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Viromics of extant insect orders unveil the evolution of the flavi-like superfamily.

ABSTRACT: Insects are the most diversified and species-rich group of animals and harbor an immense diversity of viruses. Several taxa in the flavi-like superfamily, such as the genus Flavivirus, are associated with insects; however, systematic studies on insect virus genetic diversity are lacking, limiting our understanding of the evolution of the flavi-like superfamily. Here, we examined the diversity of flavi-like viruses within the most complete and up-to-date insect transcriptome collection comprising 1,243 insect species by employing a Flaviviridae RdRp profile hidden Markov model search. We identified seventy-six viral sequences in sixty-one species belonging to seventeen insect, one entognathan, and one arachnidan orders. Phylogenetic analyses revealed that twenty-seven sequences fell within the Flaviviridae phylogeny but did not group with established genera. Despite the large diversity of insect hosts studied, we only detected one virus in a blood-feeding insect, which branched within the genus Flavivirus, indicating that this genus likely diversified only in hematophagous arthropods. Nine new jingmenviruses with novel host associations were identified. One of the jingmenviruses established a deep rooting lineage additional to the insect- and tick-associated clades. Segment co-segregation phylogenies support the separation of tick- and insect-associated groups within jingmenviruses, with evidence for segment reassortment. In addition, fourteen viruses grouped with unclassified flaviviruses encompassing genome length of up to 20 kb. Species-specific clades for Hymenopteran- and Orthopteran-associated viruses were identified. Forty-nine viruses populated three highly diversified clades in distant relationship to Tombusviridae, a plant-infecting virus family, suggesting the detection of three previously unknown insect-associated families that contributed to tombusvirus evolution.

SUBMITTER: Paraskevopoulou S

PROVIDER: S-EPMC8129625 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: Previous studies on insect DNA barcoding provide contradictory results and suggest not consistent performances across orders. This work aims at providing a general evaluation of insect DNA barcoding and "mini-barcoding" by performing simulations on a large database of 15,948 DNA barcodes. We compared the proportions of correctly identified queries across a) six insect orders (Coleoptera, Diptera, Hemiptera, Hymenoptera, Lepidoptera and Orthoptera), b) four identification criteria (Best Match: BM; Best Close Match: BCM; All Species Barcodes: ASB; tree-based identification: NJT), and c) reference databases with different taxon coverage (100, 500, 1,000, 1,500 and 1,995 insect species). RESULTS: Analysis of variance revealed highly significant differences among ID criteria and insect orders. A posteriori comparisons of means showed that NJT had always a significantly lower identification success (NJT = 0.656, S.D. = 0.118) compared to both BM and BCM (BM = 0.948, S.D. = 0.026; BCM = 0.946, S.D. = 0.031). NJT showed significant variations among orders, with the highest proportion of correctly identified queries in Hymenoptera and Orthoptera and the lowest in Diptera. Conversely, the proportions of correct matches of BM and BCM were consistent across orders but a progressive increase in false identification was observed when larger reference databases were used. CONCLUSIONS: Regardless the relatively low proportion of Type I errors (misidentification of queries which are represented in the reference database) of BM and BCM, the lack of reference DNA barcodes for 98% of the known insect species implies that insect DNA barcoding is heavily biased by Type II errors (misidentification of queries without conspecifics in the database). The detrimental effects of Type II errors could be circumvented if insect DNA barcoding is used to verify the lack of correspondence between a query and a list of properly referenced target species (e.g. insect pests). This "negative identification" would only be subjected to Type I errors and could be profitably adopted in insect quarantine procedures.

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Viromics of extant insect orders unveil the evolution of the flavi-like superfamily.

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