Multiple modes of convergent adaptation in the spread of glyphosate-resistant Amaranthus tuberculatus

Julia M. Kreiner, Darci Ann Giacomini, Felix Bemm, Bridgit Waithaka, Julian Regalado, Christa Lanz, Julia Hildebrandt, Peter H. Sikkema, Patrick J. Tranel, Detlef Weigel, John R. Stinchcombe, Stephen I. Wright

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
Pages (from-to)21076-21084
Number of pages9
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number42
DOIs
StatePublished - Oct 15 2019

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Keywords

  • De novo mutation
  • Gene flow
  • Herbicide resistance
  • Parallel evolution
  • Population genomics

ASJC Scopus subject areas

  • General

Cite this

Kreiner, J. M., Giacomini, D. A., Bemm, F., Waithaka, B., Regalado, J., Lanz, C., Hildebrandt, J., Sikkema, P. H., Tranel, P. J., Weigel, D., Stinchcombe, J. R., & Wright, S. I. (2019). Multiple modes of convergent adaptation in the spread of glyphosate-resistant Amaranthus tuberculatus. Proceedings of the National Academy of Sciences of the United States of America, 116(42), 21076-21084. https://doi.org/10.1073/pnas.1900870116