4.5 Article

Convergent molecular evolution among ash species resistant to the emerald ash borer

Journal

NATURE ECOLOGY & EVOLUTION
Volume 4, Issue 8, Pages 1116-+

Publisher

NATURE PORTFOLIO
DOI: 10.1038/s41559-020-1209-3

Keywords

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Funding

  1. QMUL Research-IT
  2. Living with Environmental Change Tree Health and Plant Biosecurity Initiative -Phase 2 - BBSRC [BB/L012162/1]
  3. Living with Environmental Change Tree Health and Plant Biosecurity Initiative -Phase 2 - Defra [BB/L012162/1]
  4. Living with Environmental Change Tree Health and Plant Biosecurity Initiative -Phase 2 - ESRC [BB/L012162/1]
  5. Living with Environmental Change Tree Health and Plant Biosecurity Initiative -Phase 2 - Forestry Commission [BB/L012162/1]
  6. Living with Environmental Change Tree Health and Plant Biosecurity Initiative -Phase 2 - NERC [BB/L012162/1]
  7. Living with Environmental Change Tree Health and Plant Biosecurity Initiative -Phase 2 - Scottish Government [BB/L012162/1]
  8. DEFRA Future Proofing Plant Health scheme
  9. Erica Waltraud Albrecht Endowment Fund
  10. Walsh Scholarship Programme of the Department of Agriculture, Food and the Marine, Ireland
  11. Marie Sklodowska-Curie Individual Fellowship 'FraxiFam' [660003]
  12. BBSRC [BB/L012162/1] Funding Source: UKRI
  13. NERC [NE/K01112X/1] Funding Source: UKRI
  14. Marie Curie Actions (MSCA) [660003] Funding Source: Marie Curie Actions (MSCA)

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Recent studies show that molecular convergence plays an unexpectedly common role in the evolution of convergent phenotypes. We exploited this phenomenon to find candidate loci underlying resistance to the emerald ash borer (EAB, Agrilus planipennis), the United States' most costly invasive forest insect to date, within the pan-genome of ash trees (the genus Fraxinus). We show that EAB-resistant taxa occur within three independent phylogenetic lineages. In genomes from these resistant lineages, we detect 53 genes with evidence of convergent amino acid evolution. Gene-tree reconstruction indicates that, for 48 of these candidates, the convergent amino acids are more likely to have arisen via independent evolution than by another process such as hybridization or incomplete lineage sorting. Seven of the candidate genes have putative roles connected to the phenylpropanoid biosynthesis pathway and 17 relate to herbivore recognition, defence signalling or programmed cell death. Evidence for loss-of-function mutations among these candidates is more frequent in susceptible species than in resistant ones. Our results on evolutionary relationships, variability in resistance, and candidate genes for defence response within the ash genus could inform breeding for EAB resistance, facilitating ecological restoration in areas invaded by this beetle. By assembling the genomes of 22 Fraxinus species and conducting comparisons including further species, the authors identify candidate loci for emerald ash borer resistance that have evolved convergently.

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