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Large haploblocks underlie rapid adaptation in an invasive weed

View ORCID ProfilePaul Battlay, Jonathan Wilson, View ORCID ProfileVanessa C. Bieker, Christopher Lee, Diana Prapas, Bent Petersen, Sam Craig, View ORCID ProfileLotte van Boheemen, Romain Scalone, Nissanka P. de Silva, Amit Sharma, Bojan Konstantinović, Kristin A. Nurkowski, View ORCID ProfileLoren H. Rieseberg, View ORCID ProfileTim Connallon, View ORCID ProfileMichael D. Martin, Kathryn A. Hodgins
doi: https://doi.org/10.1101/2022.03.02.482376
Paul Battlay
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
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  • For correspondence: pbattlay@gmail.com
Jonathan Wilson
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
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Vanessa C. Bieker
2Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology (NTNU), Trondheim, Norway
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Christopher Lee
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
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Diana Prapas
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
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Bent Petersen
3Center for Evolutionary Hologenomics, GLOBE Institute, University of Copenhagen, Denmark
4Centre of Excellence for Omics-Driven Computational Biodiscovery (COMBio), AIMST University, 08100 Kedah, Malaysia
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Sam Craig
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
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Lotte van Boheemen
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
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Romain Scalone
5Department of Crop Production Ecology, Uppsala Ecology Center, Swedish University of Agricultural Sciences, Uppsala, Sweden
6Department of Grapevine Breeding, Hochschule Geisenheim University, Geisenheim, Germany
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Nissanka P. de Silva
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
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Amit Sharma
7Cell, Molecular Biology and Genomics Group, Department of Biology, Norwegian University of Science and Technology (NTNU), Trondheim, Norway
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Bojan Konstantinović
8Department of Environmental and Plant Protection, University of Novi Sad, Novi Sad, Serbia
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Kristin A. Nurkowski
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
9Department of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, Canada
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Loren H. Rieseberg
9Department of Botany and Biodiversity Research Centre, University of British Columbia, Vancouver, Canada
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Tim Connallon
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
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Michael D. Martin
2Department of Natural History, NTNU University Museum, Norwegian University of Science and Technology (NTNU), Trondheim, Norway
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Kathryn A. Hodgins
1School of Biological Sciences, Monash University, Melbourne, Victoria, Australia
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ABSTRACT

Adaptation is the central feature and leading explanation for the evolutionary diversification of life. Adaptation is also notoriously difficult to study in nature, owing to its complexity and logistically prohibitive timescale. We leverage extensive contemporary and historical collections of Ambrosia artemisiifolia—an aggressively invasive weed and primary cause of pollen-induced hayfever—to track the phenotypic and genetic causes of recent local adaptation across its native and invasive ranges in North America and Europe, respectively. Large haploblocks— indicative of chromosomal inversions—contain a disproportionate share (26%) of genomic regions conferring parallel adaptation to local climates between ranges, are associated with rapidly adapting traits, and exhibit dramatic frequency shifts over space and time. These results highlight the importance of large-effect standing variants in rapid adaptation, which have been critical to A. artemisiifolia’s global spread across vast climatic gradients.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵These authors jointly supervised this work: Kathryn A. Hodgins, Michael D. Martin

  • Assembled a new chromosome-level phased diploid Ambrosia artemisiifolia reference genome. Repeated all population-genomic analyses with samples aligned to one haplotype of this new reference. Identified eight additional haploblocks. Used an alignment of the two haplotypes in our diploid assembly to validate four haploblocks segregating in the reference. Added Fay & Wu's H scans for each modern population in historic-modern population pairs to support selective sweep analyses in these populations.

  • https://www.dropbox.com/s/98qy9bokn28z1vh/ragweed-natcomms-suptables.xlsx?dl=0

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted January 31, 2023.
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Large haploblocks underlie rapid adaptation in an invasive weed
Paul Battlay, Jonathan Wilson, Vanessa C. Bieker, Christopher Lee, Diana Prapas, Bent Petersen, Sam Craig, Lotte van Boheemen, Romain Scalone, Nissanka P. de Silva, Amit Sharma, Bojan Konstantinović, Kristin A. Nurkowski, Loren H. Rieseberg, Tim Connallon, Michael D. Martin, Kathryn A. Hodgins
bioRxiv 2022.03.02.482376; doi: https://doi.org/10.1101/2022.03.02.482376
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Large haploblocks underlie rapid adaptation in an invasive weed
Paul Battlay, Jonathan Wilson, Vanessa C. Bieker, Christopher Lee, Diana Prapas, Bent Petersen, Sam Craig, Lotte van Boheemen, Romain Scalone, Nissanka P. de Silva, Amit Sharma, Bojan Konstantinović, Kristin A. Nurkowski, Loren H. Rieseberg, Tim Connallon, Michael D. Martin, Kathryn A. Hodgins
bioRxiv 2022.03.02.482376; doi: https://doi.org/10.1101/2022.03.02.482376

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