Antennal Transcriptome Analysis and Identification of Candidate Chemosensory Genes of the Harlequin Ladybird Beetle, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae).

Nicolas Montagné,Eric Conti,Alessandro Roman,Emmanuelle Jacquin-Joly,Gabriele Rondoni,Camille Meslin

doi:10.3390/insects12030209

Abstract

Simple SummaryThe predatory harlequin ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) has been widely released for classical and augmentative biological control programs of insect herbivores and is now distributed worldwide. Because of its invasive behavior and the threat it can pose to local biodiversity, this ladybird has been adopted as a model species for invasive biocontrol predators. A huge amount of existing literature is available on this species. However, little is known about the mechanisms underlying H. axyridis smell and taste, even though these senses are important in this ladybird for courtship, mating, and for locating suitable habitats for feeding and oviposition. Here we describe the first chemosensory gene repertoire that is expressed in the antennae of male and female H. axyridis. Our findings would likely represent the basis for future functional studies aiming at increasing the efficacy of H. axyridis in biological control or at reducing its populations in those areas where the ladybird has become a matter of concern due to its invasiveness.In predatory ladybirds (Coleoptera: Coccinellidae), antennae are important for chemosensory reception used during food and mate location, and for finding a suitable oviposition habitat. Based on NextSeq 550 Illumina sequencing, we assembled the antennal transcriptome of mated Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) males and females and described the first chemosensory gene repertoire expressed in this species. We annotated candidate chemosensory sequences encoding 26 odorant receptors (including the coreceptor, Orco), 17 gustatory receptors, 27 ionotropic receptors, 31 odorant-binding proteins, 12 chemosensory proteins, and 4 sensory neuron membrane proteins. Maximum-likelihood phylogenetic analyses allowed to assign candidate H. axyridis chemosensory genes to previously described groups in each of these families. Differential expression analysis between males and females revealed low variability between sexes, possibly reflecting the known absence of relevant sexual dimorphism in the structure of the antennae and in the distribution and abundance of the sensilla. However, we revealed significant differences in expression of three chemosensory genes, namely two male-biased odorant-binding proteins and one male-biased odorant receptor, suggesting their possible involvement in pheromone detection. Our data pave the way for improving the understanding of the molecular basis of chemosensory reception in Coccinellidae.

Highlights

Chemosensory reception is important in insects, including predacious ladybirds (Coleoptera: Coccinellidae), for food and mate location and for finding a suitable oviposition habitat [1,2,3]
Bioinformatics analyses identified a total of 117 unigenes from H. axyridis
It is known from previous studies that H. axyridis males and females respond differently to odors in wind tunnel [89] or electroantennography [90]

Summary

Introduction

Chemosensory reception is important in insects, including predacious ladybirds (Coleoptera: Coccinellidae), for food and mate location and for finding a suitable oviposition habitat [1,2,3]. Volatile molecules are typically detected by insects through neurons housed in chemosensory sensilla mainly located on the antennae. In these organs, the chemical stimuli are transformed into electrical signals that will be transmitted to the brain [4]. In the proposed process of odorant detection, molecules are first bound and transported by odorant-binding proteins (OBPs) and possibly chemosensory proteins (CSPs) within the sensillum lymph, detected by odorant receptors (ORs) or/and ionotropic receptors (IRs) expressed at the membrane of olfactory sensory neurons. Other protein families are involved, such as the sensory neuron membrane proteins (SNMPs) for pheromone detection in some species [4,5]. The function and characteristics of all these gene families in insects have been extensively reviewed, especially in model species such as Drosophila melanogaster (Meigen) [4,7,8,9,10]

Methods

Results

Conclusion