The interaction of <i>Serratia</i> bacteria and harmonine in harlequin ladybird confers an interspecies competitive edge.

Abstract

The harlequin ladybird, <i>Harmonia axyridis</i>, is a predatory beetle used globally to control pests such as aphids and scale insects. Originating from East Asia, this species has become highly invasive since its introduction in the late 19th century to Europe and North America, posing a threat to local biodiversity. Intraguild predation is hypothesized to drive the success of this invasive species, but the underlying mechanisms remain unknown. In this study, a feeding assay revealed that while harlequin ladybirds survive feeding on seven-spotted ladybird eggs, the reverse is not true. However, seven-spotted ladybirds that had fed on harlequin ladybird eggs were able to survive the feeding assay when treated with penicillin. Microbiome sequencing and whole genome analysis of harlequin ladybird eggs revealed a newly discovered pathogenic bacterium strain named <i>Serratia harmoniae.</i> The median lethal concentration (LC50) of <i>S. harmoniae</i> was found to be 2.1 × 10⁵ times higher in the harlequin ladybird compared to the seven-spotted ladybird. The high tolerance observed in harlequin ladybirds was attributed to harmonine, specifically produced in the fat body of this species. Silencing three key genes in the harmonine biosynthesis pathway-<i>Spidey</i>, <i>Sca2</i>, and <i>Desat-</i>reduced the production of the compound, leading to increased <i>S. harmoniae</i> levels and higher mortality. Treating RNAi-altered individuals with penicillin reversed this effect, successfully reducing <i>S. harmoniae</i> presence and increasing insect survival. Taken together, these findings demonstrate that <i>S. harmoniae</i>, a newly identified pathogenic bacterium carried by harlequin ladybirds, interacts with harmonine to confer an interspecies competitive advantage over native ladybird species in nonnative regions.