Colletotrichum gloeosporioides s.l. in North America: sex, host, and habitat-mediated diversity in a plant-associated ascomycetes

Determining the factors that drive the evolution of pathogenic fungi is central to revealing the mechanisms of virulence and host preference, as well as developing effective disease control measures. Prerequisite to these pursuits is the accurate delimitation of species boundaries. Colletotrichum gloeosporioides s.l. is a species complex of plant pathogens and endophytic fungi for which reliable species recognition has only recently become possible through a multi-locus phylogenetic approach. Through intensive regional sampling that encompasses multiple hosts within and beyond agricultural zones associated with cranberry (Vaccinium macrocarpon Aiton), we have integrated North American strains of Colletotrichum gloeosporioides s.l. from these habitats into a broader phylogenetic framework and characterized some of the factors that influence species diversity. We have developed polymorphic microsatellite markers for C. fructivorum, a species determined to be responsible for cranberry fruit-rot in agricultural areas throughout North America, in order to understand the biotic and abiotic factors that shape populations within the species complex. These markers amplify across several species within the C. gloeosporioides species complex and some are variable within two species, C. rhexiae and C. kahawae, that are closely related to C. fructivorum. Broad geographical and fine-scale hierarchical sampling of C. fructivorum and C. rhexiae coupled with multilocus genotyping has allowed us to gain insight into the forces that shape populations of these species. Human-mediated dispersal is an important factor dissipating the population structure of C. fructivorum throughout its range in commercial cranberry bogs. In contrast, limited evidence suggests C. rhexiae is geographically structured within a more restricted range, implying distinct patterns of diversity between Colletotrichum species associated with wild versus agricultural hosts. We also investigate the reproductive mode of C. fructivorum using estimates of haploid disequilibrium and genotypic diversity, inferring a mixed (sexual and asexual) mode of reproduction in field populations. We discuss the importance of sexual and asexual reproduction on population dynamics and speciation within the C. gloeosporioides species complex.