Home LiteratureArticle Details
PMID: 12930753 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Natural selection drives Drosophila immune system evolution.

Genetics ·Vol. 164 ·No. 4 ·2003-08-00 ·Pages 1471-80

Schlenke TA, Begun DJ

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.

MeSH Terms
Animals Chromosomes Codon Drosophila/genetics,immunology Evolution, Molecular Female Gene Frequency Genes, Insect Genetic Linkage Haplotypes Heterozygote Immune System Molecular Sequence Data Mutation Polymorphism, Genetic Selection, Genetic Species Specificity X Chromosome
Chemicals
Codon
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Schlenke Todd A
Section of Evolution and Ecology, Division of Biological Sciences, Storer Hall, University of California, Davis, CA 95616, USA. [email protected]
Begun David J
References (47)
47 references, click to expand
  1. Arms races between and within species.
    Proc R Soc Lond B Biol Sci. 1979 Sep 21;205(1161):489-511 PMID: 42057
  2. The hitch-hiking effect of a favourable gene.
    Genet Res. 1974 Feb;23(1):23-35 PMID: 4407212
  3. 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):150-74 PMID: 3916709
  4. A conserved signaling pathway: the Drosophila toll-dorsal pathway.
    Annu Rev Cell Dev Biol. 1996;12:393-416 PMID: 8970732
  5. Testing the neutral theory of molecular evolution with genomic data from Drosophila.
    Nature. 2002 Feb 28;415(6875):1024-6 PMID: 11875569
  6. Adaptive protein evolution in Drosophila.
    Nature. 2002 Feb 28;415(6875):1022-4 PMID: 11875568
  7. Protein variation in Drosophila simulans, and comparison of genes from centromeric versus noncentromeric regions of chromosome 3.
    Mol Biol Evol. 2002 Feb;19(2):201-3 PMID: 11801748
  8. NF-kappaB signaling pathways in mammalian and insect innate immunity.
    Genes Dev. 2001 Sep 15;15(18):2321-42 PMID: 11562344
  9. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA.
    Genetics. 1995 Feb;139(2):1067-76 PMID: 7713409
  10. Plant-pathogen arms races at the molecular level.
    Curr Opin Plant Biol. 2000 Aug;3(4):299-304 PMID: 10873849
  11. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis.
    Bioinformatics. 1999 Feb;15(2):174-5 PMID: 10089204
  12. Adaptive protein evolution at the Adh locus in Drosophila.
    Nature. 1991 Jun 20;351(6328):652-4 PMID: 1904993
  13. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster.
    Nature. 1992 Apr 9;356(6369):519-20 PMID: 1560824
  14. The role of population size in molecular evolution.
    Theor Popul Biol. 1999 Apr;55(2):145-56 PMID: 10329514
  15. 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):5322-7 PMID: 10805791
  16. Type III protein secretion systems in bacterial pathogens of animals and plants.
    Microbiol Mol Biol Rev. 1998 Jun;62(2):379-433 PMID: 9618447
  17. Rate variation of DNA sequence evolution in the Drosophila lineages.
    Genetics. 1998 Jun;149(2):959-70 PMID: 9611206
  18. Positive darwinian selection observed at the variable-region genes of immunoglobulins.
    Mol Biol Evol. 1989 Sep;6(5):447-59 PMID: 2796726
  19. Nucleotide variation in the triosephosphate isomerase (Tpi) locus of Drosophila melanogaster and Drosophila simulans.
    Mol Biol Evol. 1998 Jun;15(6):756-69 PMID: 9615457
  20. Rates of DNA sequence evolution are not sex-biased in Drosophila melanogaster and D. simulans.
    Mol Biol Evol. 1997 Dec;14(12):1252-7 PMID: 9402735
  21. Adaptive evolution of relish, a Drosophila NF-kappaB/IkappaB protein.
    Genetics. 2000 Mar;154(3):1231-8 PMID: 10757765
  22. The effect of deleterious mutations on neutral molecular variation.
    Genetics. 1993 Aug;134(4):1289-303 PMID: 8375663
  23. DNA sequence variation at the period locus within and among species of the Drosophila melanogaster complex.
    Genetics. 1993 Feb;133(2):375-87 PMID: 8436278
  24. Evolutionary relationship of DNA sequences in finite populations.
    Genetics. 1983 Oct;105(2):437-60 PMID: 6628982
  25. Contrasting patterns of X-linked and autosomal nucleotide variation in Drosophila melanogaster and Drosophila simulans.
    Mol Biol Evol. 2001 Mar;18(3):279-90 PMID: 11230529
  26. Hitchhiking under positive Darwinian selection.
    Genetics. 2000 Jul;155(3):1405-13 PMID: 10880498
  27. The evolution and genetics of innate immunity.
    Nat Rev Genet. 2001 Apr;2(4):256-67 PMID: 11283698
  28. The frequency distribution of nucleotide variation in Drosophila simulans.
    Mol Biol Evol. 2001 Jul;18(7):1343-52 PMID: 11420372
  29. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms.
    Genetics. 1995 Jun;140(2):783-96 PMID: 7498754
  30. The "hitchhiking effect" revisited.
    Genetics. 1989 Dec;123(4):887-99 PMID: 2612899
  31. The signature of positive selection at randomly chosen loci.
    Genetics. 2002 Mar;160(3):1179-89 PMID: 11901132
  32. 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
  33. 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):14614-9 PMID: 9405661
  34. Reduced X-linked nucleotide polymorphism in Drosophila simulans.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):5960-5 PMID: 10823947
  35. The 'effective number of codons' used in a gene.
    Gene. 1990 Mar 1;87(1):23-9 PMID: 2110097
  36. Molecular evolution of the Cecropin multigene family in Drosophila. functional genes vs. pseudogenes.
    Genetics. 1998 Sep;150(1):157-71 PMID: 9725836
  37. Evolutionary history and mechanism of the Drosophila cecropin gene family.
    Immunogenetics. 1998 May;47(6):417-29 PMID: 9553148
  38. Molecular population genetics of Drosophila immune system genes.
    Genetics. 1997 Oct;147(2):713-24 PMID: 9335607
  39. 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):1067-79 PMID: 9680199
  40. Readers object to 'anti-natalist' article..
    Can Fam Physician. 1982 Jun;28:1067 PMID: 21286156
  41. 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):515-24 PMID: 2283951
  42. Differences in crossover frequency and distribution among three sibling species of Drosophila.
    Genetics. 1996 Feb;142(2):507-23 PMID: 8852849
  43. Chloroplast DNA codon use: evidence for selection at the psb A locus based on tRNA availability.
    J Mol Evol. 1993 Sep;37(3):273-80 PMID: 8230251
  44. Molecular mimicry and the generation of host defense protein diversity.
    Cell. 1993 Mar 26;72(6):823-6 PMID: 8458078
  45. Junk ain't what junk does: neutral alleles in a selected context.
    Gene. 1997 Dec 31;205(1-2):291-9 PMID: 9461403
  46. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection.
    Nature. 1988 Sep 8;335(6186):167-70 PMID: 3412472
  47. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection.
    Proc Natl Acad Sci U S A. 1989 Feb;86(3):958-62 PMID: 2492668
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
Published
2003-08-00
Pages
1471-80
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1462669
Subset
IM
Grants
NIGMS NIH HHS · GM 55298 · United States
Databases
GENBANK
AF544231, AF544232, AF544233, AF544234, AF544235, AF544236, AF544237, AF544238, AF544239, AY349649, AY349650, AY349651, AY349652, AY349653, AY349654, AY349655, AY349656, AY349657, AY349658, AY349659, AY349660, AY349661, AY349662, AY349663, AY349664, AY349665, AY349666, AY349667, AY349668, AY349669, AY349670, AY349671, AY349672, AY349673, AY349674, AY349675, AY349684, AY349685, AY349686, AY349687, AY349688, AY349689, AY349690, AY349691, AY349692, AY349693, AY349694, AY349695, AY349696, AY349697, AY349698, AY349699, AY349700, AY349701, AY349702, AY349703, AY349704, AY349705, AY349706, AY349707, AY349708, AY349709, AY349710, AY349711, AY349712, AY349713, AY349714, AY349715, AY349716, AY349717, AY349718, AY349719, AY349720, AY349721, AY349722, AY349723, AY349724, AY349725, AY349726, AY349727, AY349728, AY349729, AY349730, AY349731, AY349732, AY349733, AY349734, AY349735, AY349736, AY349745, AY349746, AY349747, AY349748, AY349749, AY349750, AY349751, AY349752, AY349761, AY349762, AY349763, AY349764, AY349765, AY349766, AY349767, AY349768, AY349769, AY349770, AY349771, AY349772, AY349773, AY349774, AY349775, AY349776, AY349777, AY349778, AY349779, AY349780, AY349781, AY349782, AY349783, AY349784, AY349785, AY349786, AY349787, AY349788, AY349789, AY349790, AY349791, AY349792, AY349793, AY349794, AY349795, AY349796, AY349797, AY349798, AY349799, AY349800, AY349801, AY349802, AY349803, AY349804, AY349805, AY349806, AY349807, AY349808, AY349809, AY349810, AY349811, AY349812, AY349813, AY349814, AY349815, AY349816, AY349817, AY349818, AY349819, AY349820, AY349821, AY349822, AY349823, AY349824, AY349825, AY349826, AY349827, AY349828, AY349829, AY349830, AY349831, AY349832, AY349833, AY349834, AY349835, AY349836, AY349837, AY349838, AY349839, AY349840, AY349841, AY349842, AY349843, AY349844, AY349845, AY349846, AY349847, AY349848, AY349849, AY349850, AY349851, AY349852, AY349853, AY349854, AY349855, AY349856, AY349857, AY349858, AY349859, AY349860, AY349861, AY349862, AY349863, AY349864, AY349865, AY349866, AY349867, AY349868, AY349869, AY349870, AY349871, AY349872, AY349873, AY349874, AY349875, AY349876, AY349877, AY349878, AY349879, AY349880, AY349881, AY349882, AY349883, AY349884, AY349885, AY349886, AY349887, AY349888, AY349889, AY349890, AY349891, AY349892, AY349893, AY349894, AY349895, AY349896, AY349897, AY349898, AY349899, AY349900, AY349901, AY349902, AY349903, AY349904, AY349905, AY349906, AY349907, AY349908, AY349909, AY349910, AY349911, AY349912, AY349913, AY349914, AY349915, AY349916, AY349917, AY349918, AY349919, AY349920, AY349921, AY349922, AY349923, AY349924, AY349925, AY349926, AY349927, AY349928, AY349929, AY349930, AY349931, AY349932, AY352227, AY352228, AY352229, AY352230, AY352231, AY352232, AY352233, AY352234, AY352235, AY352236, AY352237, AY352238, AY352239, AY352240, AY352241, AY352242, AY352243, AY352244, AY352245, AY352246, AY352247, AY352248, AY352249, AY352250, AY352251, AY352252, AY352253, AY352254, AY352255, AY352256, AY352257, AY352258, AY352259, AY352260, AY352261, AY352262, AY352263, AY352264, AY352265, AY354407, AY354408, AY354409, AY354410, AY354411, AY354412, AY354413, AY354414, AY354415, AY354416, AY354417, AY354418, AY354419, AY354420, AY354421, AY354422, AY354423, AY354424, AY354425, AY354426, AY354427, AY354428, AY354429, AY354430, AY354431, AY354432, AY354433, AY354434, AY354435, AY354436, AY354437, AY354438, AY354439, AY354440, AY354441, AY354442, AY354443, AY354444, AY354445, AY354446, AY354447, AY354448, AY354449, AY354450, AY354451, AY354452, AY354453, AY354454
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]