Adaptation During the Shift from Entomopathogen to Endosymbiont Is Accompanied by Gene Loss and Intensified Selection

Fungi have been found to be associated with many insect species, with some species transitioning to reside within insects as symbionts. However, the evolutionary pressures and genomic consequences associated with this transition are not well understood. Pathogenic fungi of the genus Ophiocordyceps have undergone multiple, independent transitions from pathogen to endosymbiont lifestyles, where they reside within the fatty tissues of infected soft-scale insects transgenerationally without killing their hosts. To gain an understanding of the genomic adaptations underlying this life history shift, long-read sequencing was utilized to assemble the genomes of both the soft-scale insect Parthenolecanium corni and its Ophiocordyceps endosymbiont from a single insect. Assembly and metagenomic-based binning produced a highly contiguous genome for Pa. corni and a chromosome-level assembly for the Ophiocordyceps endosymbiont. The endosymbiont genome was characterized by 524 gene loss events compared to free-living pathogenic Ophiocordyceps relatives, with predicted roles in hyphal growth, cell wall integrity, metabolism, gene regulation, and toxin production. Contrasting patterns of selection were observed between the nuclear and mitochondrial genomes specific to the endosymbiont lineage. Intensified selection was most frequently observed across orthologs in the nuclear genome, whereas selection on most mitochondrial genes was found to be relaxed. Scans for positive selection were enriched within the fatty acid metabolism pathway with endosymbiont specific selection within three adjacent enzymes catalyzing the conversion of acetoacetate to acetyl-coenzyme A, suggesting that the endosymbiont lineage is under selective pressure to effectively exploit the lipid rich environment of the insect fat bodies in which it is found.