Global urban environmental change drives adaptation in white clover

James S. Santangelo; Rob W. Ness; Beata Cohan; CR Fitzpatrick; Simon G. Innes; Sophie Koch; Lindsay S. Miles; Samreen Munim; Pedro R. Peres-Neto; Cindy Prashad; AT Tong; Windsor E. Aguirre; Philips O. Akinwole; Marina Alberti; Jackie Álvarez; JT Anderson; JJ Anderson; Yoshino Ando; Nigel R. Andrew; Fabio Angeoletto; DN Anstett; J Anstett; Felipe Aoki-Gonçalves; AZA 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; AJ Crawford; KM Crawford; Maxime Dahirel; Santiago David; Haan R De; 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; Jennifer Rowntree

doi:10.1126/science.abk0989

Global urban environmental change drives adaptation in white clover

James S. Santangelo, Rob W. Ness, Beata Cohan, CR Fitzpatrick, Simon G. Innes, Sophie Koch, Lindsay S. Miles, Samreen Munim, Pedro R. Peres-Neto, Cindy Prashad, AT Tong, Windsor E. Aguirre, Philips O. Akinwole, Marina Alberti, Jackie Álvarez, JT Anderson, JJ Anderson, Yoshino Ando, Nigel R. Andrew, Fabio AngeolettoDN Anstett, J Anstett, Felipe Aoki-Gonçalves, AZA 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, AJ Crawford, KM Crawford, Maxime Dahirel, Santiago David, Haan R De, 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, Jennifer Rowntree

School of Biological and Marine Sciences

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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)	1275-1281
Journal	Science
Volume	375
Issue number	6586
DOIs	https://doi.org/10.1126/science.abk0989
Publication status	Published - 18 Mar 2022

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2022 Santangelo ScienceAccepted author manuscript, 1.57 MB

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Santangelo, J. S., Ness, R. W., Cohan, B., Fitzpatrick, CR., Innes, S. G., Koch, S., Miles, L. S., Munim, S., Peres-Neto, P. R., Prashad, C., Tong, AT., Aguirre, W. E., Akinwole, P. O., Alberti, M., Álvarez, J., Anderson, JT., Anderson, JJ., Ando, Y., Andrew, N. R., ... Rowntree, J. (2022). Global urban environmental change drives adaptation in white clover. Science, 375(6586), 1275-1281. https://doi.org/10.1126/science.abk0989

@article{092f90a1a6b14b65aef5d5e2a1877355,

title = "Global urban environmental change drives adaptation in white clover",

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.",

author = "Santangelo, \{James S.\} and Ness, \{Rob W.\} and Beata Cohan and CR Fitzpatrick and Innes, \{Simon G.\} and Sophie Koch and Miles, \{Lindsay S.\} and Samreen Munim and Peres-Neto, \{Pedro R.\} and Cindy Prashad and AT Tong and Aguirre, \{Windsor E.\} and Akinwole, \{Philips O.\} and Marina Alberti and Jackie {\'A}lvarez and JT Anderson and JJ Anderson and Yoshino Ando and Andrew, \{Nigel R.\} and Fabio Angeoletto and DN Anstett and J Anstett and Felipe Aoki-Gon{\c c}alves and AZA Arietta and Arroyo, \{Mary T.K.\} and Austen, \{Emily J.\} and Fernanda Baena-D{\'i}az and Barker, \{Cory A.\} and Baylis, \{Howard A.\} and Beliz, \{Julia M.\} and Alfonso Benitez-Mora and David Bickford and Gabriela Biedebach and Blackburn, \{Gwylim S.\} and Boehm, \{Mannfred M.A.\} and Bonser, \{Stephen P.\} and Dries Bonte and Bragger, \{Jesse R.\} and Cristina Branquinho and Brans, \{Kristien I.\} and Bresciano, \{Jorge C.\} and Brom, \{Peta D.\} and Anna Bucharova and Briana Burt and Cahill, \{James F.\} and Campbell, \{Katelyn D.\} and Carlen, \{Elizabeth J.\} and Diego Carmona and Castellanos, \{Maria Clara\} and Giada Centenaro and Izan Chalen and Chaves, \{Jaime A.\} and Mariana Ch{\'a}vez-Pesqueira and Chen, \{Xiao Yong\} and Chilton, \{Angela M.\} and Chomiak, \{Kristina M.\} and Cisneros-Heredia, \{Diego F.\} and Cisse, \{Ibrahim K.\} and Classen, \{Aim{\'e}e T.\} and Comerford, \{Mattheau S.\} and Fradinger, \{Camila Cordoba\} and Hannah Corney and AJ Crawford and KM Crawford and Maxime Dahirel and Santiago David and De, \{Haan R\} and Deacon, \{Nicholas J.\} and Clare Dean and Ek del-Val and Deligiannis, \{Eleftherios K.\} and Derek Denney and Dettlaff, \{Margarete A.\} and DiLeo, \{Michelle F.\} and Ding, \{Yuan Yuan\} and Dom{\'i}nguez-L{\'o}pez, \{Mois{\'e}s E.\} and Dominoni, \{Davide M.\} and Draud, \{Savannah L.\} and Karen Dyson and Jacintha Ellers and Espinosa, \{Carlos I.\} and Liliana Essi and Mohsen Falahati-Anbaran and Jennifer Rowntree",

year = "2022",

month = mar,

day = "18",

doi = "10.1126/science.abk0989",

language = "English",

volume = "375",

pages = "1275--1281",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6586",

}

Santangelo, JS, Ness, RW, Cohan, B, Fitzpatrick, CR, Innes, SG, Koch, S, Miles, LS, Munim, S, Peres-Neto, PR, Prashad, C, Tong, AT, Aguirre, WE, Akinwole, PO, Alberti, M, Álvarez, J, Anderson, JT, Anderson, JJ, Ando, Y, Andrew, NR, Angeoletto, F, Anstett, DN, Anstett, J, Aoki-Gonçalves, F, Arietta, AZA, Arroyo, MTK, Austen, EJ, Baena-Díaz, F, Barker, CA, Baylis, HA, Beliz, JM, Benitez-Mora, A, Bickford, D, Biedebach, G, Blackburn, GS, Boehm, MMA, Bonser, SP, Bonte, D, Bragger, JR, Branquinho, C, Brans, KI, Bresciano, JC, Brom, PD, Bucharova, A, Burt, B, Cahill, JF, Campbell, KD, Carlen, EJ, Carmona, D, Castellanos, MC, Centenaro, G, Chalen, I, Chaves, JA, Chávez-Pesqueira, M, Chen, XY, Chilton, AM, Chomiak, KM, Cisneros-Heredia, DF, Cisse, IK, Classen, AT, Comerford, MS, Fradinger, CC, Corney, H, Crawford, AJ, Crawford, KM, Dahirel, M, David, S, De, HR, Deacon, NJ, Dean, C, del-Val, E, Deligiannis, EK, Denney, D, Dettlaff, MA, DiLeo, MF, Ding, YY, Domínguez-López, ME, Dominoni, DM, Draud, SL, Dyson, K, Ellers, J, Espinosa, CI, Essi, L, Falahati-Anbaran, M & Rowntree, J 2022, 'Global urban environmental change drives adaptation in white clover', Science, vol. 375, no. 6586, pp. 1275-1281. https://doi.org/10.1126/science.abk0989

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, CR

AU - Innes, Simon G.

AU - Koch, Sophie

AU - Miles, Lindsay S.

AU - Munim, Samreen

AU - Peres-Neto, Pedro R.

AU - Prashad, Cindy

AU - Tong, AT

AU - Aguirre, Windsor E.

AU - Akinwole, Philips O.

AU - Alberti, Marina

AU - Álvarez, Jackie

AU - Anderson, JT

AU - Anderson, JJ

AU - Ando, Yoshino

AU - Andrew, Nigel R.

AU - Angeoletto, Fabio

AU - Anstett, DN

AU - Anstett, J

AU - Aoki-Gonçalves, Felipe

AU - Arietta, AZA

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, AJ

AU - Crawford, KM

AU - Dahirel, Maxime

AU - David, Santiago

AU - De, Haan R

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 - Rowntree, Jennifer

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 - https://pearl.plymouth.ac.uk/bms-research/2025/

U2 - 10.1126/science.abk0989

DO - 10.1126/science.abk0989

M3 - Article

SN - 0036-8075

VL - 375

SP - 1275

EP - 1281

JO - Science

JF - Science

IS - 6586

ER -

Global urban environmental change drives adaptation in white clover

Abstract

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