Coevolution by common descent of fungal symbionts (Epichloe spp.) and grass hosts

Abstract

Epichloe species are ascomycetous fungi (family Clavicipitaceae) that are ecologically obligate symbionts of grasses. Because they can enhance host fitness by protection from biotic and abiotic stresses, but can aim reduce host seed production, these symbionts span a continuum from antagonistic (highly pathogenic) to mutualistic. Their mutualistic or antagonistic effects are directly related to the relative importance of their sexual and asexual life cycles. The sexual cycle of the fungus occurs only on 'choked' tillers on which no seeds are produced, so the more antagonistic Epichloe species permit almost no host seed production and only transmit horizontally (contagiously). Other Epichloe species are called 'pleiotropic symbionts' because they have both mutualistic and antagonistic effects, being transmitted both vertically (in host seeds) and horizontally. The possibility of coevolution by common descent of Epichloe and grass species was addressed by surveying grasses for pleiotropic or antagonistic symbionts, identifying the biological species of Epichloe associated with each host, conducting molecular phylogenetic analysis of the symbionts based on noncoding portions of nuclear genes for β-tubulin and rRNA, and comparing gene trees with each other and with the established molecular phylogeny of the host tribes. A total of nine confirmed or likely biological species of Epichloe were identified, eight of which were specialized to groups of related host species or genera within a single tribe. Five of the Epichloe species were pleiotropic whereas the other four species were antagonistic. Phylogenetic analysis indicated that the five pleiotropic species and two of the four antagonistic species coevolved by common descent with their hosts. Of the two species for which common descent was not evident, one had a broad host range and was paraphyletic to a pleiotropic species, and the other had discordant gene phylogenies suggestive of a hybrid origin. These results suggested that common descent is more likely in pleotropic than in antagonistic symbioses of grasses with these fungi.