Abstract

Orthopteran insects have high reproductive rates leading to boom-bust population dynamics with high local densities that are ideal for short, episodic disease epidemics. Viruses are particularly well suited for such host population dynamics, due to their supreme ability to adapt to changing transmission criteria. However, very little is known about the viruses of Orthopteran insects. Since Orthopterans are increasingly reared commercially, for animal feed and human consumption, there is a risk that viruses naturally associated with these insects can adapt to commercial rearing conditions, and cause disease. We therefore explored the virome of the house cricket Acheta domesticus, which is both part of the natural Swedish landscape and reared commercially for the pet feed market. Only 1% of the faecal RNA and DNA from wild-caught A. domesticus consisted of viruses. These included both known and novel viruses associated with crickets/insects, their bacterial-fungal microbiome, or their plant food. Relatively abundant among these viral Operational Taxonomic Units (OTUs) was a novel Iflavirus, tentatively named Acheta domesticus Iflavirus (AdIV). Quantitative analyses showed that AdIV was also abundant in frass and insect samples from commercially reared crickets. Interestingly, the wild and commercial AdIV strains had short, extremely divergent variation hotspots throughout the genome, which may indicate specific adaptation to their hosts’ distinct rearing environments.

Highlights

  • Viruses were first identified through their association with disease symptoms, and only subsequently described genetically

  • A classic example of this is the deformed wing virus, which is currently the most common and lethal virus disease of honeybees worldwide [6,7], but was practically undetectable until it became associated with a new and highly potent transmission route, the ectoparasitic mite Varroa destructor [8,9]. This change in transmission route, pathological profile, and virulence proceeded through typical evolutionary virology stages and mechanisms [10,11,12], involving the evolution of distinct derivative strains optimized to the new transmission route [13,14], the co-circulation and spread of pre- and post-adapted strains through a common quasi-species [15] and the management of viral pathology, virulence, and quasi-species composition through control of the new transmission route [9,14,15]

  • The study design consisted of an initial target-free screening of both the DNA and RNA phases of a single frass sample of wild-caught Swedish house crickets, followed by targeted screening, full genome assembly, and genomic comparison of two distinct strains of a novel Iflavirus isolated from wild and commercially reared A. domesticus

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Summary

Introduction

Viruses were first identified through their association with disease symptoms, and only subsequently described genetically. This process is reversed in modern virus prospecting, where the viral agents are first identified and described genetically [1,2], and only subsequently investigated for possible biological roles or disease associations [3,4] This has led to the realization that virus diversity is chronically underrepresented in the public nucleotide databases and that the vast majority of viruses are largely asymptomatic, with pathological viruses the exception rather than the rule [5]. This change in transmission route, pathological profile, and virulence proceeded through typical evolutionary virology stages and mechanisms [10,11,12], involving the evolution of distinct derivative strains optimized to the new transmission route [13,14], the co-circulation and spread of pre- and post-adapted strains through a common quasi-species [15] and the management of viral pathology, virulence, and quasi-species composition through control of the new transmission route [9,14,15]

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