TY - JOUR
T1 - Multiple modes of convergent adaptation in the spread of glyphosate-resistant Amaranthus tuberculatus
AU - Kreiner, Julia M.
AU - Giacomini, Darci Ann
AU - Bemm, Felix
AU - Waithaka, Bridgit
AU - Regalado, Julian
AU - Lanz, Christa
AU - Hildebrandt, Julia
AU - Sikkema, Peter H.
AU - Tranel, Patrick J.
AU - Weigel, Detlef
AU - Stinchcombe, John R.
AU - Wright, Stephen I.
N1 - Funding Information:
ACKNOWLEDGMENTS. We thank Tyler Kent and Anna O’Brien for useful discussion; Rebecca Schwab, Fernando Rabanal, and Talia Karasov for comments; and Yunchen Gong for computational support. We also thank and recognize the Ojibwe, Potawatomi, and Odawa peoples of the Walpole Island First Nation. This work was supported by Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grants (S.I.W. and J.R.S.); an NSERC E.W.R. Steacie Memorial Fellowship (S.I.W.); an NSERC Postgraduate Scholarship–Doctoral (J.M.K.); the Department of Ecology and Evolutionary Biology at University of Toronto (J.M.K.); International Max Planck Research School “Molecules to Organisms” (B.W.); Max Planck Society and Ministry of Science, Research and the Arts of Baden-Württemberg in the Regio-Research-Alliance “Yield Stability in Dynamic Environments” (D.W.).
Publisher Copyright:
© 2019 National Academy of Sciences. All rights reserved.
PY - 2019/10/15
Y1 - 2019/10/15
N2 - The selection pressure exerted by herbicides has led to the repeated evolution of herbicide resistance in weeds. The evolution of herbicide resistance on contemporary timescales in turn provides an outstanding opportunity to investigate key questions about the genetics of adaptation, in particular the relative importance of adaptation from new mutations, standing genetic variation, or geographic spread of adaptive alleles through gene flow. Glyphosate-resistant Amaranthus tuberculatus poses one of the most significant threats to crop yields in the Midwestern United States, with both agricultural populations and herbicide resistance only recently emerging in Canada. To understand the evolutionary mechanisms driving the spread of resistance, we sequenced and assembled the A. tuberculatus genome and investigated the origins and population genomics of 163 resequenced glyphosate-resistant and susceptible individuals from Canada and the United States. In Canada, we discovered multiple modes of convergent evolution: in one locality, resistance appears to have evolved through introductions of preadapted US genotypes, while in another, there is evidence for the independent evolution of resistance on genomic backgrounds that are historically nonagricultural. Moreover, resistance on these local, nonagricultural backgrounds appears to have occurred predominantly through the partial sweep of a single haplotype. In contrast, resistant haplotypes arising from the Midwestern United States show multiple amplification haplotypes segregating both between and within populations. Therefore, while the remarkable species-wide diversity of A. tuberculatus has facilitated geographic parallel adaptation of glyphosate resistance, more recently established agricultural populations are limited to adaptation in a more mutation-limited framework.
AB - The selection pressure exerted by herbicides has led to the repeated evolution of herbicide resistance in weeds. The evolution of herbicide resistance on contemporary timescales in turn provides an outstanding opportunity to investigate key questions about the genetics of adaptation, in particular the relative importance of adaptation from new mutations, standing genetic variation, or geographic spread of adaptive alleles through gene flow. Glyphosate-resistant Amaranthus tuberculatus poses one of the most significant threats to crop yields in the Midwestern United States, with both agricultural populations and herbicide resistance only recently emerging in Canada. To understand the evolutionary mechanisms driving the spread of resistance, we sequenced and assembled the A. tuberculatus genome and investigated the origins and population genomics of 163 resequenced glyphosate-resistant and susceptible individuals from Canada and the United States. In Canada, we discovered multiple modes of convergent evolution: in one locality, resistance appears to have evolved through introductions of preadapted US genotypes, while in another, there is evidence for the independent evolution of resistance on genomic backgrounds that are historically nonagricultural. Moreover, resistance on these local, nonagricultural backgrounds appears to have occurred predominantly through the partial sweep of a single haplotype. In contrast, resistant haplotypes arising from the Midwestern United States show multiple amplification haplotypes segregating both between and within populations. Therefore, while the remarkable species-wide diversity of A. tuberculatus has facilitated geographic parallel adaptation of glyphosate resistance, more recently established agricultural populations are limited to adaptation in a more mutation-limited framework.
KW - De novo mutation
KW - Gene flow
KW - Herbicide resistance
KW - Parallel evolution
KW - Population genomics
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U2 - 10.1073/pnas.1900870116
DO - 10.1073/pnas.1900870116
M3 - Article
C2 - 31570613
AN - SCOPUS:85073309830
VL - 116
SP - 21076
EP - 21084
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
SN - 0027-8424
IS - 42
ER -