The oldest fossil evidence of animal parasitism by fungi supports a Cretaceous diversification of fungal–arthropod symbioses

Abstract

Paleoophiocordyceps coccophagus, a fungal parasite of a scale insect from the Early Cretaceous (Upper Albian), is reported and described here. This fossil not only provides the oldest fossil evidence of animal parasitism by fungi but also contains morphological features similar to asexual states of Hirsutella and Hymenostilbe of the extant genus Ophiocordyceps (Ophiocordycipitaceae, Hypocreales, Sordariomycetes, Pezizomycotina, Ascomycota). Because species of Hypocreales collectively exhibit a broad range of nutritional modes and symbioses involving plants, animals and other fungi, we conducted ancestral host reconstruction coupled with phylogenetic dating analyses calibrated with P. coccophagus. These results support a plant-based ancestral nutritional mode for Hypocreales, which then diversified ecologically through a dynamic process of intra- and interkingdom host shifts involving fungal, higher plant and animal hosts. This is especially evident in the families Cordycipitaceae, Clavicipitaceae and Ophiocordycipitaceae, which are characterized by a high occurrence of insect pathogens. The ancestral ecologies of Clavicipitaceae and Ophiocordycipitaceae are inferred to be animal pathogens, a trait inherited from a common ancestor, whereas the ancestral host affiliation of Cordycipitaceae was not resolved. Phylogenetic dating supports both a Jurassic origin of fungal–animal symbioses within Hypocreales and parallel diversification of all three insect pathogenic families during the Cretaceous, concurrent with the diversification of insects and angiosperms.