A switch from constitutive chemical defence to inducible innate immune responses in the invasive ladybird Harmonia axyridis

Abstract

The harlequin ladybird, Harmonia axyridis, has emerged as a model species for invasion biology, reflecting its remarkable capacity to outcompete native ladybird species when introduced into new habitats. This ability may be associated with its prominent resistance to pathogens and intraguild predation. We recently showed that the constitutive antibacterial activity present in the haemolymph of H. axyridis beetles can be attributed to the chemical defence compound harmonine. Here, we demonstrate that H. axyridis differs from other insects, including the native ladybird Coccinella septempunctata, by reducing rather than increasing the antimicrobial activity of its haemolymph following the injection of bacteria. However, both species produce new or more abundant proteins in the haemolymph, indicating that bacterial challenge induces innate immune responses associated with the synthesis of immunity-related proteins. Our results suggest that H. axyridis beetles can switch from constitutive chemical defence to inducible innate immune responses, supporting hypothesis that inducible antimicrobial peptides protect host beetles against pathogens that survive constitutive defences. These alternative antimicrobial defence mechanisms may reflect a trade-off resulting from fitness-related costs associated with the simultaneous synthesis of harmonine and antimicrobial peptides/proteins.

Behavioral and Immunological Features Promoting the Invasive Performance of the Harlequin Ladybird Harmonia axyridis

“…The harmonine concentration in the hemolymph increases during development, reaching 27 mM in adult beetles (Schmidtberg et al, 2013). Interestingly, harmonine is active against a broad spectrum of bacteria, particularly against mycobacteria.…”

Transcriptomic insight into the immune defenses in the ghost moth, Hepialus xiaojinensis, during an Ophiocordyceps sinensis fungal infection

“…Recent advances in molecular genetics technologies, as well as high-throughput sequencing have provided in-depth insights into the immune systems of many insects, including the Hymenopteran bee, Apis mellifera (Evans et al, 2006); three Dipteran insects, Drosophila melanogaster , Anopheles gambiae (Christophides et al, 2002), and Aedes aegypti (Waterhouse et al, 2007); three Coleopteran beetles, Tribolium castaneum (Zou et al, 2007), Harmonia axyridis (Schmidtberg et al, 2013), and Meligethes aeneus (Vogel et al, 2014); and three Lepidopteran moths, Bombyx mori (Tanaka et al, 2008), Manduca sexta (Gunaratna and Jiang, 2013), and Ostrinia furnacalis (Liu et al, 2014). Immunity-related genes have enabled the identification of orthologues in these insect species; the expansion and loss of genes and gene families may reflect natural selection, enabling adaptation to ecological and physiological conditions.…”

RNA‐sequencing analysis reveals abundant developmental stage‐specific and immunity‐related genes in the pollen beetle Meligethes aeneus

“…Next‐generation sequencing has been used to investigate the immunity‐related transcriptome of the invasive ladybird Harmonia axyridis , revealing the most diverse spectrum of antimicrobial peptides (AMPs) and proteins reported thus far for any animal species. The remarkable expansion of the H. axyridis AMP repertoire may have promoted its invasive success (Schmidtberg et al ., ; Vilcinskas et al ., 2013a,b). Most beetles feed solely on plants, but with the notable exception of the mountain pine beetle (Keeling et al ., ) we lack insight into the adaptive mechanisms of strictly phytophagous beetles that are highly adapted to both the nutrients and the defensive chemicals produced by their host plants.…”