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

Abstract

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 <i>Escovopsis</i>, a specialized parasite of fungus-growing ant gardens. Based on 25 high-quality draft genomes, we show that <i>Escovopsis</i> 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 <i>Escovopsis</i> 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 <i>Escovopsis,</i> 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 <i>Escovopsis</i> 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 <i>Escovopsis</i> and their sister taxa. Taken together, our results indicate that <i>Escovopsis</i> spp. evolved unique genomic repertoires to specialize on the fungus-growing ant-microbe symbiosis.