Long evolutionary history of an emerging fungal pathogen of diverse tree species in eastern Asia, Australia, and the Pacific Islands

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 an unsampled population
to Malaysia and the Pacific Islands, with subsequent spread to Taiwan and
Australia. Furthermore, ABC analyses indicate 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. noxiusin 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.