Population genomics revealed cryptic species within host-specific zombie-ant fungi (Ophiocordyceps unilateralis)
Abstract
The identification and delimitation of species boundaries are essential for understanding speciation
and adaptation processes and for the management of biodiversity as well as development for
applications. Ophiocordyceps unilateralis sensu lato is a complex of fungal pathogens parasitizing
Formicine ants, inducing zombie behaviors in their hosts. Previous taxonomic works with limited
numbers of samples and markers led to the “one ant-one fungus” paradigm, resulting in the use of
ant species as a proxy for fungal identification. Here, a population genomic study with sampling on
three ant species across Thailand supported the existence of host-specific species in O. unilateralis
s.l. with no footprints of long term introgression despite occasional host shifts and first-generation
hybrids. We further detected genetic clusters within the previously delimited fungal species, with
each little footprints of recombination, suggesting high levels of inbreeding. The clusters within
each of O. camponoti-leonardi and O. camponoti-saundersi were supported by differentiation
throughout the genome, suggesting they may constitute further cryptic species parasitizing the same
host, challenging the one ant-one fungus paradigm. These genetic clusters had different
geographical ranges, supporting different biogeographic influences between the north/center and the
south of Thailand, reinforcing the scenario in which Thailand endured compartmentation during the
latest Pleistocene glacial cycles.
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