• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of geneticsGeneticsCurrent IssueInformation for AuthorsEditorial BoardSubscribeSubmit a Manuscript
Genetics. Aug 2003; 164(4): 1471–1480.
PMCID: PMC1462669

Natural selection drives Drosophila immune system evolution.

Abstract

Evidence from disparate sources suggests that natural selection may often play a role in the evolution of host immune system proteins. However, there have been few attempts to make general population genetic inferences on the basis of analysis of several immune-system-related genes from a single species. Here we present DNA polymorphism and divergence data from 34 genes thought to function in the innate immune system of Drosophila simulans and compare these data to those from 28 nonimmunity genes sequenced from the same lines. Several statistics, including average K(A)/K(S) ratio, average silent heterozygosity, and average haplotype diversity, significantly differ between the immunity and nonimmunity genes, suggesting an important role for directional selection in immune system protein evolution. In contrast to data from mammalian immunoglobulins and other proteins, we find no strong evidence for the selective maintenance of protein diversity in Drosophila immune system proteins. This may be a consequence of Drosophila's generalized innate immune response.

Full Text

The Full Text of this article is available as a PDF (97K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Andolfatto P. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 2001 Mar;18(3):279–290. [PubMed]
  • Bauer VL, Aquadro CF. Rates of DNA sequence evolution are not sex-biased in Drosophila melanogaster and D. simulans. Mol Biol Evol. 1997 Dec;14(12):1252–1257. [PubMed]
  • Begun DJ. The frequency distribution of nucleotide variation in Drosophila simulans. Mol Biol Evol. 2001 Jul;18(7):1343–1352. [PubMed]
  • Begun David J. Protein variation in Drosophila simulans, and comparison of genes from centromeric versus noncentromeric regions of chromosome 3. Mol Biol Evol. 2002 Feb;19(2):201–203. [PubMed]
  • Begun DJ, Aquadro CF. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster. Nature. 1992 Apr 9;356(6369):519–520. [PubMed]
  • Begun DJ, Whitley P. Adaptive evolution of relish, a Drosophila NF-kappaB/IkappaB protein. Genetics. 2000 Mar;154(3):1231–1238. [PMC free article] [PubMed]
  • Begun DJ, Whitley P. Reduced X-linked nucleotide polymorphism in Drosophila simulans. Proc Natl Acad Sci U S A. 2000 May 23;97(11):5960–5965. [PMC free article] [PubMed]
  • Belvin MP, Anderson KV. A conserved signaling pathway: the Drosophila toll-dorsal pathway. Annu Rev Cell Dev Biol. 1996;12:393–416. [PubMed]
  • Bishop JG, Dean AM, Mitchell-Olds T. Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution. Proc Natl Acad Sci U S A. 2000 May 9;97(10):5322–5327. [PMC free article] [PubMed]
  • Braverman JM, Hudson RR, Kaplan NL, Langley CH, Stephan W. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics. 1995 Jun;140(2):783–796. [PMC free article] [PubMed]
  • Charlesworth B, Morgan MT, Charlesworth D. The effect of deleterious mutations on neutral molecular variation. Genetics. 1993 Aug;134(4):1289–1303. [PMC free article] [PubMed]
  • Clark AG, Wang L. Molecular population genetics of Drosophila immune system genes. Genetics. 1997 Oct;147(2):713–724. [PMC free article] [PubMed]
  • Date A, Satta Y, Takahata N, Chigusa SI. Evolutionary history and mechanism of the Drosophila cecropin gene family. Immunogenetics. 1998 May;47(6):417–429. [PubMed]
  • Dawkins R, Krebs JR. Arms races between and within species. Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):489–511. [PubMed]
  • Fay JC, Wu CI. Hitchhiking under positive Darwinian selection. Genetics. 2000 Jul;155(3):1405–1413. [PMC free article] [PubMed]
  • Fay Justin C, Wyckoff Gerald J, Wu Chung-I. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature. 2002 Feb 28;415(6875):1024–1026. [PubMed]
  • Gillespie JH. Junk ain't what junk does: neutral alleles in a selected context. Gene. 1997 Dec 31;205(1-2):291–299. [PubMed]
  • Gillespie JH. The role of population size in molecular evolution. Theor Popul Biol. 1999 Apr;55(2):145–156. [PubMed]
  • Hasson E, Wang IN, Zeng LW, Kreitman M, Eanes WF. Nucleotide variation in the triosephosphate isomerase (Tpi) locus of Drosophila melanogaster and Drosophila simulans. Mol Biol Evol. 1998 Jun;15(6):756–769. [PubMed]
  • Hueck CJ. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev. 1998 Jun;62(2):379–433. [PMC free article] [PubMed]
  • Hughes AL, Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. [PubMed]
  • Hughes AL, Nei M. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci U S A. 1989 Feb;86(3):958–962. [PMC free article] [PubMed]
  • Akashi H. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA. Genetics. 1995 Feb;139(2):1067–1076. [PMC free article] [PubMed]
  • Hughes AL, Ota T, Nei M. Positive Darwinian selection promotes charge profile diversity in the antigen-binding cleft of class I major-histocompatibility-complex molecules. Mol Biol Evol. 1990 Nov;7(6):515–524. [PubMed]
  • Akashi H. 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):1297–1307. [PMC free article] [PubMed]
  • Kaplan NL, Hudson RR, Langley CH. The "hitchhiking effect" revisited. Genetics. 1989 Dec;123(4):887–899. [PMC free article] [PubMed]
  • Kimbrell DA, Beutler B. The evolution and genetics of innate immunity. Nat Rev Genet. 2001 Apr;2(4):256–267. [PubMed]
  • Schesser K, Spiik AK, Dukuzumuremyi JM, Neurath MF, Pettersson S, Wolf-Watz H. The yopJ locus is required for Yersinia-mediated inhibition of NF-kappaB activation and cytokine expression: YopJ contains a eukaryotic SH2-like domain that is essential for its repressive activity. Mol Microbiol. 1998 Jun;28(6):1067–1079. [PubMed]
  • Kliman RM, Hey J. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex. Genetics. 1993 Feb;133(2):375–387. [PMC free article] [PubMed]
  • Mol A. Readers object to 'anti-natalist' article.. Can Fam Physician. 1982 Jun;28:1067–1067. [PMC free article] [PubMed]
  • Lemaitre B, Reichhart JM, Hoffmann JA. Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms. Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14614–14619. [PMC free article] [PubMed]
  • Silverman N, Maniatis T. NF-kappaB signaling pathways in mammalian and insect innate immunity. Genes Dev. 2001 Sep 15;15(18):2321–2342. [PubMed]
  • Li WH, Wu CI, Luo CC. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes. Mol Biol Evol. 1985 Mar;2(2):150–174. [PubMed]
  • Smith Nick G C, Eyre-Walker Adam. Adaptive protein evolution in Drosophila. Nature. 2002 Feb 28;415(6875):1022–1024. [PubMed]
  • Smith JM, Haigh J. The hitch-hiking effect of a favourable gene. Genet Res. 1974 Feb;23(1):23–35. [PubMed]
  • McDonald JH, Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 1991 Jun 20;351(6328):652–654. [PubMed]
  • Stahl EA, Bishop JG. Plant-pathogen arms races at the molecular level. Curr Opin Plant Biol. 2000 Aug;3(4):299–304. [PubMed]
  • Morton BR. Chloroplast DNA codon use: evidence for selection at the psb A locus based on tRNA availability. J Mol Evol. 1993 Sep;37(3):273–280. [PubMed]
  • Murphy PM. Molecular mimicry and the generation of host defense protein diversity. Cell. 1993 Mar 26;72(6):823–826. [PubMed]
  • Tajima F. Evolutionary relationship of DNA sequences in finite populations. Genetics. 1983 Oct;105(2):437–460. [PMC free article] [PubMed]
  • Takano TS. Rate variation of DNA sequence evolution in the Drosophila lineages. Genetics. 1998 Jun;149(2):959–970. [PMC free article] [PubMed]
  • Tanaka T, Nei M. Positive darwinian selection observed at the variable-region genes of immunoglobulins. Mol Biol Evol. 1989 Sep;6(5):447–459. [PubMed]
  • Przeworski Molly. The signature of positive selection at randomly chosen loci. Genetics. 2002 Mar;160(3):1179–1189. [PMC free article] [PubMed]
  • True JR, Mercer JM, Laurie CC. Differences in crossover frequency and distribution among three sibling species of Drosophila. Genetics. 1996 Feb;142(2):507–523. [PMC free article] [PubMed]
  • Ramos-Onsins S, Aguadé M. Molecular evolution of the Cecropin multigene family in Drosophila. functional genes vs. pseudogenes. Genetics. 1998 Sep;150(1):157–171. [PMC free article] [PubMed]
  • Wright F. The 'effective number of codons' used in a gene. Gene. 1990 Mar 1;87(1):23–29. [PubMed]
  • Rozas J, Rozas R. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics. 1999 Feb;15(2):174–175. [PubMed]

Articles from Genetics are provided here courtesy of Genetics Society of America

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • Gene
    Gene
    Gene links
  • Gene (nucleotide)
    Gene (nucleotide)
    Records in Gene identified from shared sequence links
  • GEO Profiles
    GEO Profiles
    Related GEO records
  • MedGen
    MedGen
    Related information in MedGen
  • Nucleotide
    Nucleotide
    Published Nucleotide sequences
  • Pathways + GO
    Pathways + GO
    Pathways, annotations and biological systems (BioSystems) that cite the current article.
  • PopSet
    PopSet
    Published population set
  • Protein
    Protein
    Published protein sequences
  • PubMed
    PubMed
    PubMed citations for these articles
  • Taxonomy
    Taxonomy
    Related taxonomy entry
  • Taxonomy Tree
    Taxonomy Tree

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...