SummaryCrop disease outbreaks are often associated with clonal expansions of single pathogenic lineages. To determine 20 whether similar boom-and-bust scenarios hold for wild plant pathogens, we carried out a multi-year multi-site 21 survey of Pseudomonas in the natural host Arabidopsis thaliana. The most common Pseudomonas lineage 22 corresponded to a pathogenic clade present in all sites. Sequencing of 1,524 Pseudomonas genomes revealed 23 this lineage to have diversified approximately 300,000 years ago, containing dozens of genetically distinct 24 pathogenic sublineages. These sublineages have expanded in parallel within the same populations and are 25 differentiated both at the level of gene content and disease phenotype. Such coexistence of diverse sublineages 26indicates that in contrast to crop systems, no single strain has been able to overtake these A. thaliana 27 populations in the recent past. Our results suggest that the selective pressures acting on a plant pathogen in 28 wild hosts may be more complex than those in agricultural systems. 29
Introduction
30In agricultural and clinical settings, pathogenic colonizations are frequently associated with expansions of single 31 or a few genetically identical microbial lineages (Butler et al., 2013; Cai et al., 2011;Kolmer, 2005; Park et al., 32 2015;Stukenbrock and McDonald, 2008; Yoshida et al., 2013). The conditions that lead to such epidemics-such 33 as reduced host genetic diversity (Zhu et al., 2000), absence of competing microbial communities (Brown et al., 34 2013) or high transmission rates (Park et al., 2015)-are, however, by no means a universal feature of 35 pathogenic infections. Instead, many, if not most, pathogens can colonize host populations that are both 36 genetically diverse and that can accommodate a diversity of other microbes (Barrett et al., 2009; Falkinham et 37 al., 2015;Woolhouse et al., 2001). 38Factors that drive pathogen success in such more complex situations are less well understood than for 39 clonal epidemics. For example, if a pathogen species persists at high numbers in non-host environments, does 40 each host become infected by a different pathogen strain? Or does a multitude of genetically distinct pathogens 41 infect each host? And do different colonizing strains use disparate mechanisms to become established even 42 within genetically similar host individuals? The answers to these questions inform on how (and if) a host 43 population can evolve partial or even complete pathogen resistance (Anderson and May, 1982; Barrett et al., 44 2009; Karasov et al., 2014a;Laine et al., 2011). Several studies over the past 20 years have attempted to infer 45 the distributions of non-epidemic pathogens in both host and non-host environments (Falkinham et al., 2015; 46 Wiehlmann et al., 2007). These studies, which have observed a range of different patterns, are unfortunately 47 often limited to the historic strains that are available, and the conclusions vary for different collections, even of 48 the same pathogen ...