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Long evolutionary history of an emerging fungal pathogen of diverse tree species in eastern Asia, Australia, and the Pacific Islands
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  • Olga Kozhar,
  • Mee-Sook Kim,
  • Jorge Ibarra Caballero,
  • Ned Klopfenstein,
  • Phil Cannon,
  • Jane Stewart
Olga Kozhar
Colorado State University

Corresponding Author:olga.kozhar@colostate.edu

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Mee-Sook Kim
United States Department of Agriculture Forest Service Pacific Northwest Region
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Jorge Ibarra Caballero
Colorado State University
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Ned Klopfenstein
United States Department of Agriculture Forest Service Rocky Mountain Research Station
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Phil Cannon
United States Department of Agriculture Forest Service Forest Health Protection
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Jane Stewart
Colorado State University
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Abstract

Emerging plant pathogens have been increasing exponentially over the last century. To address this issue, it is critical to determine whether these pathogens are native to ecosystems or have been recently introduced. Understanding the ecological and evolutionary processes fostering emergence can help to manage their spread and predict epidemics/epiphytotics. Using restriction site-associated DNA sequencing data, we studied genetic relationships, pathways of spread, and evolutionary history of Phellinus noxius, an emerging root-rotting fungus of unknown origin, in eastern Asia, Australia, and the Pacific Islands. We analyzed patterns of genetic variation using Bayesian inference, maximum likelihood phylogeny, populations splits and mixtures measuring correlations in allele frequencies and genetic drift, and finally applied coalescent based theory using Approximate Bayesian computation (ABC) with supervised machine learning. Population structure analyses revealed five genetic groups with signatures of complex recent and ancient migration histories. The most probable scenario of ancient pathogen spread is movement from ghost population to Malaysia and the Pacific Islands, with subsequent spread to Taiwan and Australia. Furthermore, ABC analyses indicate that P. noxius spread occurred thousands of generations ago, contradicting previous assumptions that this pathogen was recently introduced to multiple geographic regions. Our results suggest that recent emergence of P. noxius in eastern Asia, Australia, and the Pacific Islands is likely driven by anthropogenic and natural disturbances, such as deforestation, land-use change, severe weather events, and/or introduction of exotic plants. This study provides a novel example of applying genome-wide allele frequency data to unravel dynamics of pathogen emergence under changing ecosystem conditions.
28 Dec 2021Submitted to Molecular Ecology
29 Dec 2021Reviewer(s) Assigned
17 Jan 2022Review(s) Completed, Editorial Evaluation Pending
19 Jan 2022Editorial Decision: Revise Minor
27 Jan 2022Review(s) Completed, Editorial Evaluation Pending
27 Jan 20221st Revision Received
31 Jan 2022Editorial Decision: Accept
Apr 2022Published in Molecular Ecology volume 31 issue 7 on pages 2013-2031. 10.1111/mec.16384