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

Author:

Whiting James R.ORCID,Booker Tom R.,Rougeux Clément,Lind Brandon M.,Singh Pooja,Lu MengmengORCID,Huang KaichiORCID,Whitlock Michael C.ORCID,Aitken Sally N.ORCID,Andrew Rose L.ORCID,Borevitz Justin O.,Bruhl Jeremy J.,Collins Timothy L.,Fischer Martin C.ORCID,Hodgins Kathryn A.ORCID,Holliday Jason A.,Ingvarsson Pär K.ORCID,Janes Jasmine K.ORCID,Khandaker Momena,Koenig DanielORCID,Kreiner Julia M.,Kremer AntoineORCID,Lascoux MartinORCID,Leroy ThibaultORCID,Milesi PascalORCID,Murray Kevin D.ORCID,Pyhäjärvi TanjaORCID,Rellstab ChristianORCID,Rieseberg Loren H.ORCID,Roux FabriceORCID,Stinchcombe John R.ORCID,Telford Ian R. H.,Todesco MarcoORCID,Tyrmi Jaakko S.,Wang BaoshengORCID,Weigel DetlefORCID,Willi Yvonne,Wright Stephen I.ORCID,Zhou Lecong,Yeaman SamORCID

Abstract

AbstractClosely 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 (~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.

Funder

Alberta Innovates | Alberta Innovates - Health Solutions

Gouvernement du Canada | Natural Sciences and Engineering Research Council of Canada

Publisher

Springer Science and Business Media LLC

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