The genetic and transcriptional basis of variation in fungal entomopathogen susceptibility

Abstract

Herbivorous insects pose a major threat to global crop production, and there is growing need for biological alternatives to chemical control. Entomopathogenic fungi are a possible candidate, yet how susceptibility varies, what drives it, and whether it is consistent across environments remain poorly understood — questions crucial to their long-term viability as biocontrol agents. This thesis investigates variation in susceptibility to entomopathogenic fungi in Helicoverpa armigera, a globally significant crop pest with a history of resistance evolution. We asked whether heritable variation in susceptibility existed across outbred families; whether resistance or tolerance better explained survival differences; whether transcriptional differences were constitutive or induced; and whether susceptibility loci were consistent across pathogen species and host-plant diets. Survival varied substantially across larval families challenged with Beauveria bassiana, consistent with a genetic basis to susceptibility differences. Results were most consistent with resistance as the dominant mechanism — pathogen load declined between days two and six post-exposure, and family mortality correlated positively with fungal burden, with limited evidence for tolerance. Larval weight was the strongest predictor of pathogen load, with the lightest larvae carrying 12–20-fold more fungal DNA than the heaviest. Transcriptomic analysis identified 145 differentially expressed genes between susceptibility extremes, of which 85% reflected constitutive differences; induced immune responses were detectable only in the most susceptible families. Susceptible families constitutively expressed higher levels of a predicted immune down-regulator (PGRP-LB) and trypsin-like serine proteases. A genome-wide association study revealed susceptibility to B. bassiana and Metarhizium anisopliae was highly polygenic, with 5–107 QTLs across four pathogen–diet combinations and minimal overlap between treatments. Together, these findings reveal that resistance to entomopathogenic fungi in H. armigera is polygenic, context-dependent, and architecturally complex. This underscores the importance of understanding the genetic and environmental context of host-pathogen interactions when evaluating the long-term prospects of fungal biopesticides as biocontrol agents.