The genetic architecture of repeated local adaptation to climate in distantly related plants

被引:19
作者
Whiting, James R. [1 ]
Booker, Tom R. [2 ,3 ]
Rougeux, Clement [1 ]
Lind, Brandon M. [1 ,3 ]
Singh, Pooja [1 ,4 ,5 ]
Lu, Mengmeng [1 ,6 ]
Huang, Kaichi [7 ,8 ]
Whitlock, Michael C. [2 ]
Aitken, Sally N. [3 ]
Andrew, Rose L. [9 ]
Borevitz, Justin O. [10 ]
Bruhl, Jeremy J. [9 ]
Collins, Timothy L. [11 ,12 ]
Fischer, Martin C. [13 ]
Hodgins, Kathryn A. [14 ]
Holliday, Jason A. [15 ]
Ingvarsson, Par K. [16 ]
Janes, Jasmine K. [17 ,18 ,19 ]
Khandaker, Momena [9 ]
Koenig, Daniel [20 ,21 ]
Kreiner, Julia M. [7 ,8 ,22 ]
Kremer, Antoine [23 ]
Lascoux, Martin [24 ,25 ]
Leroy, Thibault [26 ]
Milesi, Pascal [24 ,25 ]
Murray, Kevin D. [10 ,27 ]
Pyhajarvi, Tanja [28 ,29 ]
Rellstab, Christian [30 ]
Rieseberg, Loren H. [7 ,8 ]
Roux, Fabrice [31 ]
Stinchcombe, John R. [22 ]
Telford, Ian R. H. [9 ]
Todesco, Marco [7 ,8 ,32 ,33 ]
Tyrmi, Jaakko S. [34 ]
Wang, Baosheng [35 ]
Weigel, Detlef [27 ]
Willi, Yvonne [36 ]
Wright, Stephen I. [22 ]
Zhou, Lecong [15 ]
Yeaman, Sam [1 ]
机构
[1] Univ Calgary, Dept Biol Sci, Calgary, AB, Canada
[2] Univ British Columbia, Fac Sci, Dept Zool, Vancouver, BC, Canada
[3] Univ British Columbia, Fac Forestry, Dept Forest & Conservat Sci, Vancouver, BC, Canada
[4] Univ Bern, Inst Ecol & Evolut, Aquat Ecol & Evolut, Bern, Switzerland
[5] EAWAG, Swiss Fed Inst Aquat Sci & Technol, Dubendorf, Switzerland
[6] Univ Notre Dame, Dept Biol Sci, Notre Dame, IN USA
[7] Univ British Columbia, Dept Bot, Vancouver, BC, Canada
[8] Univ British Columbia, Biodivers Res Ctr, Vancouver, BC, Canada
[9] Univ New England, Sch Environm & Rural Sci, Armidale, NSW, Australia
[10] Australian Natl Univ, Res Sch Biol, Canberra, ACT, Australia
[11] Dept Planning & Environm, Queanbeyan, NSW, Australia
[12] Dept Climate Change Energy Environm & Water, Queanbeyan, NSW, Australia
[13] Swiss Fed Inst Technol, Inst Integrat Biol IBZ, Zurich, Switzerland
[14] Monash Univ, Sch Biol Sci, Melbourne, Vic, Australia
[15] Virginia Tech, Dept Forest Resources & Environm Conservat, Blacksburg, VA USA
[16] Swedish Univ Agr Sci, Dept Plant Biol, Uppsala, Sweden
[17] Vancouver Isl Univ, Biol Dept, Nanaimo, BC, Canada
[18] Univ Northern British Columbia, Dept Ecosyst Sci & Management, Prince George, BC, Canada
[19] IUCN North Amer, Species Survival Commiss, Orchid Specialist Grp, Washington, DC USA
[20] Univ Calif Riverside, Dept Bot & Plant Sci, Riverside, CA USA
[21] Univ Calif Riverside, Inst Integrat Genome Biol, Riverside, CA USA
[22] Univ Toronto, Dept Ecol & Evolutionary Biol, Toronto, ON, Canada
[23] Univ Bordeaux, UMR BIOGECO, INRAE, 69 Route Arcachon, Cestas, France
[24] Uppsala Univ, Evolutionary Biol Ctr, Dept Ecol & Genet, Program Plant Ecol & Evolut, Uppsala, Sweden
[25] Uppsala Univ, Sci Life Lab, Uppsala, Sweden
[26] Univ Toulouse, GenPhySE, INRAE, ENVT, Castanet Tolosan, France
[27] Max Planck Inst Biol Tubingen, Dept Mol Biol, Tubingen, Germany
[28] Univ Helsinki, Dept Forest Sci, Helsinki, Finland
[29] Univ Helsinki, Viikki Plant Sci Ctr, Helsinki, Finland
[30] Swiss Fed Res Inst WSL, Birmensdorf, Switzerland
[31] Univ Toulouse, Inst Natl Rech Agr Alimentat & Environm, Lab Interact Plantes Microbes Environm, CNRS, Castanet-tolosan, France
[32] Univ British Columbia, Michael Smith Labs, Vancouver, BC, Canada
[33] Univ British Columbia, Dept Biol, Kelowna, BC, Canada
[34] Univ Oulu, Dept Ecol & Genet, Oulu, Finland
[35] South China Natl Bot Garden, Guangzhou, Peoples R China
[36] Univ Basel, Dept Environm Sci, Basel, Switzerland
基金
加拿大自然科学与工程研究理事会;
关键词
GENOMES REVEAL; EVOLUTION; CONVERGENCE; PARALLELISM; PLEIOTROPY; EXPRESSION; RESPONSES; MULTIPLE; COST;
D O I
10.1038/s41559-024-02514-5
中图分类号
Q14 [生态学(生物生态学)];
学科分类号
071012 ; 0713 ;
摘要
Closely related species often use the same genes to adapt to similar environments. However, we know little about why such genes possess increased adaptive potential and whether this is conserved across deeper evolutionary lineages. Adaptation to climate presents a natural laboratory to test these ideas, as even distantly related species must contend with similar stresses. Here, we re-analyse genomic data from thousands of individuals from 25 plant species as diverged as lodgepole pine and Arabidopsis (similar to 300 Myr). We test for genetic repeatability based on within-species associations between allele frequencies in genes and variation in 21 climate variables. Our results demonstrate significant statistical evidence for genetic repeatability across deep time that is not expected under randomness, identifying a suite of 108 gene families (orthogroups) and gene functions that repeatedly drive local adaptation to climate. This set includes many orthogroups with well-known functions in abiotic stress response. Using gene co-expression networks to quantify pleiotropy, we find that orthogroups with stronger evidence for repeatability exhibit greater network centrality and broader expression across tissues (higher pleiotropy), contrary to the 'cost of complexity' theory. These gene families may be important in helping wild and crop species cope with future climate change, representing important candidates for future study.
引用
收藏
页码:1933 / 1947
页数:26
相关论文
共 98 条
[1]   Hormone interactions in stomatal function [J].
Acharya, Biswa R. ;
Assmann, Sarah M. .
PLANT MOLECULAR BIOLOGY, 2009, 69 (04) :451-462
[2]   1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana [J].
Alonso-Blanco, Carlos ;
Andrade, Jorge ;
Becker, Claude ;
Bemm, Felix ;
Bergelson, Joy ;
Borgwardt, Karsten M. ;
Cao, Jun ;
Chae, Eunyoung ;
Dezwaan, Todd M. ;
Ding, Wei ;
Ecker, Joseph R. ;
Exposito-Alonso, Moises ;
Farlow, Ashley ;
Fitz, Joffrey ;
Gan, Xiangchao ;
Grimm, Dominik G. ;
Hancock, Angela M. ;
Henz, Stefan R. ;
Holm, Svante ;
Horton, Matthew ;
Jarsulic, Mike ;
Kerstetter, Randall A. ;
Korte, Arthur ;
Korte, Pamela ;
Lanz, Christa ;
Lee, Cheng-Ruei ;
Meng, Dazhe ;
Michael, Todd P. ;
Mott, Richard ;
Muliyati, Ni Wayan ;
Nagele, Thomas ;
Nagler, Matthias ;
Nizhynska, Viktoria ;
Nordborg, Magnus ;
Novikova, Polina Yu. ;
Pico, F. Xavier ;
Platzer, Alexander ;
Rabanal, Fernando A. ;
Rodriguez, Alex ;
Rowan, Beth A. ;
Salome, Patrice A. ;
Schmid, Karl J. ;
Schmitz, Robert J. ;
Seren, Umit ;
Sperone, Felice Gianluca ;
Sudkamp, Mitchell ;
Svardal, Hannes ;
Tanzer, Matt M. ;
Todd, Donald ;
Volchenboum, Samuel L. .
CELL, 2016, 166 (02) :481-491
[3]   Plant adaptation to climate change-Where are we? [J].
Anderson, Jill T. ;
Song, Bao-Hua .
JOURNAL OF SYSTEMATICS AND EVOLUTION, 2020, 58 (05) :533-545
[4]   Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? [J].
Arendt, Jeff ;
Reznick, David .
TRENDS IN ECOLOGY & EVOLUTION, 2008, 23 (01) :26-32
[5]   Contingency and determinism in evolution: Replaying life's tape [J].
Blount, Zachary D. ;
Lenski, Richard E. ;
Losos, Jonathan B. .
SCIENCE, 2018, 362 (6415)
[6]   Divergence time shapes gene reuse during repeated adaptation [J].
Bohutinska, Magdalena ;
Peichel, Catherine L. .
TRENDS IN ECOLOGY & EVOLUTION, 2024, 39 (04) :396-407
[7]   Genomic basis of parallel adaptation varies with divergence in Arabidopsis and its relatives [J].
Bohutinska, Magdalena ;
Vlcek, Jakub ;
Yair, Sivan ;
Laenen, Benjamin ;
Konecna, Veronika ;
Fracassetti, Marco ;
Slotte, Tanja ;
Kolar, Filip .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2021, 118 (21)
[8]   Novelty and Convergence in Adaptation to Whole Genome Duplication [J].
Bohutinska, Magdalena ;
Alston, Mark ;
Monnahan, Patrick ;
Mandakova, Terezie ;
Bray, Sian ;
Paajanen, Pirita ;
Kolar, Filip ;
Yant, Levi .
MOLECULAR BIOLOGY AND EVOLUTION, 2021, 38 (09) :3910-3924
[9]   (Non)Parallel Evolution [J].
Bolnick, Daniel I. ;
Barrett, Rowan D. H. ;
Oke, Krista B. ;
Rennison, Diana J. ;
Stuart, Yoel E. .
ANNUAL REVIEW OF ECOLOGY, EVOLUTION, AND SYSTEMATICS, VOL 49, 2018, 49 :303-330
[10]   Using genome scans to identify genes used repeatedly for adaptation [J].
Booker, Tom R. ;
Yeaman, Sam ;
Whitlock, Michael C. .
EVOLUTION, 2023, 77 (03) :801-811