Fungal pathogen promotes caterpillar feeding and weight gain using a host-like trehalase

Parasite-mediated extended phenotypes in hosts are of particular interest in biology. However, few parasite genes have been characterized for their selfish role in altering host behaviors to benefit parasite transmission or reproduction. The entomopathogenic fungus Cordyceps militaris infects caterpillar larvae without killing them until after pupation. Here, we report that fungal infection of silkworm larvae induces increased feeding and weight gain, which is manifested by starvation-like responses, including the constant upregulation of the orexigenic peptide HemaP and a sharp reduction in hemolymph trehalose levels. Engineered fungal strains overexpressing HemaP further enhance silkworms' excessive feeding and weight gain. Disruption of HemaP in silkworms reduced trehalose production and pupal weight, thereby decreasing fungal fruiting body formation on mutant pupae. Consistent with the depletion of blood sugars, an insect-like trehalase gene was upregulated in fungal cells growing within insect body cavities, and deleting this gene in C. militaris abolished fungal ability to promote weight gain in silkworms after infection. Our data shed light on a previously unsuspected extended phenotype: fungal promotion of insect feeding through the function of a host-like gene, ultimately benefiting fungal reproduction.