Genomic diversification of the specialized parasite of the fungus-growing ant symbiosis


 Fungi shape the diversity of life. Characterizing the evolution of fungi is critical to understanding symbiotic associations across kingdoms. In this study, we investigate the genomic and metabolomic diversity of the genus
 Escovopsis
 , a specialized parasite of fungus-growing ant gardens. Based on 25 high-quality draft genomes, we show that
 Escovopsis
 forms a monophyletic group arising from a mycoparasitic fungal ancestor 61.82 million years ago (Mya). Across the evolutionary history of fungus-growing ants, the dates of origin of most clades of
 Escovopsis
 correspond to the dates of origin of the fungus-growing ants whose gardens they parasitize. We reveal that genome reduction, determined by both genomic sequencing and flow cytometry, is a consistent feature across the genus
 Escovopsis,
 largely occurring in coding regions, specifically in the form of gene loss and reductions in copy numbers of genes. All functional gene categories have reduced copy numbers, but resistance and virulence genes maintain functional diversity. Biosynthetic gene clusters (BGCs) contribute to phylogenetic differences among
 Escovopsis
 spp., and sister taxa in the Hypocreaceae. The phylogenetic patterns of co-diversification among BGCs are similarly exhibited across mass spectrometry analyses of the metabolomes of
 Escovopsis
 and their sister taxa. Taken together, our results indicate that
 Escovopsis
 spp. evolved unique genomic repertoires to specialize on the fungus-growing ant-microbe symbiosis.
