Vertically transmitted viral endosymbionts of insects: do sigma viruses walk alone?

Longdon, Ben; Jiggins, Francis M.

doi:10.1098/rspb.2012.1208

Cited by 57 publications

(74 citation statements)

References 98 publications

(130 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…It has been demonstrated that this biparental transmission is highly invasive, even if the virus imposes a cost on its host (Longdon et al, 2011). For instance, a strain of sigma virus (Rhabdovirus) has invaded populations of Drosophila obscura in the UK, reaching 39 % infection in less than 11 years (Longdon et al, 2011) despite the cost imposed by the virus on the fly host (Longdon & Jiggins, 2012), demonstrating the invasive power of biparental transmission. Thus, independently of any positive effect on fitness, the biparental transmission of LbTV may explain its worldwide distribution and high prevalence in natural populations.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Additional heritable virus in the parasitic wasp Leptopilina boulardi: prevalence, transmission and phenotypic effects

Martinez

Lepetit

Ravallec

et al. 2016

Journal of General Virology

View full text Add to dashboard Cite

Parasitoid wasps can be found in association with heritable viruses. Although some viruses have been shown to profoundly affect the biology and evolution of parasitoid wasps, the genetic and phenotypic diversity of parasitoid-associated viruses remains largely unexplored. We previously discovered a behaviour-manipulating DNA virus in the parasitoid wasp Leptopilina boulardi. In this species, which lays its eggs inside Drosophila larvae, Leptopilina boulardi filamentous virus (LbFV) forces the females to lay their eggs in already parasitized Drosophila larvae. This behavioural manipulation increases the chances for the horizontal transmission of the virus. Here, we describe in the same parasitoid species another virus, which we propose to call Leptopilina boulardi toti-like virus (LbTV). This doublestranded RNA virus is highly prevalent in insect laboratory lines as well as in parasitoids caught in the field. In some cases, LbTV was found in coinfection with LbFV, but did not affect the behaviour of the wasp. Instead we found that the presence of LbTV correlates with an increase in the number of offspring, mostly due to increased survival of parasitoid larvae. LbTV is vertically transmitted mostly through the maternal lineage even if frequent paternal transmission also occurs. Unlike LbFV, LbTV is not horizontally transmitted. Its genome encodes a putative RNA-dependent RNA polymerase (RdRp) showing similarities with RdRps of Totiviridae. These results underline the high incidence and diversity of inherited viruses in parasitoids as well as their potential impact on the phenotype of their hosts.

show abstract

Section: Discussionmentioning

confidence: 99%

“…In addition, LbTV was paternally transmitted, although with a much lower rate than for maternal transmission. Paternal transmission is a common route of transmission for Drosophila sigma viruses (Longdon & Jiggins, 2012;Longdon et al, 2011) or the Drosophila S virus (Ló pez Ferber et al, 1997).…”

Section: Discussionmentioning

confidence: 99%

Additional heritable virus in the parasitic wasp Leptopilina boulardi: prevalence, transmission and phenotypic effects

Martinez

Lepetit

Ravallec

et al. 2016

Journal of General Virology

View full text Add to dashboard Cite

show abstract

“…Of these, testis-specific dosage compensation seems the least likely to drive testis specificity because the MSL complex, which Ago2 directs to X-linked genes to carry out dosage compensation in the soma of D. melanogaster, is absent from testis (Conrad and Akhtar 2012). Testis-specific antiviral defense seems similarly unlikely, as the only known paternally transmitted Drosophila viruses (Sigmaviruses; Rhabdoviridae) pass through both the male and female gametes (Longdon and Jiggins 2012), and so the potential benefits of testis specificity seem unclear. Alternatively, testis-specific Ago2 duplicates could be coevolving with other testis-specific genes through the hairpin RNA pathway, in which siRNAs generated from endogenous hairpin-forming RNAs (hpRNAs) bind Ago2 and regulate the expression of host genes .…”

Section: Potential Testis-specific Functionsmentioning

confidence: 99%

Repeated duplication of Argonaute2 is associated with strong selection and testis specialization inDrosophila

Lewis

Webster

Salmela

et al. 2016

Preprint

View full text Add to dashboard Cite

Argonaute2 (Ago2) is a rapidly evolving nuclease in the Drosophila melanogaster RNA interference (RNAi) pathway that targets viruses and transposable elements in somatic tissues. Here we reconstruct the history of Ago2 duplications across the D. obscura group and use patterns of gene expression to infer new functional specialization. We show that some duplications are old, shared by the entire species group, and that losses may be common, including previously undetected losses in the lineage leading to D. pseudoobscura. We find that while the original (syntenic) gene copy has generally retained the ancestral ubiquitous expression pattern, most of the novel Ago2 paralogs have independently specialized to testis-specific expression. Using population genetic analyses, we show that most testis-specific paralogs have significantly lower genetic diversity than the genome-wide average. This suggests recent positive selection in three different species, and model-based analyses provide strong evidence of recent hard selective sweeps in or near four of the six D. pseudoobscura Ago2 paralogs. We speculate that the repeated evolution of testis specificity in obscura group Ago2 genes, combined with their dynamic turnover and strong signatures of adaptive evolution, may be associated with highly derived roles in the suppression of transposable elements or meiotic drive. Our study highlights the lability of RNAi pathways, even within well-studied groups such as Drosophila, and suggests that strong selection may act quickly after duplication in RNAi pathways, potentially giving rise to new and unknown RNAi functions in nonmodel species. KEYWORDS Argonaute; RNAi; Drosophila; duplication; testis A RGONAUTE genes are found in almost all eukaryotes, where they play a key role in antiviral immune defense, gene regulation, and genome stability. They perform this diverse range of functions through their role in RNA interference (RNAi) mechanisms, an ancient system of nucleic acid manipulation in which small RNA (sRNA) molecules guide Argonaute proteins to nucleic acid targets through base complementarity (reviewed in Meister 2013). Gene duplication has occurred throughout the evolution of the Argonaute gene family, with ancient duplication events characteristic of some lineages-such as three duplications early in plant evolution (Singh et al. 2015) and multiple expansions and losses throughout the evolution of nematodes (reviewed in Buck and Blaxter 2013) and the Diptera . After duplication, Argonautes have often undergone functional divergence, involving changes in expression patterns and altered sRNA binding partners (Lu et al. 2011;Leebonoi et al. 2015;Miesen et al. 2015). Duplication early in eukaryotic evolution produced two distinct Argonaute subfamilies, Ago and Piwi, which have since been retained in the vast majority of Metazoa (Cerutti and Casas-Mollano 2006). Members of the Ago subfamily are expressed in both somatic and germline tissue, and variously bind sRNAs derived from host transcripts (miRNAs, endo-siRNAs) ...

show abstract

“…The gap in knowledge is perhaps largest for arthropod hosts in which viruses are either asymptomatic or beneficial to the host (7). Several authors have suggested publication and detection biases for pathogenic interactions over nonpathogenic interactions (7)(8)(9). Thus, for some groups of RNA viruses, the "silent" majority may remain undetected, because genetic probes, sequence and motif searches, and even host preservation methods favor either pathogenic or DNA-based taxa.…”

mentioning

confidence: 99%

Discovery and Evolution of Bunyavirids in Arctic Phantom Midges and Ancient Bunyavirid-Like Sequences in Insect Genomes

Ballinger

Bruenn

Hay

et al. 2014

J Virol

View full text Add to dashboard Cite

Bunyaviridae is a large family of RNA viruses chiefly comprised of vertebrate and plant pathogens. We discovered novel bunyavirids that are approximately equally divergent from each of the five known genera. We characterized novel genome sequences for two bunyavirids, namely, Kigluaik phantom virus (KIGV), from tundra-native phantom midges (Chaoborus), and Nome phantom virus (NOMV), from tundra-invading phantom midges, and demonstrated that these bunyavirid-like sequences belong to an infectious virus by passaging KIGV in mosquito cell culture, although the infection does not seem to be well sustained beyond a few passages. Virus and host gene sequences from individuals collected on opposite ends of North America, a region spanning 4,000 km, support a long-term, vertically transmitted infection of KIGV in Chaoborus trivittatus. KIGV-like sequences ranging from single genes to full genomes are present in transcriptomes and genomes of insects belonging to six taxonomic orders, suggesting an ancient association of this clade with insect hosts. In Drosophila, endogenous virus genes have been coopted, forming an orthologous tandem gene family that has been maintained by selection during the radiation of the host genus. Our findings indicate that bunyavirid-host interactions in nonbloodsucking arthropods have been much more extensive than previously thought. IMPORTANCEVery little is known about the viral diversity in polar freshwater ponds, and perhaps less is known about the effects that climateinduced habitat changes in these regions will have on virus-host interactions in the coming years. Our results show that at the tundra-boreal boundary, a hidden viral landscape is being altered as infected boreal phantom midges colonize tundra ponds. Likewise, relatively little is known of the deeper evolutionary history of bunyavirids that has led to the stark lifestyle contrasts between some genera. The discovery of this novel bunyavirid group suggests that ancient and highly divergent bunyavirid lineages remain undetected in nature and may offer fresh insight into host reservoirs, potential sources of emerging disease, and major lifestyle shifts in the evolutionary history of viruses in the family Bunyaviridae.

show abstract

Vertically transmitted viral endosymbionts of insects: do sigma viruses walk alone?

Cited by 57 publications

References 98 publications

Additional heritable virus in the parasitic wasp Leptopilina boulardi: prevalence, transmission and phenotypic effects

Additional heritable virus in the parasitic wasp Leptopilina boulardi: prevalence, transmission and phenotypic effects

Repeated duplication of Argonaute2 is associated with strong selection and testis specialization inDrosophila

Discovery and Evolution of Bunyavirids in Arctic Phantom Midges and Ancient Bunyavirid-Like Sequences in Insect Genomes

Contact Info

Product

Resources

About