Abstract
BackgroundRNA interference (RNAi) related pathways provide defense against viruses and transposable elements, and have been implicated in the suppression of meiotic drive elements. Genes in these pathways often exhibit high levels of adaptive substitution, and over longer timescales show gene duplication and loss—most likely as a consequence of their role in mediating conflict with these parasites. This is particularly striking for Argonaute 2 (Ago2), which is ancestrally the key effector of antiviral RNAi in insects, but has repeatedly formed new testis-specific duplicates in the recent history of the obscura species-group of Drosophila.ResultsHere we take advantage of publicly available genomic and transcriptomic data to identify six further RNAi-pathway genes that have duplicated in this clade of Drosophila, and examine their evolutionary history. As seen for Ago2, we observe high levels of adaptive amino-acid substitution and changes in sex-biased expression in many of the paralogs. However, our phylogenetic analysis suggests that co-duplications of the RNAi machinery were not synchronous, and our expression analysis fails to identify consistent male-specific expression.ConclusionsThese results confirm that RNAi genes, including genes of the antiviral and piRNA pathways, have undergone multiple independent duplications and that their history has been particularly labile within the obscura group. However, they also suggest that the selective pressures driving these changes have not been consistent, implying that more than one selective agent may be responsible.
Highlights
RNA interference (RNAi) related pathways provide defense against viruses and transposable elements, and have been implicated in the suppression of meiotic drive elements
Obscura group Argonaute 2 genes are duplicated and show male-biased expression The obscura group has experienced multiple duplications of Ago2 and it has previously been shown that these are associated with positive selection and testis-specific expression [4]
In agreement with the previous analysis of Ago2 [4], we found that the duplications giving rise to Ago2e and Ago2f predated the split between the obscura and pseudoobscura subgroups, with a subsequent loss of Ago2f from the pseudoobscura subgroup (Fig. 3)
Summary
RNA interference (RNAi) related pathways provide defense against viruses and transposable elements, and have been implicated in the suppression of meiotic drive elements Genes in these pathways often exhibit high levels of adaptive substitution, and over longer timescales show gene duplication and loss—most likely as a consequence of their role in mediating conflict with these parasites. The RNAi-related pathways comprise a range of small-RNA mechanisms best known for their roles in mediating the control of gene expression, antiviral responses, and defence against mobile genetic elements These include the miRNA pathway (Dicer-1 and Argonaute-1 in insects [6]), the siRNA pathway (Dcr-2 and Argounate 2 in insects [7]), and the piRNA pathway (piwi-family Argonaute AGO3 and Piwi/Aub in Crysnanto and Obbard BMC Evolutionary Biology (2019) 19:99 insects [8, 9]). It has been hypothesized that this may be a consequence of parasite-mediated ‘arms-race’ coevolution [21, 24], either through conflict with parasite-encoded immune suppressors—as widely seen in RNA viruses [25]—or in the case of the piRNA pathway, through selection for ‘re-tuning’ suppression mechanisms [26]
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