title: Repeated Duplication of Argonaute2 Is Associated with Strong Selection and Testis Specialization in Drosophila.
abstract: 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.
authors.affiliation: Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, EH9 3FL, United Kingdom sam.lewis@gen.cam.ac.uk.
authors.forename: Samuel H
authors.initials: SH
authors.lastname: Lewis
authors.affiliation: Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, EH9 3FL, United Kingdom.
authors.forename: Claire L
authors.initials: CL
authors.lastname: Webster
authors.affiliation: Department of Biosciences, Centre of Excellence in Biological Interactions, University of Helsinki, Finland.
authors.forename: Heli
authors.initials: H
authors.lastname: Salmela
authors.affiliation: Institute of Evolutionary Biology, University of Edinburgh, Ashworth Laboratories, EH9 3FL, United Kingdom Centre for Immunity, Infection and Evolution, University of Edinburgh, Ashworth Laboratories, EH9 3FL, United Kingdom.
authors.forename: Darren J
authors.initials: DJ
authors.lastname: Obbard
mesh_terms: D000818:Animals; D060565:Argonaute Proteins / Q000235:genetics*; D004251:DNA Transposable Elements / Q000235:genetics; D029721:Drosophila Proteins / Q000235:genetics*; D004331:Drosophila melanogaster / Q000235:genetics* / Q000254:growth & development; D019143:Evolution, Molecular; D020440:Gene Duplication / Q000235:genetics; D018507:Gene Expression Regulation, Developmental; D005828:Genetics, Population; D049750:Genome, Insect; D008297:Male; D009928:Organ Specificity / Q000235:genetics; D012641:Selection, Genetic / Q000235:genetics*; D017385:Sequence Homology; D013737:Testis / Q000254:growth & development
chemical_list: C433807:AGO2 protein, Drosophila; D060565:Argonaute Proteins; D004251:DNA Transposable Elements; D029721:Drosophila Proteins
keywords: Argonaute; Drosophila; RNAi; duplication; testis