Population-specific expression of antimicrobial peptides conferring pathogen resistance in the invasive ladybird Harmonia axyridis

Tobias Gegner,Andreas Vilcinskas,Heiko Vogel,Henrike Schmidtberg

doi:10.1038/s41598-018-21781-4

Abstract

The harlequin ladybird Harmonia axyridis has emerged as a model species in the context of invasion biology and possesses an expanded repertoire of antimicrobial peptides (AMPs). Here we measured the expression of 22 AMP genes in adult beetles from native and introduced populations, and from a biocontrol population, allowing us to compare populations differing in terms of invasive performance. Strikingly, we observed population-specific expression profiles for particular AMPs. Following an immune challenge, the genes for Coleoptericin1 (Col1), Coleoptericin-likeB and Defensin1 were induced up to several thousand times more strongly in the invasive populations compared to the native and biocontrol populations. To determine the role of Col1 in pathogen resistance, the corresponding gene was silenced by RNA interference (RNAi), causing higher mortality in beetles subsequently infected with the entomopathogen Pseudomonas entomophila. The RNAi-triggered susceptibility to this pathogen was reversed by the injection of a synthetic Col1 peptide. We show that a native population is more susceptible to P. entomomophila infection than an invasive population. This is the first study demonstrating population-specific differences in the immune system of an invasive species and suggests that rapid gene expression changes and a highly adaptive immune system could promote pathogen resistance and thereby invasive performance.

Highlights

Harmonia axyridis, known as the harlequin ladybird, multicoloured ladybird or Asian ladybird beetle, has emerged as a powerful model species for studies of biological invasions[1]
A recent comparative analysis of the immunity-related transcriptomes of three ladybird beetles revealed an expansion in the number of antimicrobial peptides (AMPs) in the invasive ladybird H. axyridis compared to the native ladybirds C. septempunctata and A. bipunctata[15]
The gradient of AMP diversity and induction ratio from A. bipunctata to H. axyridis corresponds to a gradient of increasing resistance against microsporidia and the entomopathogenic fungus B. bassiana[15,16,17,18]

Summary

Introduction

Known as the harlequin ladybird, multicoloured ladybird or Asian ladybird beetle, has emerged as a powerful model species for studies of biological invasions[1]. Another study has shown that the laboratory mass-rearing of a European population used for biocontrol has resulted in the selection of mutations that are not prevalent in native or invasive beetles, including mutations that increase susceptibility to the entomopathogenic fungus Beauveria bassiana[4]. Our comparative analysis using untreated and immune-induced beetles revealed that specific genes, especially Col[1], are induced by a bacterial challenge much more strongly in invasive populations than in native or biocontrol populations, suggesting a role in survival after pathogen exposure. To investigate the role of Col[1] in pathogen resistance, we silenced its expression by RNA interference (RNAi) and compared the mortality of RNAi-treated and untreated beetles infected with the bacterial entomopathogen Pseudomonas entomophila. The comparative analysis of populations differing in their invasive characteristics should facilitate the identification of features that are responsible for invasive success

Methods

Results

Conclusion