeymaekers, Joost A.M.; Raveala, Krista M.; Rennison, Diana J.; Ribeiro, Milton C.; Richardson, Jonathan L.; Rivas-Torres, Gonzalo; Rivera, Benjamin J.; Roddy, Adam B.; Rodriguez-Muñoz, Erika; Román, José Raúl; Rossi, Laura S.; Rowntree, Jennifer K.; Ryan, Travis J.; Salinas, Santiago; Sanders, Nathan J.; Santiago-Rosario, Luis Y.; Savage, Amy M.; Scheepens, J. F.; Schilthuizen, Menno; Schneider, Adam C.; Scholier, Tiffany; Scott, Jared L.; Shaheed, Summer A.; Shefferson, Richard P.; Shepard, Caralee A.; Shykoff, Jacqui A.; Silveira, Georgianna; Smith, Alexis D.; Solis-Gabriel, Lizet; Soro, Antonella; Spellman, Katie V.; Whitney, Kaitlin Stack; Starke-Ottich, Indra; Stephan, Jörg G.; Stephens, Jessica D.; Szulc, Justyna; Szulkin, Marta; Tack, Ayco J.M.; Tamburrino, Ítalo; Tate, Tayler D.; Tergemina, Emmanuel; Theodorou, Panagiotis; Thompson, Ken A.; Threlfall, Caragh G.; Tinghitella, Robin M.; Toledo-Chelala, Lilibeth; Tong, Xin; Uroy, Léa; Utsumi, Shunsuke; Vandegehuchte, Martijn L.; VanWallendael, Acer; Vidal, Paula M.; Wadgymar, Susana M.; Wang, Ai Ying; Wang, Nian; Warbrick, Montana L.; Whitney, Kenneth D.; Wiesmeier, Miriam; Wiles, J. Tristian; Wu, Jianqiang; Xirocostas, Zoe A.; Yan, Zhaogui; Yao, Jiahe; Yoder, Jeremy B.; Yoshida, Owen; Zhang, Jingxiong; Zhao, Zhigang; Ziter, Carly D.; Zuellig, Matthew P.; Zufall, Rebecca A.; Zurita, Juan E.; Zytynska, Sharon E.; Johnson, Marc T.J.
In: Science (New York, N.Y.), Vol. 375, No. 6586, 18.03.2022, p. 1-118.Research output: Contribution to Journal › Article › Academic › peer-review
TY - JOUR
T1 - Global urban environmental change drives adaptation in white clover
AU - Santangelo, James S.
AU - Ness, Rob W.
AU - Cohan, Beata
AU - Fitzpatrick, Connor R.
AU - Innes, Simon G.
AU - Koch, Sophie
AU - Miles, Lindsay S.
AU - Munim, Samreen
AU - Peres-Neto, Pedro R.
AU - Prashad, Cindy
AU - Tong, Alex T.
AU - Aguirre, Windsor E.
AU - Akinwole, Philips O.
AU - Alberti, Marina
AU - Álvarez, Jackie
AU - Anderson, Jill T.
AU - Anderson, Joseph J.
AU - Ando, Yoshino
AU - Andrew, Nigel R.
AU - Angeoletto, Fabio
AU - Anstett, Daniel N.
AU - Anstett, Julia
AU - Aoki-Gonçalves, Felipe
AU - Arietta, A. Z.Andis
AU - Arroyo, Mary T.K.
AU - Austen, Emily J.
AU - Baena-Díaz, Fernanda
AU - Barker, Cory A.
AU - Baylis, Howard A.
AU - Beliz, Julia M.
AU - Benitez-Mora, Alfonso
AU - Bickford, David
AU - Biedebach, Gabriela
AU - Blackburn, Gwylim S.
AU - Boehm, Mannfred M.A.
AU - Bonser, Stephen P.
AU - Bonte, Dries
AU - Bragger, Jesse R.
AU - Branquinho, Cristina
AU - Brans, Kristien I.
AU - Bresciano, Jorge C.
AU - Brom, Peta D.
AU - Bucharova, Anna
AU - Burt, Briana
AU - Cahill, James F.
AU - Campbell, Katelyn D.
AU - Carlen, Elizabeth J.
AU - Carmona, Diego
AU - Castellanos, Maria Clara
AU - Centenaro, Giada
AU - Chalen, Izan
AU - Chaves, Jaime A.
AU - Chávez-Pesqueira, Mariana
AU - Chen, Xiao Yong
AU - Chilton, Angela M.
AU - Chomiak, Kristina M.
AU - Cisneros-Heredia, Diego F.
AU - Cisse, Ibrahim K.
AU - Classen, Aimée T.
AU - Comerford, Mattheau S.
AU - Fradinger, Camila Cordoba
AU - Corney, Hannah
AU - Crawford, Andrew J.
AU - Crawford, Kerri M.
AU - Dahirel, Maxime
AU - David, Santiago
AU - De Haan, Robert
AU - Deacon, Nicholas J.
AU - Dean, Clare
AU - Del-Val, Ek
AU - Deligiannis, Eleftherios K.
AU - Denney, Derek
AU - Dettlaff, Margarete A.
AU - DiLeo, Michelle F.
AU - Ding, Yuan Yuan
AU - Domínguez-López, Moisés E.
AU - Dominoni, Davide M.
AU - Draud, Savannah L.
AU - Dyson, Karen
AU - Ellers, Jacintha
AU - Espinosa, Carlos I.
AU - Essi, Liliana
AU - Falahati-Anbaran, Mohsen
AU - Falcão, Jéssica C.F.
AU - Fargo, Hayden T.
AU - Fellowes, Mark D.E.
AU - Fitzpatrick, Raina M.
AU - Flaherty, Leah E.
AU - Flood, Pádraic J.
AU - Flores, María F.
AU - Fornoni, Juan
AU - Foster, Amy G.
AU - Frost, Christopher J.
AU - Fuentes, Tracy L.
AU - Fulkerson, Justin R.
AU - Gagnon, Edeline
AU - Garbsch, Frauke
AU - Garroway, Colin J.
AU - Gerstein, Aleeza C.
AU - Giasson, Mischa M.
AU - Girdler, E. Binney
AU - Gkelis, Spyros
AU - Godsoe, William
AU - Golemiec, Anneke M.
AU - Golemiec, Mireille
AU - González-Lagos, César
AU - Gorton, Amanda J.
AU - Gotanda, Kiyoko M.
AU - Granath, Gustaf
AU - Greiner, Stephan
AU - Griffiths, Joanna S.
AU - Grilo, Filipa
AU - Gundel, Pedro E.
AU - Hamilton, Benjamin
AU - Hardin, Joyce M.
AU - He, Tianhua
AU - Heard, Stephen B.
AU - Henriques, André F.
AU - Hernández-Poveda, Melissa
AU - Hetherington-Rauth, Molly C.
AU - Hill, Sarah J.
AU - Hochuli, Dieter F.
AU - Hodgins, Kathryn A.
AU - Hood, Glen R.
AU - Hopkins, Gareth R.
AU - Hovanes, Katherine A.
AU - Howard, Ava R.
AU - Hubbard, Sierra C.
AU - Ibarra-Cerdeña, Carlos N.
AU - Iñiguez-Armijos, Carlos
AU - Jara-Arancio, Paola
AU - Jarrett, Benjamin J.M.
AU - Jeannot, Manon
AU - Jiménez-Lobato, Vania
AU - Johnson, Mae
AU - Johnson, Oscar
AU - Johnson, Philip P.
AU - Johnson, Reagan
AU - Josephson, Matthew P.
AU - Jung, Meen Chel
AU - Just, Michael G.
AU - Kahilainen, Aapo
AU - Kailing, Otto S.
AU - Kariñho-Betancourt, Eunice
AU - Karousou, Regina
AU - Kirn, Lauren A.
AU - Kirschbaum, Anna
AU - Laine, Anna Liisa
AU - LaMontagne, Jalene M.
AU - Lampei, Christian
AU - Lara, Carlos
AU - Larson, Erica L.
AU - Lázaro-Lobo, Adrián
AU - Le, Jennifer H.
AU - Leandro, Deleon S.
AU - Lee, Christopher
AU - Lei, Yunting
AU - León, Carolina A.
AU - Lequerica Tamara, Manuel E.
AU - Levesque, Danica C.
AU - Liao, Wan Jin
AU - Ljubotina, Megan
AU - Locke, Hannah
AU - Lockett, Martin T.
AU - Longo, Tiffany C.
AU - Lundholm, Jeremy T.
AU - MacGillavry, Thomas
AU - Mackin, Christopher R.
AU - Mahmoud, Alex R.
AU - Manju, Isaac A.
AU - Mariën, Janine
AU - Martínez, D. Nayeli
AU - Martínez-Bartolomé, Marina
AU - Meineke, Emily K.
AU - Mendoza-Arroyo, Wendy
AU - Merritt, Thomas J.S.
AU - Merritt, Lila Elizabeth L.
AU - Migiani, Giuditta
AU - Minor, Emily S.
AU - Mitchell, Nora
AU - Mohammadi Bazargani, Mitra
AU - Moles, Angela T.
AU - Monk, Julia D.
AU - Moore, Christopher M.
AU - Morales-Morales, Paula A.
AU - Moyers, Brook T.
AU - Muñoz-Rojas, Miriam
AU - Munshi-South, Jason
AU - Murphy, Shannon M.
AU - Murúa, Maureen M.
AU - Neila, Melisa
AU - Nikolaidis, Ourania
AU - Njunjić, Iva
AU - Nosko, Peter
AU - Núñez-Farfán, Juan
AU - Ohgushi, Takayuki
AU - Olsen, Kenneth M.
AU - Opedal, Øystein H.
AU - Ornelas, Cristina
AU - Parachnowitsch, Amy L.
AU - Paratore, Aaron S.
AU - Parody-Merino, Angela M.
AU - Paule, Juraj
AU - Paulo, Octávio S.
AU - Pena, João Carlos
AU - Pfeiffer, Vera W.
AU - Pinho, Pedro
AU - Piot, Anthony
AU - Porth, Ilga M.
AU - Poulos, Nicholas
AU - Puentes, Adriana
AU - Qu, Jiao
AU - Quintero-Vallejo, Estela
AU - Raciti, Steve M.
AU - Raeymaekers, Joost A.M.
AU - Raveala, Krista M.
AU - Rennison, Diana J.
AU - Ribeiro, Milton C.
AU - Richardson, Jonathan L.
AU - Rivas-Torres, Gonzalo
AU - Rivera, Benjamin J.
AU - Roddy, Adam B.
AU - Rodriguez-Muñoz, Erika
AU - Román, José Raúl
AU - Rossi, Laura S.
AU - Rowntree, Jennifer K.
AU - Ryan, Travis J.
AU - Salinas, Santiago
AU - Sanders, Nathan J.
AU - Santiago-Rosario, Luis Y.
AU - Savage, Amy M.
AU - Scheepens, J. F.
AU - Schilthuizen, Menno
AU - Schneider, Adam C.
AU - Scholier, Tiffany
AU - Scott, Jared L.
AU - Shaheed, Summer A.
AU - Shefferson, Richard P.
AU - Shepard, Caralee A.
AU - Shykoff, Jacqui A.
AU - Silveira, Georgianna
AU - Smith, Alexis D.
AU - Solis-Gabriel, Lizet
AU - Soro, Antonella
AU - Spellman, Katie V.
AU - Whitney, Kaitlin Stack
AU - Starke-Ottich, Indra
AU - Stephan, Jörg G.
AU - Stephens, Jessica D.
AU - Szulc, Justyna
AU - Szulkin, Marta
AU - Tack, Ayco J.M.
AU - Tamburrino, Ítalo
AU - Tate, Tayler D.
AU - Tergemina, Emmanuel
AU - Theodorou, Panagiotis
AU - Thompson, Ken A.
AU - Threlfall, Caragh G.
AU - Tinghitella, Robin M.
AU - Toledo-Chelala, Lilibeth
AU - Tong, Xin
AU - Uroy, Léa
AU - Utsumi, Shunsuke
AU - Vandegehuchte, Martijn L.
AU - VanWallendael, Acer
AU - Vidal, Paula M.
AU - Wadgymar, Susana M.
AU - Wang, Ai Ying
AU - Wang, Nian
AU - Warbrick, Montana L.
AU - Whitney, Kenneth D.
AU - Wiesmeier, Miriam
AU - Wiles, J. Tristian
AU - Wu, Jianqiang
AU - Xirocostas, Zoe A.
AU - Yan, Zhaogui
AU - Yao, Jiahe
AU - Yoder, Jeremy B.
AU - Yoshida, Owen
AU - Zhang, Jingxiong
AU - Zhao, Zhigang
AU - Ziter, Carly D.
AU - Zuellig, Matthew P.
AU - Zufall, Rebecca A.
AU - Zurita, Juan E.
AU - Zytynska, Sharon E.
AU - Johnson, Marc T.J.
PY - 2022/3/18
Y1 - 2022/3/18
N2 - 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.
AB - 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.
UR - http://www.scopus.com/inward/record.url?scp=85126689688&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85126689688&partnerID=8YFLogxK
U2 - 10.1126/science.abk0989
DO - 10.1126/science.abk0989
M3 - Article
C2 - 35298255
AN - SCOPUS:85126689688
VL - 375
SP - 1
EP - 118
JO - Science
JF - Science
SN - 1095-9203
IS - 6586
ER -