Comparative morphological and transcriptomic analyses reveal chemosensory genes in the poultry red mite, Dermanyssus gallinae

Biswajit Bhowmick,Fang Lin,Rickard Ignell,Qian Han,Øivind Øines,Bill S Hansson,Yu Tang,Jianguo Zhao,Chenghong Liao

doi:10.1038/s41598-020-74998-7

Abstract

Detection of chemical cues via chemosensory receptor proteins are essential for most animals, and underlies critical behaviors, including location and discrimination of food resources, identification of sexual partners and avoidance of predators. The current knowledge of how chemical cues are detected is based primarily on data acquired from studies on insects, while our understanding of the molecular basis for chemoreception in acari, mites in particular, remains limited. The poultry red mite (PRM), Dermanyssus gallinae, is one of the most important blood-feeding ectoparasites of poultry. PRM are active at night which suck the birds' blood during periods of darkness and hide themselves in all kinds of gaps and cracks during the daytime. The diversity in habitat usage, as well as the demonstrated host finding and avoidance behaviors suggest that PRM relies on their sense of smell to orchestrate complex behavioral decisions. Comparative transcriptome analyses revealed the presence of candidate variant ionotropic receptors, odorant binding proteins, niemann-pick proteins type C2 and sensory neuron membrane proteins. Some of these proteins were highly and differentially expressed in the forelegs of PRM. Rhodopsin-like G protein-coupled receptors were also identified, while insect-specific odorant receptors and odorant co-receptors were not detected. Furthermore, using scanning electron microscopy, the tarsomeres of all leg pairs were shown to be equipped with sensilla chaetica with or without tip pores, while wall-pored olfactory sensilla chaetica were restricted to the distal-most tarsomeres of the forelegs. This study is the first to describe the presence of chemosensory genes in any Dermanyssidae family. Our findings make a significant step forward in understanding the chemosensory abilities of D. gallinae.

Highlights

Detection of chemical cues via chemosensory receptor proteins are essential for most animals, and underlies critical behaviors, including location and discrimination of food resources, identification of sexual partners and avoidance of predators
Niemann Pick type C2 (NPC2) proteins have recently been reported in adult predatory mites, suggesting a putative role in detecting of the female sex p heromones[27].Other proteins commonly expressed in the chemosensory system include sensory neuron membrane proteins (SNMPs), which are related to scavenger proteins of the CD36 family, and several classes of G protein-coupled receptors (GPCRs) which allow neurons to sense a variety of extracellular signals, including e.g. hormones and n eurotransmitters[28]
Even though tip pores on the Sc-tp of the distalmost tarsomeres (DT) I-II were indistinct in the scanning electron microscope (SEM) (Fig. 1E), tip pores on DT III-IV were delimited by a round margin (Fig. 1F)