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Varaldi, J.

Publications and source records attributed to Varaldi, J..

9 recordsLinked to original sources

A Vertically and Horizontally Transmitted RNA Virus Facilitates Egg Hatching of a Parasitoid Wasp

Information on the impacts of RNA viruses inhabiting insect hosts is scarce. Here, we studied the effects of a recently described RNA virus, termed AnvRV, on its host, the parasitoid wasp Anagyrus vladimiri (Hymenoptera: Encyrtidae), an important natural enemy of mealybug pests. AnvRV was found to be maternally transmitted with very high fidelity but not paternally. Additionally, AnvRV was horizontally transferred at an efficiency of 23% from infected to uninfected wasp larvae that develop together inside the same mealybug host (superparasitism). To test the effects of AnvRV on A. vladimiri, the virus horizontal transmission was utilized to establish AnvRV-infected (RV+) and uninfected (RV-) isogenic wasp lines, a method rarely applied and novel to RNA virus-parasitoid systems. Longevity, developmental time, sex ratio, and fecundity of RV+ and RV- A. vladimiri were very similar. Nonetheless, the egg hatching rate of RV+ wasps was markedly and significantly higher than that of RV- wasps, especially in hosts that were not superparasitized. Additionally, less encapsulation marks (the main form of mealybug immunity) were found around RV+ eggs inside parasitized mealybug hosts. Taken together, the data suggest that AnvRV is affecting the mealybugs physiology in a way that improves first stages of wasps development. These findings present a rare example of interaction between an RNA virus and a parasitoid and may provide a tool for the improvement of biological control efforts.

microbiology↗

Dating the origin of a viral domestication event in parasitoid wasps attacking Diptera

Over the course of evolution, hymenopteran parasitoids have developed a close relationship with heritable viruses, sometimes even integrating viral genes into their chromosomes. For example, in Drosophila parasitoids belonging to the Leptopilina genus, 13 viral genes from the Filamentoviridae family have been integrated and domesticated to deliver immunosuppressive factors to host immune cells, thereby protecting parasitoid offspring from host immune responses. The present study aims to comprehensively characterise this domestication event in terms of the viral genes involved, the wasp diversity affected by this event, and its chronology. Our genomic analysis of 41 Cynipoidea wasps from six subfamilies revealed 18 viral genes that were endogenised during the early radiation of the Eucoilini+Trichoplastini clade around 75 million years ago. Wasps from this highly diverse clade develop not only from Drosophila but also from a variety of Schizophora. This event coincides with the radiation of Schizophora, a highly speciose Diptera clade, suggesting that viral domestication facilitated wasp diversification in response to host diversification. Additionally, at least one viral gene was replaced by another Filamentovirus gene in one of the species, highlighting the dynamic nature of viral endogenisation. This study highlights the impact of viral domestication on the diversification of parasitoid wasps.

evolutionary biology↗

Transcriptomic response to pyrethroid treatment in closely related bed bug strains varying in resistance

The common bed bug, Cimex lectularius, is one of the main human parasites. The world-wide resurgence of this pest is mainly due to globalization, and the spread of insecticide resistance. A few studies have compared the transcriptomes of susceptible and resistant strains. However, these studies usually relied on strains originating fromdistant locations, possibly explaining their extended candidate gene lists. Here, we compared the transcriptomes of two strains originating from the same location and showing low overall genetic differentiation (FST =0.018) but varying in their susceptibility to pyrethroids, before and after insecticide exposure. In sharp contrast with previous studies, only 24 genes showing constitutive differential expression between the strainswere identified. Interestingly, most of the genes with increased expression in the resistant strain encoded cuticular proteins. However, those changes were not associated with significant difference in cuticular thickness, suggesting that they might be involved in qualitative changes in the cuticle. In contrast, insecticide exposure induced the expression of a multitude of genes, mostly involved in detoxification. Finally, our set of transcriptome candidate loci showed little overlap with a set of loci strongly genetically differentiated in a previous study using the same strains. Several hypothesis explaining this discrepancy are discussed.

evolutionary biology↗

Community structure of heritable viruses in a Drosophila-parasitoids complex

The diversity and phenotypic impacts related to the presence of heritable bacteria in insects have been extensively studied in the last decades. On the contrary, heritable viruses have been overlooked for several reasons, including technical ones. This is regrettable because of the size of this gap knowledge and because case study indicate that viruses may have profound impact on the functionning of individuals and communities. Additionally, the factors that may shape viral communities are poorly known, except in some very specific viral-insect systems. Here we analyze the community structure of heritable viruses in a multi-hosts-multi-parasitoids community. Drosophilidae and their larval and pupal parasitoids were sampled in two locations, two years and two seasons. After two lab generations, putative DNA and RNA viruses were purified and sequenced. Our analysis revealed the presence of 53 viruses (including 37 new viruses), the great majority of which were RNA viruses. The "species" factor was by far the most significant one, explaining more than 50% of the variance in viral structure. Additionally, parasitoids had a higher number of heritable viruses compared to their hosts, suggesting that this lifestyle favours the association with viruses. Finally, our community-level survey challenged previous interpretation concerning the host range of some previously described viruses.

evolutionary biology↗

A major 6 Mb superlocus is involved in pyrethroid resistance in the common bed bug Cimex lectularius

In the last few years, the bed bug Cimex lectularius has been an increasing problem world-wide, mainly due to the development of insecticide resistance to pyrethroids. The characterization of resistance alleles is a prerequisite to improve surveillance and resistance management. To identify genomic variants associated with pyrethroid resistance in Cimex lectularius, we compared the genetic composition of two recent and resistant populations with that of two ancientsusceptible strains using a genome-wide pool-seq design. We identified a large 6 Mb "superlocus" showing particularly high genetic differentiation and association with the resistance phenotype. This superlocus contained several clustered resistance genes, and was also characterized by a high density of structural variants (inversions, duplications). The possibility that this superlocus constitutes a resistance "supergene" that evolved after the clustering of alleles adapted to insecticide and after reduction in recombination is discussed.

evolutionary biology↗

Endo-parasitoid lifestyle promotes endogenization and domestication of dsDNA viruses

The accidental endogenization of viral elements within eukaryotic genomes can occasionally provide significant evolutionary benefits, giving rise to their long-term retention, that is, to viral domestication. For instance, in some endoparasitoid wasps (whose immature stages develop inside their hosts), the membrane-fusion property of double-stranded DNA viruses has been repeatedly domesticated following ancestral endogenizations. The endogenized genes provide female wasps with a delivery tool to inject virulence factors that are essential to the developmental success of their offspring. Because all known cases of viral domestication involve endoparasitic wasps, we hypothesized that this lifestyle, relying on a close interaction between individuals, may have promoted the endogenization and domestication of viruses. By analyzing the composition of 124 Hymenoptera genomes, spread over the diversity of this clade and including free-living, ecto- and endoparasitoid species, we tested this hypothesis. Our analysis first revealed that double-stranded DNA viruses, in comparisons with other viral genomic structures (ssDNA, dsRNA, ssRNA), are more often endogenized and domesticated (that is, retained by selection) than expected from their estimated abundance in insect viral communities. Secondly, our analysis indicates that the rate at which dsDNA viruses are endogenized is higher in endoparasitoids than in ectoparasitoids or free-living hymenopterans, which also translates into more frequent events of domestication. Hence, these results are consistent with the hypothesis that the endoparasitoid lifestyle has facilitated the endogenization of dsDNA viruses, in turn increasing the opportunities of domestications that now play a central role in the biology of many endoparasitoid lineages.

genomics↗

Genomic characterization of viruses associated with the parasitoid Anagyrus vladimiri (Hymenoptera: Encyrtidae)

The knowledge on symbiotic microorganisms of insects has increased in recent years, yet relatively little data is available on non-pathogenic viruses. Here we studied the virome of the parasitoid wasp Anagyrus vladimiri (Hymenoptera: Encyrtidae), a biocontrol agent of mealybugs. By high-throughput sequencing of viral nucleic acids, we revealed three novel viruses, belonging to the families Reoviridae (provisionally termed AnvRV [Anagyrus vladimiri reovirus]), Iflaviridae (AnvIFV) and Dicistroviridae (AnvDV). Phylogenetic analysis further classified the AnvRV in the genus Idnoreovirus, and the AnvDV in the genus Triatovirus. The genome of AnvRV is comprised of 10 distinct genomic segments ranging in length from 1.5 to 4.2 Kbp, but only two out of the 10 open reading frames (ORFs) have a known function. AnvIFV and AnvDV each have one polypeptide ORF, which is typical to iflaviruses but very un-common among dicistroviruses. AnvRV was found to be fixed in a mass-reared population of A. vladimiri, whereas its prevalence in field-collected wasps was ~15%. Similarly, the prevalence of AnvIFV and AnvDV were much higher in the mass rearing population than in the field population. Transmission electron micrographs of females ovaries revealed clusters and viroplasms of Reovirus-like particles in follicle cells. AnvRV was not detected in the mealybugs, suggesting that this virus is truly associated with the wasps. The possible effects of these viruses on A. vladimiris biology, and on biocontrol agents in general are discussed. Our findings identify RNA viruses as potential players involved in the multitrophic system of mealybugs, their parasitoids and other members of the holobiont. ImportanceDifferent biological control approaches use industrially mass-reared natural enemy insects to reduce damage of arthropod pests. Such mass-reared cultures may be positively and/or negatively affected by various microorganisms, including viruses. Yet, current knowledge on virus diversity, especially in arthropods, is limited. Here, we provide the first virome characterization of a member of the wasps family Encyrtidae - the member being the parasitoid Anagyrus vladimiri - a commercially important natural enemy of mealybug pests. We describe the genome of three previously unknown RNA viruses, co-inhabiting this parasitoid, and elaborate on the prevalence of those viruses in individual wasps of both mass-reared and environmental origins. Microscopy images suggest that at least one of the viruses is transmitted maternally via the ovaries. We discuss the genomic structure of the viruses and the possible relationship between those viruses and the A. vladimiri host, with implications on improvement of biocontrol of mealybug pests.

microbiology↗

DROP: Molecular voucher database for identification of Drosophila parasitoids

Molecular identification is increasingly used to speed up biodiversity surveys and laboratory experiments. However, many groups of organisms cannot be reliably identified using standard databases such as GenBank or BOLD due to lack of sequenced voucher specimens identified by experts. Sometimes a large number of sequences are available, but with too many errors to allow identification. Here we address this problem for parasitoids of Drosophila by introducing a curated open-access molecular reference database, DROP (Drosophila parasitoids). Identifying Drosophila parasitoids is challenging and poses a major impediment to realize the full potential of this model system in studies ranging from molecular mechanisms to food webs, and in biological control of Drosophila suzukii. In DROP (http://doi.org/10.5281/zenodo.4519656), genetic data are linked to voucher specimens and, where possible, the voucher specimens are identified by taxonomists and vetted through direct comparison with primary type material. To initiate DROP, we curated 154 laboratory strains, 856 vouchers, 554 DNA sequences, 16 genomes, 14 transcriptomes, and 6 proteomes drawn from a total of 183 operational taxonomic units (OTUs): 114 described Drosophila parasitoid species and 69 provisional species. We found species richness of Drosophila parasitoids to be heavily underestimated and provide an updated taxonomic catalogue for the community. DROP offers accurate molecular identification and improves cross-referencing between individual studies that we hope will catalyze research on this diverse and fascinating model system. Our effort should also serve as an example for researchers facing similar molecular identification problems in other groups of organisms.

genomics↗

Immuno-suppressive Virus-like particles of Drosophila parasitoids derive from the domestication of a behaviour-manipulating virus relative

To circumvent host immune response, some hymenopteran endo-parasitoids produce virus-like structures in their reproductive apparatus that are injected into the host together with the eggs. These viral-like structures are absolutely necessary for the reproduction of these wasps. The viral evolutionary origin of these viral-like particles has been demonstrated in only a few cases of wasp species all belonging to the Ichneumonoidea superfamily. In addition, the nature of the initial virus-wasp association remains unknown for all. This is either because no closely related descendant infects the wasps, because it has not been sampled yet, or because the virus lineage went extinct. In this paper, we show that the virus-like particles (VLPs) produced by endoparasitoids of Drosophila belonging to the Leptopilina genus (superfamily Cynipoidea) do have a viral origin, solving the debate on their origin. Furthermore, the ancestral donor virus still has close relatives infecting one of the wasp species, thus giving us insights on the ecological interaction that possibly allowed the domestication process. Intriguingly, this contemporary virus is both vertically and horizontally transmitted and has the particularity to manipulate the superparasitism behavior of the wasp. This raises the possibility that behavior manipulation has been instrumental in the birth of such association between wasps and viruses.

evolutionary biology↗