RECURRENT AND RECENT SELECTIVE SWEEPS IN THE piRNA PATHWAY

Uncontrolled transposable element (TE) insertions and excisions can cause chromosome breaks and mutations with dramatic deleterious effects. The PIWI interacting RNA (piRNA) pathway functions as an adaptive TE silencing system during germline development. Several essential piRNA pathway proteins appear to be rapidly evolving, suggesting that TEs and the silencing machinery may be engaged in a classical “evolutionary arms race.” Using a variety of molecular evolutionary and population genetic approaches, we find that the piRNA pathway genes rhino, krimper, and aubergine show patterns suggestive of extensive recurrent positive selection across Drosophila species. We speculate that selection on these proteins reflects crucial roles in silencing unfamiliar elements during vertical and horizontal transmission of TEs into naïve populations and species, respectively.

[1]  Zhiping Weng,et al.  Adaptation to P Element Transposon Invasion in Drosophila melanogaster , 2011, Cell.

[2]  J. Mell,et al.  Molecular evolution under increasing transposable element burden in Drosophila: A speed limit on the evolutionary arms race , 2011, BMC Evolutionary Biology.

[3]  E. Zelentsova,et al.  Expression of Drosophila virilis Retroelements and Role of Small RNAs in Their Intrastrain Transposition , 2011, PloS one.

[4]  Bryan D. Kolaczkowski,et al.  Recurrent adaptation in RNA interference genes across the Drosophila phylogeny. , 2011, Molecular biology and evolution.

[5]  F. Jiggins,et al.  Recent and Recurrent Selective Sweeps of the Antiviral RNAi Gene Argonaute-2 in Three Species of Drosophila , 2010, Molecular biology and evolution.

[6]  Ziheng Yang,et al.  The effect of insertions, deletions, and alignment errors on the branch-site test of positive selection. , 2010, Molecular biology and evolution.

[7]  Anna-Sophie Fiston-Lavier,et al.  Drosophila melanogaster recombination rate calculator. , 2010, Gene.

[8]  R. Sachidanandam,et al.  Small RNA-based silencing strategies for transposons in the process of invading Drosophila species. , 2010, RNA.

[9]  M. Siomi,et al.  How does the royal family of Tudor rule the PIWI-interacting RNA pathway? , 2010, Genes & development.

[10]  E. P. Lei,et al.  HP1 Recruitment in the Absence of Argonaute Proteins in Drosophila , 2010, PLoS genetics.

[11]  A. Domínguez,et al.  Genomic distribution of retrotransposons 297, 1731, copia, mdg1 and roo in the Drosophila melanogaster species subgroup , 2010, Genetica.

[12]  Z. Weng,et al.  The Drosophila HP1 Homolog Rhino Is Required for Transposon Silencing and piRNA Production by Dual-Strand Clusters , 2009, Cell.

[13]  Pablo Librado,et al.  DnaSP v5: a software for comprehensive analysis of DNA polymorphism data , 2009, Bioinform..

[14]  Z. Weng,et al.  Collapse of Germline piRNAs in the Absence of Argonaute3 Reveals Somatic piRNAs in Flies , 2009, Cell.

[15]  Julius Brennecke,et al.  Specialized piRNA Pathways Act in Germline and Somatic Tissues of the Drosophila Ovary , 2009, Cell.

[16]  David Osumi-Sutherland,et al.  FlyBase: enhancing Drosophila Gene Ontology annotations , 2008, Nucleic Acids Res..

[17]  R. Nielsen,et al.  Synonymous and nonsynonymous rate variation in nuclear genes of mammals , 1998, Journal of Molecular Evolution.

[18]  S. Elgin,et al.  Small RNA-directed heterochromatin formation in the context of development: what flies might learn from fission yeast. , 2009, Biochimica et biophysica acta.

[19]  F. Jiggins,et al.  The evolution of RNAi as a defence against viruses and transposable elements , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[20]  Melanie A. Huntley,et al.  Evolution of genes and genomes on the Drosophila phylogeny , 2007, Nature.

[21]  Colin N. Dewey,et al.  Discovery of functional elements in 12 Drosophila genomes using evolutionary signatures , 2007, Nature.

[22]  Seth D Findley,et al.  Drosophila PIWI associates with chromatin and interacts directly with HP1a. , 2007, Genes & development.

[23]  Ziheng Yang.  PAML 4: phylogenetic analysis by maximum likelihood. , 2007, Molecular biology and evolution.

[24]  T. Schüpbach,et al.  zucchini and squash encode two putative nucleases required for rasiRNA production in the Drosophila germline. , 2007, Developmental cell.

[25]  T. Kai,et al.  Unique germ-line organelle, nuage, functions to repress selfish genetic elements in Drosophila melanogaster , 2007, Proceedings of the National Academy of Sciences.

[26]  Manolis Kellis,et al.  Discrete Small RNA-Generating Loci as Master Regulators of Transposon Activity in Drosophila , 2007, Cell.

[27]  Kuniaki Saito,et al.  A Slicer-Mediated Mechanism for Repeat-Associated siRNA 5' End Formation in Drosophila , 2007, Science.

[28]  Vladimir Gvozdev,et al.  A Distinct Small RNA Pathway Silences Selfish Genetic Elements in the Germline , 2006, Science.

[29]  Hsiao-Pei Yang,et al.  Genomewide Comparative Analysis of the Highly Abundant Transposable Element DINE-1 Suggests a Recent Transpositional Burst in Drosophila yakuba , 2006, Genetics.

[30]  D. Halligan,et al.  Natural Selection Drives Extremely Rapid Evolution in Antiviral RNAi Genes , 2006, Current Biology.

[31]  R. Nielsen,et al.  Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. , 2005, Molecular biology and evolution.

[32]  Carlos Bustamante,et al.  Genomic scans for selective sweeps using SNP data. , 2005, Genome research.

[33]  Ari Löytynoja,et al.  An algorithm for progressive multiple alignment of sequences with insertions. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[34]  C. Bustamante,et al.  Distinguishing Between Selective Sweeps and Demography Using DNA Polymorphism Data , 2005, Genetics.

[35]  S. Henikoff,et al.  Positive Selection Drives the Evolution of rhino, a Member of the Heterochromatin Protein 1 Family in Drosophila , 2005, PLoS genetics.

[36]  P. Capy,et al.  The First Steps of Transposable Elements Invasion , 2005, Genetics.

[37]  A. Wong,et al.  Evolutionary Expressed Sequence Tag Analysis of Drosophila Female Reproductive Tracts Identifies Genes Subjected to Positive Selection , 2004, Genetics.

[38]  Nick Goldman,et al.  Accuracy and Power of Statistical Methods for Detecting Adaptive Evolution in Protein Coding Sequences and for Identifying Positively Selected Sites , 2004, Genetics.

[39]  H. Kazazian.  Mobile Elements: Drivers of Genome Evolution , 2004, Science.

[40]  James A. Birchler,et al.  Heterochromatic Silencing and HP1 Localization in Drosophila Are Dependent on the RNAi Machinery , 2004, Science.

[41]  Molly Przeworski,et al.  The signature of positive selection at randomly chosen loci. , 2002, Genetics.

[42]  W. Stephan,et al.  Detecting a local signature of genetic hitchhiking along a recombining chromosome. , 2002, Genetics.

[43]  J. Birchler,et al.  RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. , 2002, Molecular cell.

[44]  Justin C. Fay,et al.  Hitchhiking under positive Darwinian selection. , 2000, Genetics.

[45]  M. Kreitman,et al.  Adaptive protein evolution at the Adh locus in Drosophila , 1991, Nature.

[46]  M. G. Kidwell,et al.  Evidence for horizontal transmission of the P transposable element between Drosophila species. , 1990, Genetics.

[47]  D. Anxolabéhère,et al.  Molecular characteristics of diverse populations are consistent with the hypothesis of a recent invasion of Drosophila melanogaster by mobile P elements. , 1988, Molecular biology and evolution.

[48]  M. Nei,et al.  Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. , 1986, Molecular biology and evolution.