A new family of ant-associated fungi in Chaetothyriales

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The order Chaetothyriales comprises the black yeasts and relatives, of which numerous species are prevalent as opportunists on human hosts. The present paper introduces a clade of species that live in ant nests inside hollow structures of tropical plants (so-called domatia) and their closest relatives. To clarify the evolutionary trajectory of the domatia-associated clade, molecular, morphological, and physiological data were analysed. The position of the domatia clade within the Chaetothyriales was assessed by phylogenetic analysis of ITS and LSU. Species delimitations were calculated and genealogical concordance performed with a dataset including the gene of the ribosomal operon, β-tubulin (BT2) and RNA polymerase II largest subunit (RBP1). Genome sequencing allowed additional analysis of mating types, mitochondrial genomes, and estimation of a species tree based on the proteins of 770 single copy orthologous genes. A new family with two new genera in Chaetothyriales was introduced to accommodate the taxa from ant-inhabited domatia and a related clade of plant- and rock-colonizing species. The family is monophyletic and has strong statistical support. Although species delimitation criteria suggested the separation of more than 10 species in the domatia-clade, genealogical concordance of ribosomal and housekeeping gene markers indicated genetic exchange. Seven new species were delineated, with species also being characterized by phenotypic features of fungal colony morphology, micromorphology, physiology and ecology. However, intra-specific variability remained exceptionally large and did not always match with ecological and geographic data. It is hypothesized that the high degrees of intra- and interspecific variability of some of the clades acknowledged as separate species might be related to extended periods of molecular evolution. The newly described species seem to have their preferred habitat in tropical ant nests, and they have adapted to this specific environment. Ant-domatia provide a remarkable habitat rich in volatile chemicals, which could be tolerated by the fungi under study. The family is distantly related to the family Herpotrichiellaceae comprising numerous human-opportunistic species, where hydrocarbon tolerance has been hypothesized to play a role in black yeast evolution.