First molecular evidence of lichen-inhabiting Acrospermum and new insights into the evolution of lifestyles of Acrospermales (Dothideomycetes).

Abstract

Acrospermales represent one of the least studied lineages of Dothideomycetes and are characterized by diverse ecological strategies, including saprotrophic, epiphytic, fungicolous, lichenicolous, and bryophilous lifestyles. The order is composed of two teleomorphic genera, Acrospermum and Oomyces, and five anamorphic genera of unclear relationships. The objectives of the study were to establish the phylogenetic position of Acrospermum species collected from lichens in the tropical forest of Bolivia and to infer the evolution of the lichenicolous lifestyle in Acrospermales. Our results reveal that the examined specimens from Bolivia represent a new species, A. bolivianum, which is well characterized by its phylogenetic distinctness, morphological characteristics, and host selection. The new species is the first lichenicolous member of Acrospermum and forms a well-supported clade sister to the bryophilous Acrospermum adeanum. The evolution of lifestyles, concluded by phylogenetic analyses and ancestral state reconstructions, indicated that the saprotrophic lifestyle is ancestral to Acrospermales. This corresponds to their close relationship to other saprotrophic lineages of Dothideomycetes and indicates that the wide spectrum of nutritional strategies, currently observed in Acrospermales, may be a result of more recent shifts in their ecology. Our results also suggest that the lichenicolous lifestyle in Acrospermales appeared independently at least two times. Lichenicolous species are represented in our data set by Acrospermum bolivianum and Gonatophragmium physciae, which evolved from lichenicolous and plant-parasite ancestors, respectively. The genus Oomyces, represented by O. carneoalbus, was included for the first time in the phylogenetic analysis and showed a sister relationship to the remaining taxa of Acrospermales.