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PMID: 17989258 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Validation Study

Evolutionary rate analyses of orthologs and paralogs from 12 Drosophila genomes.

Genome research ·Vol. 17 ·No. 12 ·2007-12-00 ·Pages 1837-49

Heger A, Ponting CP

Abstract

The newly sequenced genome sequences of 11 Drosophila species provide the first opportunity to investigate variations in evolutionary rates across a clade of closely related species. Protein-coding genes were predicted using established Drosophila melanogaster genes as templates, with recovery rates ranging from 81%-97% depending on species divergence and on genome assembly quality. Orthology and paralogy assignments were shown to be self-consistent among the different Drosophila species and to be consistent with regions of conserved gene order (synteny blocks). Next, we investigated the rates of diversification among these species' gene repertoires with respect to amino acid substitutions and to gene duplications. Constraints on amino acid sequences appear to have been most pronounced on D. ananassae and least pronounced on D. simulans and D. erecta terminal lineages. Codons predicted to have been subject to positive selection were found to be significantly over-represented among genes with roles in immune response and RNA metabolism, with the latter category including each subunit of the Dicer-2/r2d2 heterodimer. The vast majority of gene duplications (96.5%) and synteny rearrangements were found to occur, as expected, within single Müller elements. We show that the rate of ancient gene duplications was relatively uniform. However, gene duplications in terminal lineages are strongly skewed toward very recent events, consistent with either a rapid-birth and rapid-death model or the presence of large proportions of copy number variable genes in these Drosophila populations. Duplications were significantly more frequent among trypsin-like proteases and DM8 putative lipid-binding domain proteins.

MeSH Terms
Animals Conserved Sequence Drosophila Proteins/genetics Drosophila melanogaster/genetics,metabolism Evolution, Molecular Genetic Variation Genome, Insect Sequence Homology, Nucleic Acid Synteny/genetics
Chemicals
Drosophila Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Heger Andreas
Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3QX, United Kingdom. [email protected]
Ponting Chris P
References (49)
49 references, click to expand
  1. How malleable is the eukaryotic genome? Extreme rate of chromosomal rearrangement in the genus Drosophila.
    Genome Res. 2001 Feb;11(2):230-9 PMID: 11157786
  2. Genomic relationships and speciation times of human, chimpanzee, and gorilla inferred from a coalescent hidden Markov model.
    PLoS Genet. 2007 Feb 23;3(2):e7 PMID: 17319744
  3. Fast protein evolution and germ line expression of a Drosophila parental gene and its young retroposed paralog.
    Mol Biol Evol. 2006 Nov;23(11):2191-202 PMID: 16916943
  4. Slightly deleterious mutant substitutions in evolution.
    Nature. 1973 Nov 9;246(5428):96-8 PMID: 4585855
  5. Evolution of genes and genomes on the Drosophila phylogeny.
    Nature. 2007 Nov 8;450(7167):203-18 PMID: 17994087
  6. Genome sequence of the Brown Norway rat yields insights into mammalian evolution.
    Nature. 2004 Apr 1;428(6982):493-521 PMID: 15057822
  7. Constitutive expression of a complement-like protein in toll and JAK gain-of-function mutants of Drosophila.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11427-32 PMID: 11027343
  8. Initial sequencing and comparative analysis of the mouse genome.
    Nature. 2002 Dec 5;420(6915):520-62 PMID: 12466850
  9. R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway.
    Science. 2003 Sep 26;301(5641):1921-5 PMID: 14512631
  10. High intrinsic rate of DNA loss in Drosophila.
    Nature. 1996 Nov 28;384(6607):346-9 PMID: 8934517
  11. Molecular phylogeny and divergence times of drosophilid species.
    Mol Biol Evol. 1995 May;12(3):391-404 PMID: 7739381
  12. Ensembl 2006.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D556-61 PMID: 16381931
  13. Variable strength of translational selection among 12 Drosophila species.
    Genetics. 2007 Nov;177(3):1337-48 PMID: 18039870
  14. Rapid concerted evolution via gene conversion at the Drosophila hsp70 genes.
    J Mol Evol. 2002 May;54(5):569-86 PMID: 11965431
  15. FlyBase: anatomical data, images and queries.
    Nucleic Acids Res. 2006 Jan 1;34(Database issue):D484-8 PMID: 16381917
  16. The evolutionary fate and consequences of duplicate genes.
    Science. 2000 Nov 10;290(5494):1151-5 PMID: 11073452
  17. The rapid evolution of reproductive proteins.
    Nat Rev Genet. 2002 Feb;3(2):137-44 PMID: 11836507
  18. Peritrophic matrix proteins.
    Insect Biochem Mol Biol. 1999 Feb;29(2):87-101 PMID: 10196732
  19. Automated generation of heuristics for biological sequence comparison.
    BMC Bioinformatics. 2005 Feb 15;6:31 PMID: 15713233
  20. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages.
    Mol Biol Evol. 2002 Jun;19(6):908-17 PMID: 12032247
  21. An analysis of the gene complement of a marsupial, Monodelphis domestica: evolution of lineage-specific genes and giant chromosomes.
    Genome Res. 2007 Jul;17(7):969-81 PMID: 17495010
  22. Analysis of the eye developmental pathway in Drosophila using DNA microarrays.
    Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4024-9 PMID: 12655063
  23. GeneWise and Genomewise.
    Genome Res. 2004 May;14(5):988-95 PMID: 15123596
  24. The evolution of antifungal peptides in Drosophila.
    Genetics. 2005 Dec;171(4):1847-59 PMID: 16157672
  25. A brief history of Drosophila's contributions to genome research.
    Science. 2000 Mar 24;287(5461):2216-8 PMID: 10731135
  26. Molecular evolution between Drosophila melanogaster and D. simulans: reduced codon bias, faster rates of amino acid substitution, and larger proteins in D. melanogaster.
    Genetics. 1996 Nov;144(3):1297-307 PMID: 8913769
  27. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.
    Nat Genet. 2000 May;25(1):25-9 PMID: 10802651
  28. Phylogenetic reconstruction of orthology, paralogy, and conserved synteny for dog and human.
    PLoS Comput Biol. 2006 Sep 29;2(9):e133 PMID: 17009864
  29. Molecular evolution in the Drosophila melanogaster species subgroup: frequent parameter fluctuations on the timescale of molecular divergence.
    Genetics. 2006 Mar;172(3):1711-26 PMID: 16387879
  30. Inferring parameters of mutation, selection and demography from patterns of synonymous site evolution in Drosophila.
    Genetics. 2001 Jan;157(1):245-57 PMID: 11139506
  31. Drosophila C-type lectins enhance cellular encapsulation.
    Mol Immunol. 2007 Apr;44(10):2541-8 PMID: 17287021
  32. Assessing the impact of comparative genomic sequence data on the functional annotation of the Drosophila genome.
    Genome Biol. 2002;3(12):RESEARCH0086 PMID: 12537575
  33. Novel genes expressed in subsets of chemosensory sensilla on the front legs of male Drosophila melanogaster.
    Cell Tissue Res. 2002 Mar;307(3):381-92 PMID: 11904775
  34. Use of RNA interference in Drosophila S2 cells to identify host pathways controlling compartmentalization of an intracellular pathogen.
    Proc Natl Acad Sci U S A. 2005 Sep 20;102(38):13646-51 PMID: 16157870
  35. Comparative genome sequencing of Drosophila pseudoobscura: chromosomal, gene, and cis-element evolution.
    Genome Res. 2005 Jan;15(1):1-18 PMID: 15632085
  36. Drosophila melanogaster: a case study of a model genomic sequence and its consequences.
    Genome Res. 2005 Dec;15(12):1661-7 PMID: 16339363
  37. Detecting amino acid sites under positive selection and purifying selection.
    Genetics. 2005 Mar;169(3):1753-62 PMID: 15654091
  38. Splitting pairs: the diverging fates of duplicated genes.
    Nat Rev Genet. 2002 Nov;3(11):827-37 PMID: 12415313
  39. Widespread discordance of gene trees with species tree in Drosophila: evidence for incomplete lineage sorting.
    PLoS Genet. 2006 Oct 27;2(10):e173 PMID: 17132051
  40. Molecular phylogeny of the Drosophila melanogaster species subgroup.
    J Mol Evol. 2003 Nov;57(5):562-73 PMID: 14738315
  41. Novel protein domains and repeats in Drosophila melanogaster: insights into structure, function, and evolution.
    Genome Res. 2001 Dec;11(12):1996-2008 PMID: 11731489
  42. The rosy region of Drosophila melanogaster and Drosophila simulans. I. Contrasting levels of naturally occurring DNA restriction map variation and divergence.
    Genetics. 1988 Aug;119(4):875-88 PMID: 2900794
  43. ML -- a conserved domain involved in innate immunity and lipid metabolism.
    Trends Biochem Sci. 2002 May;27(5):219-21 PMID: 12076526
  44. Serine proteases and their homologs in the Drosophila melanogaster genome: an initial analysis of sequence conservation and phylogenetic relationships.
    Gene. 2003 Jan 30;304:117-31 PMID: 12568721
  45. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  46. Natural selection drives extremely rapid evolution in antiviral RNAi genes.
    Curr Biol. 2006 Mar 21;16(6):580-5 PMID: 16546082
  47. Finishing the euchromatic sequence of the human genome.
    Nature. 2004 Oct 21;431(7011):931-45 PMID: 15496913
  48. Evolution and comparative genomics of odorant- and pheromone-associated genes in rodents.
    Genome Res. 2004 Apr;14(4):591-602 PMID: 15060000
  49. Comparison of the genomes of human and mouse lays the foundation of genome zoology.
    Hum Mol Genet. 2003 Apr 1;12(7):701-9 PMID: 12651866
Article Info
Journal
Genome research
Abbr.
Genome Res
ISSN
1088-9051
Published
2007-12-00
Epub
2007-00-07
Pages
1837-49
Language
English
Region
United States
NLM ID
9518021
PMCID
PMC2099592
Subset
IM
Grants
Medical Research Council · MC_U137761446 · United Kingdom
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