A transcontinental experiment elucidates (mal)adaptation of a cosmopolitan plant to climate in space and time

Climate change and the global spread of invasive species are two of the most significant threats to biodiversity. Both of these phenomena subject populations to novel conditions, either in space (species invasion) or in time (climate change), yet the role of adaptation in how populations respond to...

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Main Authors Albano, Lucas J, Bastias, Cristina C, Estarague, Aurélien, Hendrickson, Brandon T, Innes, Simon G, King, Nevada, Patterson, Courtney M, Tudoran, Amelia, Vasseur, François, Puentes, Adriana, Violle, Cyrille, Kooyers, Nicholas J, Johnson, Marc Tj
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LanguageEnglish
Published Cold Spring Harbor Cold Spring Harbor Laboratory Press 21.11.2024
Cold Spring Harbor Laboratory
Edition1.3
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ISSN2692-8205
2692-8205
DOI10.1101/2024.09.16.613311

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Abstract Climate change and the global spread of invasive species are two of the most significant threats to biodiversity. Both of these phenomena subject populations to novel conditions, either in space (species invasion) or in time (climate change), yet the role of adaptation in how populations respond to these rapid environmental shifts is poorly understood. We conducted a large-scale trans-continental common garden experiment using white clover (Trifolium repens, Fabaceae) to test if adaptive evolution to spatiotemporal variation in climate could contribute to the ecological success of one of the most widespread invasive plant species in the world. Individuals from 96 populations of Trifolium repens (white clover) from both its native (Europe) and introduced (North America) ranges were planted into four experimental common gardens located in northern (Uppsala, Sweden) and southern (Montpellier, France) Europe, and northern (Mississauga, Canada) and southern (Louisiana, USA) North America. We recorded plant sexual and clonal fitness in each common garden and assessed whether the strength of local adaptation differed between the native and introduced ranges and whether populations are rapidly adapting to climate change. Results show that local adaptation was only evident when populations were transplanted into common gardens located in the same range (native or introduced) from which they originated and was driven by stronger selection (due to climatic factors rather than herbivory) at lower latitudes in both ranges. Our results indicate that rapid local adaptation across a large latitudinal gradient has occurred in T. repens populations in less than 400 years since its introduction to North America. However, we find evidence of an adaptation lag in the northern common garden in the introduced range, with plants from historically slightly warmer climates exhibiting the greatest fitness. These findings support two major conclusions: 1) white clover can rapidly adapt to spatial variation in climate in its introduced range as well as the native range, and 2) despite rapid adaptation to novel ranges, introduced white clover populations are not keeping pace with rapid climate change. Overall, our results provide insight into the role of adaptation in facilitating the ecological success of invasive species in a rapidly changing world.Competing Interest StatementThe authors have declared no competing interest.Footnotes* This manuscript has been revised to improve its framing in order to highlight the motivation, novelty, and significance of the work prior to resubmission to Ecological Monographs. No changes were made to the methodology, analysis, results, or major conclusions of the paper.* https://github.com/ljalbano/transcontinental_common_garden
AbstractList Climate change and the global spread of invasive species are two of the most significant threats to biodiversity. Both of these phenomena subject populations to novel conditions, either in space (species invasion) or in time (climate change), yet the role of adaptation in how populations respond to these rapid environmental shifts is poorly understood. We conducted a large-scale trans-continental common garden experiment using white clover (Trifolium repens, Fabaceae) to test if adaptive evolution to spatiotemporal variation in climate could contribute to the ecological success of one of the most widespread invasive plant species in the world. Individuals from 96 populations of Trifolium repens (white clover) from both its native (Europe) and introduced (North America) ranges were planted into four experimental common gardens located in northern (Uppsala, Sweden) and southern (Montpellier, France) Europe, and northern (Mississauga, Canada) and southern (Louisiana, USA) North America. We recorded plant sexual and clonal fitness in each common garden and assessed whether the strength of local adaptation differed between the native and introduced ranges and whether populations are rapidly adapting to climate change. Results show that local adaptation was only evident when populations were transplanted into common gardens located in the same range (native or introduced) from which they originated and was driven by stronger selection (due to climatic factors rather than herbivory) at lower latitudes in both ranges. Our results indicate that rapid local adaptation across a large latitudinal gradient has occurred in T. repens populations in less than 400 years since its introduction to North America. However, we find evidence of an adaptation lag in the northern common garden in the introduced range, with plants from historically slightly warmer climates exhibiting the greatest fitness. These findings support two major conclusions: 1) white clover can rapidly adapt to spatial variation in climate in its introduced range as well as the native range, and 2) despite rapid adaptation to novel ranges, introduced white clover populations are not keeping pace with rapid climate change. Overall, our results provide insight into the role of adaptation in facilitating the ecological success of invasive species in a rapidly changing world.Competing Interest StatementThe authors have declared no competing interest.Footnotes* This manuscript has been revised to improve its framing in order to highlight the motivation, novelty, and significance of the work prior to resubmission to Ecological Monographs. No changes were made to the methodology, analysis, results, or major conclusions of the paper.* https://github.com/ljalbano/transcontinental_common_garden
Climate change and the global spread of non-native species are two of the most significant threats to biodiversity and ecosystem function. Both these phenomena subject populations to novel conditions, either in space (species introductions) or in time (climate change), yet the role of adaptation in how populations respond to these rapid environmental shifts is poorly understood. We conducted a large-scale trans-continental common garden experiment using white clover (Trifolium repens, Fabaceae) to test whether adaptive evolution to spatiotemporal variation in climate could contribute to the ecological success of one of the most widespread plant species in the world. Individuals from 96 populations of Trifolium repens (white clover) from both its native (Europe) and introduced (North America) ranges were planted into four experimental common gardens located in northern (Uppsala, Sweden) and southern (Montpellier, France) Europe, and northern (Mississauga, Canada) and southern (Lafayette, USA) North America. We recorded plant sexual and clonal fitness in each common garden and assessed whether the strength of local adaptation differed between the native and introduced ranges and whether populations are rapidly adapting to climate change. Results show that local adaptation was only evident when populations were transplanted into common gardens located in the same range (native or introduced) from which they originated and was driven by stronger selection (due to climatic factors rather than herbivory) at lower latitudes in both ranges. Our results indicate rapid local adaptation across a large latitudinal gradient in introduced T. repens populations, along with an associated adaptation cost when transplanted back into the native range. We also find evidence of an adaptation lag in the northern common garden in the introduced range, with plants from historically warmer climates exhibiting the greatest fitness. These findings support two major conclusions: 1) white clover can rapidly adapt to spatial variation in climate in its introduced range as well as the native range, and 2) despite rapid adaptation to novel environments, introduced white clover populations are not keeping pace with rapid climate change. Overall, our results provide insight into the role of adaptation in facilitating the ecological success of non-native species in a rapidly changing world. Data are provided for peer review. All data involved in this study is available on the GitHub page for LJA (https://github.com/ljalbano/transcontinental_common_garden).
Author King, Nevada
Hendrickson, Brandon T
Estarague, Aurélien
Tudoran, Amelia
Puentes, Adriana
Kooyers, Nicholas J
Johnson, Marc Tj
Vasseur, François
Albano, Lucas J
Innes, Simon G
Bastias, Cristina C
Violle, Cyrille
Patterson, Courtney M
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Cites_doi 10.1101/2020.11.01.364349
10.1101/2024.07.09.602765
10.1101/2024.09.03.611023
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Keywords native range
common garden
local adaptation
climatic distance
Adaptation lag
provenance study
white clover
environmental variation
cyanogenesis
introduced range
non-native species
Language English
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Snippet Climate change and the global spread of invasive species are two of the most significant threats to biodiversity. Both of these phenomena subject populations...
Climate change and the global spread of non-native species are two of the most significant threats to biodiversity and ecosystem function. Both these phenomena...
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proquest
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SubjectTerms Adaptation
Biodiversity
Climate change
Evolution & development
Evolutionary Biology
Gardens & gardening
Herbivory
Introduced species
Invasive species
Nonnative species
Spatial variations
Trifolium repens
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Title A transcontinental experiment elucidates (mal)adaptation of a cosmopolitan plant to climate in space and time
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