Rapid Host Plant Adaptation via Ectopic Gene Conversion in Plutellid Moths

Abstract

Herbivorous insects face an extraordinary challenge: the chemical defenses of their host plants are highly diverse, rapidly evolving, and largely unpredictable. How insects meet this challenge remains poorly understood. Here we show that ectopic gene conversion (EGC) has repeatedly driven the evolutionary diversification of glucosinolate sulfatases (GSSs), the key larval counteradaptation in plutellid moths to glucosinolate based defenses in cruciferous plants. Across seven plutellid species, enzyme assays with heterologously expressed GSSs and 21 glucosinolates revealed distinct activity profiles: GSSs from species with broad host ranges within glucosinolate-containing plants showed balanced activity across substrates, whereas GSSs from specialists displayed profiles biased toward the glucosinolate composition of their host plants. Comparative genomic analyses identified extensive conversion among duplicated genes, both historically across the clade and in contemporary Plutella armoraciae. In this originally monophagous species, EGC-mediated diversification of GSS enzymes coincides with the rapid inclusion of a new cruciferous host within <200 years, demonstrating the potential of EGC to drive host-range expansion on strikingly short evolutionary timescales. Structural modelling and molecular dynamics simulations further support functional shifts in GSS enzymes arising from EGC-derived sequence alterations. Together, these results demonstrate that EGC provides a powerful mechanism for fine tuning detoxification enzymes, enabling herbivorous insects to adapt to chemically diverse host plants despite constrained enzymatic toolkits.