SRA

Obligate parasites are under strong selection to increase exploitation of their host to survive while evading detection by host immune defenses. This has often led to extreme host specificity and elaborate pathogen adaptations that hinder 'host-jumps' to novel host species, which nevertheless are rampant and an important driver of evolutionary diversification among pathogenic fungi. Here we investigate host adaptation in two morphologically indistinguishable closely related obligate specialist insect pathogenic fungi, Entomophthora muscae s. s. and E. muscae s. l., pathogens of houseflies (Musca domestica) and cabbage flies (Delia radicum), respectively. RNAseq reveal intra-isolate polymorphisms that indicate the multinucleate E. muscae hyphal bodies and spores contain diploid nuclei, which previously have been considered to be haploid. Analysis of within and between species single nucleotide polymorphisms (dN/dS ratios) revealed molecular signatures of positive selection in transcripts related to utilization of host lipids and potentially the secretion of host specific toxins. Comparison with the related non-obligate entomopathogenic Conidiobolus coronatus revealed the evolutionary transition to obligate insect pathogenicity in E. muscae was associated with a gene-family expansion of trehalase enzymes for efficient trehalose utilization, the main sugar in insect hemolymph. These results are in concordance with evolution of host adaptation in this system being governed by mechanisms of host tissue utilization instead of enzymatic virulence factors mediating host cuticle penetration. This implies that past and potential future entomophthoralean host-jumps to novel insect species not being restricted by the capacity for initial cuticle penetration, but by nutrient utilization and proliferation within the novel host.