Within the landscape of globally distributed pathogens, populations differentiate via both adaptive and non-adaptive forces. Individual populations are likely to show unique trends of genetic diversity, host-pathogen interaction, and ecological adaptation. In plant pathogens, allopatric divergence may occur particularly rapidly within simplified agricultural monoculture landscapes. As such, the study of plant pathogen populations in monocultures can highlight the distinct evolutionary mechanisms that lead to local genetic differentiation. Xylella fastidiosa is a plant pathogen known to infect and damage multiple monocultures worldwide. One subspecies, Xylella fastidiosa subsp. fastidiosa was first introduced to the USA ∼150 years ago, where it was found to infect and cause disease in grapevines (Pierce’s disease of grapevines, PD). Here, we studied PD-causing subsp. fastidiosa populations, with an emphasis on those found in the USA. Our study shows that following its establishment in the USA, PD-causing strains likely split into populations in the East and West Coast. This diversification has occurred via both changes in gene content (gene gain/loss events) and variations in nucleotide sequence (mutation and recombination). In addition, we reinforce the notion that PD-causing populations within the USA acted as the source for subsequent subsp. fastidiosa outbreaks in Europe and Asia.
IMPORTANCE Compared to natural environments, the reduced diversity of monoculture agricultural landscapes can lead bacterial plant pathogens to quickly adapt to local biological and ecological conditions. Because of this, accidental introductions of microbial pathogens into naïve regions represents a significant economic and environmental threat. Xylella fastidiosa is a plant pathogen with an expanding host and geographic range due to multiple intra- and inter-continental introductions. X. fastidiosa subsp. fastidiosa, infects and causes disease in grapevines (Pierce’s disease of grapevines; PD). This study focused on PD-causing X. fastidiosa populations, particularly those found in the USA but also invasions into Taiwan and Spain. The analysis shows that PD-causing X. fastidiosa has diversified via multiple co-occurring evolutionary forces acting at an intra- and inter-population level. This analysis enables a better understating of the mechanisms leading to the local adaptation of X. fastidiosa, and how a plant pathogen diverges allopatrically after multiple and sequential introduction events.