Home LiteratureArticle Details
PMID: 17988176 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans.

PLoS biology ·Vol. 5 ·No. 11 ·2007-11-06 ·Pages e310

Begun DJ, Holloway AK, Stevens K, Hillier LW, Poh YP, Hahn MW, Nista PM, Jones CD, Kern AD, Dewey CN, Pachter L, Myers E, Langley CH

Abstract

The population genetic perspective is that the processes shaping genomic variation can be revealed only through simultaneous investigation of sequence polymorphism and divergence within and between closely related species. Here we present a population genetic analysis of Drosophila simulans based on whole-genome shotgun sequencing of multiple inbred lines and comparison of the resulting data to genome assemblies of the closely related species, D. melanogaster and D. yakuba. We discovered previously unknown, large-scale fluctuations of polymorphism and divergence along chromosome arms, and significantly less polymorphism and faster divergence on the X chromosome. We generated a comprehensive list of functional elements in the D. simulans genome influenced by adaptive evolution. Finally, we characterized genomic patterns of base composition for coding and noncoding sequence. These results suggest several new hypotheses regarding the genetic and biological mechanisms controlling polymorphism and divergence across the Drosophila genome, and provide a rich resource for the investigation of adaptive evolution and functional variation in D. simulans.

MeSH Terms
Animals Chromosome Mapping Drosophila/classification,genetics Drosophila Proteins/genetics Evolution, Molecular Genetic Variation Genetics, Population Genome, Insect Genomics Linkage Disequilibrium Models, Genetic Molecular Sequence Data Polymorphism, Genetic X Chromosome
Chemicals
Drosophila Proteins
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Begun David J
Department of Evolution and Ecology, University of California Davis, Davis, California, United States of America. [email protected]
Holloway Alisha K
Stevens Kristian
Hillier Ladeana W
Poh Yu-Ping
Hahn Matthew W
Nista Phillip M
Jones Corbin D
Kern Andrew D
Dewey Colin N
Pachter Lior
Myers Eugene
Langley Charles H
References (125)
125 references, click to expand
  1. The effect of deleterious mutations on neutral molecular variation.
    Genetics. 1993 Aug;134(4):1289-303 PMID: 8375663
  2. Intron length evolution in Drosophila.
    Mol Biol Evol. 2006 Nov;23(11):2203-13 PMID: 16923822
  3. The genomic rate of adaptive amino acid substitution in Drosophila.
    Mol Biol Evol. 2004 Jul;21(7):1350-60 PMID: 15044594
  4. Multiple apoptotic caspase cascades are required in nonapoptotic roles for Drosophila spermatid individualization.
    PLoS Biol. 2004 Jan;2(1):E15 PMID: 14737191
  5. Effects of linkage on rates of molecular evolution.
    Proc Natl Acad Sci U S A. 1988 Sep;85(17):6414-8 PMID: 3413105
  6. Synonymous codon usage in Drosophila melanogaster: natural selection and translational accuracy.
    Genetics. 1994 Mar;136(3):927-35 PMID: 8005445
  7. Inferring weak selection from patterns of polymorphism and divergence at "silent" sites in Drosophila DNA.
    Genetics. 1995 Feb;139(2):1067-76 PMID: 7713409
  8. Intraspecific and interspecific variation at the y-ac-sc region of Drosophila simulans and Drosophila melanogaster.
    Genetics. 1992 Apr;130(4):805-16 PMID: 1582559
  9. Microsatellite variation and differentiation in African and non-African populations of Drosophila simulans.
    Mol Ecol. 2006 Nov;15(13):3895-905 PMID: 17054491
  10. The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts.
    J Invertebr Pathol. 1993 May;61(3):226-30 PMID: 7689622
  11. Estimating the recombination parameter of a finite population model without selection.
    Genet Res. 1987 Dec;50(3):245-50 PMID: 3443297
  12. Chromosome-wide gene-specific targeting of the Drosophila dosage compensation complex.
    Genes Dev. 2006 Apr 1;20(7):858-70 PMID: 16547172
  13. Adaptive protein evolution at the Adh locus in Drosophila.
    Nature. 1991 Jun 20;351(6328):652-4 PMID: 1904993
  14. Widespread adaptive evolution of Drosophila genes with sex-biased expression.
    Genetics. 2006 Oct;174(2):893-900 PMID: 16951084
  15. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA.
    J Mol Evol. 1985;22(2):160-74 PMID: 3934395
  16. The genetics and genomics of insecticide resistance.
    Trends Genet. 2004 Mar;20(3):163-70 PMID: 15036810
  17. Reduced X-linked nucleotide polymorphism in Drosophila simulans.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):5960-5 PMID: 10823947
  18. Hitchhiking under positive Darwinian selection.
    Genetics. 2000 Jul;155(3):1405-13 PMID: 10880498
  19. PVF1/PVR signaling and apoptosis promotes the rotation and dorsal closure of the Drosophila male terminalia.
    Int J Dev Biol. 2004 Dec;48(10):1087-94 PMID: 15602694
  20. GC-biased segregation of noncoding polymorphisms in Drosophila.
    Genetics. 2006 Jan;172(1):221-8 PMID: 16157668
  21. The hitchhiking effect on linkage disequilibrium between linked neutral loci.
    Genetics. 2006 Apr;172(4):2647-63 PMID: 16452153
  22. Natural selection drives Drosophila immune system evolution.
    Genetics. 2003 Aug;164(4):1471-80 PMID: 12930753
  23. Protein interaction mapping: a Drosophila case study.
    Genome Res. 2005 Mar;15(3):376-84 PMID: 15710747
  24. Coordination of replication and transcription along a Drosophila chromosome.
    Genes Dev. 2004 Dec 15;18(24):3094-105 PMID: 15601823
  25. The correlation between intron length and recombination in drosophila. Dynamic equilibrium between mutational and selective forces.
    Genetics. 2000 Nov;156(3):1175-90 PMID: 11063693
  26. Intraspecific nuclear DNA variation in Drosophila.
    Mol Biol Evol. 1996 Jan;13(1):261-77 PMID: 8583899
  27. MAVID: constrained ancestral alignment of multiple sequences.
    Genome Res. 2004 Apr;14(4):693-9 PMID: 15060012
  28. Expression pattern and, surprisingly, gene length shape codon usage in Caenorhabditis, Drosophila, and Arabidopsis.
    Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4482-7 PMID: 10200288
  29. X-linked genes evolve higher codon bias in Drosophila and Caenorhabditis.
    Genetics. 2005 Sep;171(1):145-55 PMID: 15965246
  30. Direct estimation of per nucleotide and genomic deleterious mutation rates in Drosophila.
    Nature. 2007 Jan 4;445(7123):82-5 PMID: 17203060
  31. Molecular population genetics of the distal portion of the X chromosome in Drosophila: evidence for genetic hitchhiking of the yellow-achaete region.
    Genetics. 1991 Dec;129(4):1147-58 PMID: 1664405
  32. Relationships within the melanogaster species subgroup of the genus Drosophila (Sophophora). II. Phylogenetic relationships between six species based upon polytene chromosome banding sequences.
    Proc R Soc Lond B Biol Sci. 1976 May 18;193(1112):275-94 PMID: 6967
  33. Reduced variation in the yellow-achaete-scute region in natural populations of Drosophila melanogaster.
    Genetics. 1989 Jul;122(3):607-15 PMID: 17246506
  34. Patterns of microsatellite variability among X chromosomes and autosomes indicate a high frequency of beneficial mutations in non-African D. simulans.
    Mol Biol Evol. 2004 Jul;21(7):1384-90 PMID: 15044592
  35. The JIL-1 kinase regulates the structure of Drosophila polytene chromosomes.
    Chromosoma. 2005 Aug;114(3):173-82 PMID: 15986206
  36. The selection-mutation-drift theory of synonymous codon usage.
    Genetics. 1991 Nov;129(3):897-907 PMID: 1752426
  37. Contrasting patterns of geographic variation in the cosmopolitan sibling species Drosophila melanogaster and Drosophila simulans.
    Biochem Genet. 1987 Feb;25(1-2):27-40 PMID: 3107542
  38. A test for faster X evolution in Drosophila.
    Mol Biol Evol. 2002 Oct;19(10):1816-9 PMID: 12270910
  39. Population structure among African and derived populations of Drosophila simulans: evidence for ancient subdivision and recent admixture.
    Genetics. 1999 Sep;153(1):305-17 PMID: 10471714
  40. Substitution rates in Drosophila nuclear genes: implications for translational selection.
    Genetics. 2001 Jan;157(1):295-305 PMID: 11139510
  41. 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
  42. The coalescent process and background selection.
    Philos Trans R Soc Lond B Biol Sci. 1995 Jul 29;349(1327):19-23 PMID: 8748015
  43. Interactions between natural selection, recombination and gene density in the genes of Drosophila.
    Genetics. 2002 Feb;160(2):595-608 PMID: 11861564
  44. Chromosomal sites necessary for normal levels of meiotic recombination in Drosophila melanogaster. I. Evidence for and mapping of the sites.
    Genetics. 1980 Mar;94(3):625-46 PMID: 6772522
  45. Identification of chromosome inheritance modifiers in Drosophila melanogaster.
    Genetics. 2001 Apr;157(4):1623-37 PMID: 11290718
  46. The frequency distribution of nucleotide variation in Drosophila simulans.
    Mol Biol Evol. 2001 Jul;18(7):1343-52 PMID: 11420372
  47. Genome-wide DNA replication profile for Drosophila melanogaster: a link between transcription and replication timing.
    Nat Genet. 2002 Nov;32(3):438-42 PMID: 12355067
  48. High-resolution ChIP-chip analysis reveals that the Drosophila MSL complex selectively identifies active genes on the male X chromosome.
    Genes Dev. 2006 Apr 1;20(7):848-57 PMID: 16547173
  49. Proceedings of the SMBE Tri-National Young Investigators' Workshop 2005. Accurate inference and estimation in population genomics.
    Mol Biol Evol. 2006 May;23(5):911-8 PMID: 16407459
  50. Patterns of intron sequence evolution in Drosophila are dependent upon length and GC content.
    Genome Biol. 2005;6(8):R67 PMID: 16086849
  51. GENETIC BASIS OF DIFFERENCES IN GENITAL MORPHOLOGY AMONG THREE SIBLING SPECIES OF DROSOPHILA.
    Evolution. 1983 Nov;37(6):1101-1118 PMID: 28556010
  52. Evolution on the X chromosome: unusual patterns and processes.
    Nat Rev Genet. 2006 Aug;7(8):645-53 PMID: 16847464
  53. ReAligner: a program for refining DNA sequence multi-alignments.
    J Comput Biol. 1997 Fall;4(3):369-83 PMID: 9278066
  54. Genomic effects of nucleotide substitutions in Drosophila simulans.
    Genetics. 2002 Dec;162(4):1753-61 PMID: 12524346
  55. Dosage compensation rox!
    Curr Opin Cell Biol. 2000 Jun;12(3):351-4 PMID: 10801462
  56. Inference of positive and negative selection on the 5' regulatory regions of Drosophila genes.
    Mol Biol Evol. 2004 Feb;21(2):374-83 PMID: 14660692
  57. The Bioperl toolkit: Perl modules for the life sciences.
    Genome Res. 2002 Oct;12(10):1611-8 PMID: 12368254
  58. Natural variation in Drosophila melanogaster diapause due to the insulin-regulated PI3-kinase.
    Proc Natl Acad Sci U S A. 2006 Oct 24;103(43):15911-5 PMID: 17043223
  59. Levels of naturally occurring DNA polymorphism correlate with recombination rates in D. melanogaster.
    Nature. 1992 Apr 9;356(6369):519-20 PMID: 1560824
  60. Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination.
    Genetics. 1999 Jan;151(1):221-38 PMID: 9872962
  61. A test of neutral molecular evolution based on nucleotide data.
    Genetics. 1987 May;116(1):153-9 PMID: 3110004
  62. Reduced variation at concertina, a heterochromatic locus in Drosophila.
    Genet Res. 1996 Oct;68(2):101-8 PMID: 8940899
  63. Ubiquitous selective constraints in the Drosophila genome revealed by a genome-wide interspecies comparison.
    Genome Res. 2006 Jul;16(7):875-84 PMID: 16751341
  64. Offsetting effects of Wolbachia infection and heat shock on sperm production in Drosophila simulans: analyses of fecundity, fertility and accessory gland proteins.
    Genetics. 2000 May;155(1):167-78 PMID: 10790392
  65. X-chromosome-wide profiling of MSL-1 distribution and dosage compensation in Drosophila.
    Genes Dev. 2006 Apr 1;20(7):871-83 PMID: 16547175
  66. PKD2 cation channel is required for directional sperm movement and male fertility.
    Curr Biol. 2003 Dec 16;13(24):2175-8 PMID: 14680633
  67. Positive selection drives the evolution of rhino, a member of the heterochromatin protein 1 family in Drosophila.
    PLoS Genet. 2005 Jul;1(1):96-108 PMID: 16103923
  68. Molecular variation at the vermilion locus in geographically diverse populations of Drosophila melanogaster and D. simulans.
    Genetics. 1995 Jul;140(3):1019-32 PMID: 7672574
  69. Gene expression during the life cycle of Drosophila melanogaster.
    Science. 2002 Sep 27;297(5590):2270-5 PMID: 12351791
  70. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.
    Mol Biol Evol. 1986 Sep;3(5):418-26 PMID: 3444411
  71. Models of nearly neutral mutations with particular implications for nonrandom usage of synonymous codons.
    J Mol Evol. 1987;24(4):337-45 PMID: 3110426
  72. Mating-responsive genes in reproductive tissues of female Drosophila melanogaster.
    Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10358-10363 PMID: 16798875
  73. Association between divergence and interspersed repeats in mammalian noncoding genomic DNA.
    Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14503-8 PMID: 11717405
  74. PCAP: a whole-genome assembly program.
    Genome Res. 2003 Sep;13(9):2164-70 PMID: 12952883
  75. Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans.
    Mol Biol Evol. 1996 Jul;13(6):735-48 PMID: 8754210
  76. The relationship of protein conservation and sequence length.
    BMC Evol Biol. 2002 Nov 1;2:20 PMID: 12410938
  77. Adaptive evolution of non-coding DNA in Drosophila.
    Nature. 2005 Oct 20;437(7062):1149-52 PMID: 16237443
  78. A superfamily of Drosophila satellite related (SR) DNA repeats restricted to the X chromosome euchromatin.
    Nucleic Acids Res. 1992 Mar 11;20(5):1113-6 PMID: 1549474
  79. Nuclear pore components are involved in the transcriptional regulation of dosage compensation in Drosophila.
    Mol Cell. 2006 Mar 17;21(6):811-23 PMID: 16543150
  80. Linkage disequilibrium and recent selection at three immunity receptor loci in Drosophila simulans.
    Genetics. 2005 Apr;169(4):2013-22 PMID: 15654108
  81. Patterns of polymorphism and divergence from noncoding sequences of Drosophila melanogaster and D. simulans: evidence for nonequilibrium processes.
    Mol Biol Evol. 2005 Jan;22(1):51-62 PMID: 15456897
  82. Lack of polymorphism on the Drosophila fourth chromosome resulting from selection.
    Genetics. 1991 Dec;129(4):1111-7 PMID: 1686006
  83. Molecular signatures of natural selection.
    Annu Rev Genet. 2005;39:197-218 PMID: 16285858
  84. A microsatellite variability screen for positive selection associated with the "out of Africa" habitat expansion of Drosophila melanogaster.
    Genetics. 2003 Nov;165(3):1137-48 PMID: 14668371
  85. The effect of linkage on limits to artificial selection.
    Genet Res. 1966 Dec;8(3):269-94 PMID: 5980116
  86. High rate of DNA loss in the Drosophila melanogaster and Drosophila virilis species groups.
    Mol Biol Evol. 1998 Mar;15(3):293-302 PMID: 9501496
  87. PAML: a program package for phylogenetic analysis by maximum likelihood.
    Comput Appl Biosci. 1997 Oct;13(5):555-6 PMID: 9367129
  88. Synthesis of ribonucleic acid by the X-chromosomes of Drosophila melanogaster and the problem of dosage compensation.
    Nature. 1965 Aug 14;207(998):785-6 PMID: 5885936
  89. BLAT--the BLAST-like alignment tool.
    Genome Res. 2002 Apr;12(4):656-64 PMID: 11932250
  90. Recombination, dominance and selection on amino acid polymorphism in the Drosophila genome: contrasting patterns on the X and fourth chromosomes.
    Genetics. 2003 Nov;165(3):1195-208 PMID: 14668375
  91. A survey of ovary-, testis-, and soma-biased gene expression in Drosophila melanogaster adults.
    Genome Biol. 2004;5(6):R40 PMID: 15186491
  92. Fine-scale crossover rate heterogeneity in Drosophila pseudoobscura.
    J Mol Evol. 2007 Jan;64(1):129-35 PMID: 17160365
  93. Adaptive protein evolution in Drosophila.
    Nature. 2002 Feb 28;415(6875):1022-4 PMID: 11875568
  94. Linkage disequilibrium as a signature of selective sweeps.
    Genetics. 2004 Jul;167(3):1513-24 PMID: 15280259
  95. A new family of adenylyl cyclase genes in the male germline of Drosophila melanogaster.
    Dev Genes Evol. 2000 Apr;210(4):200-6 PMID: 11180822
  96. 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
  97. The "hitchhiking effect" revisited.
    Genetics. 1989 Dec;123(4):887-99 PMID: 2612899
  98. Linking phylogenetics with population genetics to reconstruct the geographic origin of a species.
    Mol Phylogenet Evol. 2004 Sep;32(3):998-1009 PMID: 15288072
  99. Lack of correlation between interspecific divergence and intraspecific polymorphism at the suppressor of forked region in Drosophila melanogaster and Drosophila simulans.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):1800-3 PMID: 8095333
  100. The sex-ratio trait in Drosophila simulans: genetic analysis of distortion and suppression.
    Genetics. 1997 Oct;147(2):635-42 PMID: 9335600
  101. Adaptive evolution of Cid, a centromere-specific histone in Drosophila.
    Genetics. 2001 Mar;157(3):1293-8 PMID: 11238413
  102. Codon bias and noncoding GC content correlate negatively with recombination rate on the Drosophila X chromosome.
    J Mol Evol. 2005 Sep;61(3):315-24 PMID: 16044248
  103. Adaptive genic evolution in the Drosophila genomes.
    Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2271-6 PMID: 17284599
  104. X chromosomes and autosomes evolve at similar rates in Drosophila: no evidence for faster-X protein evolution.
    Genome Res. 2006 Apr;16(4):498-504 PMID: 16520459
  105. A protein interaction map of Drosophila melanogaster.
    Science. 2003 Dec 5;302(5651):1727-36 PMID: 14605208
  106. Global analysis of X-chromosome dosage compensation.
    J Biol. 2006;5(1):3 PMID: 16507155
  107. Deleterious background selection with recombination.
    Genetics. 1995 Dec;141(4):1605-17 PMID: 8601498
  108. Mitochondrial DNA variability in Drosophila simulans: quasi absence of polymorphism within each of the three cytoplasmic races.
    Heredity (Edinb). 1988 Dec;61 ( Pt 3):419-26 PMID: 2906636
  109. Sperm-female coevolution in Drosophila.
    Science. 2002 Nov 8;298(5596):1230-3 PMID: 12424377
  110. Multilocus Structure of Natural Populations of HORDEUM SPONTANEUM.
    Genetics. 1980 Oct;96(2):523-36 PMID: 17249067
  111. The signature of positive selection on standing genetic variation.
    Evolution. 2005 Nov;59(11):2312-23 PMID: 16396172
  112. Cloning of DNA sequences from the white locus of D. melanogaster by a novel and general method.
    Cell. 1981 Sep;25(3):693-704 PMID: 6269753
  113. A test for adaptive change in DNA sequences controlling transcription.
    Proc Biol Sci. 1995 Aug 22;261(1361):203-7 PMID: 7568273
  114. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution.
    Nature. 1996 May 16;381(6579):232-4 PMID: 8622764
  115. The hitch-hiking effect of a favourable gene.
    Genet Res. 1974 Feb;23(1):23-35 PMID: 4407212
  116. Pervasive adaptive evolution among interactors of the Drosophila hybrid inviability gene, Nup96.
    Mol Biol Evol. 2007 Jan;24(1):306-14 PMID: 17056646
  117. Molecular population genetics of Xdh and the evolution of base composition in Drosophila.
    Genetics. 2002 Dec;162(4):1725-35 PMID: 12524344
  118. A flagellar polycystin-2 homolog required for male fertility in Drosophila.
    Curr Biol. 2003 Dec 16;13(24):2179-84 PMID: 14680634
  119. SAGA unveiled.
    Trends Biochem Sci. 2005 Jan;30(1):7-10 PMID: 15653319
  120. The correlation between synonymous and nonsynonymous substitutions in Drosophila: mutation, selection or relaxed constraints?
    Genetics. 1998 Oct;150(2):767-75 PMID: 9755207
  121. Strong selective sweep associated with a transposon insertion in Drosophila simulans.
    Proc Natl Acad Sci U S A. 2004 Feb 10;101(6):1626-31 PMID: 14745026
  122. Contrasted polymorphism patterns in a large sample of populations from the evolutionary genetics model Drosophila simulans.
    Genetics. 2006 Jun;173(2):759-67 PMID: 16510794
  123. Regulation of gene expression by alternative untranslated regions.
    Trends Genet. 2006 Mar;22(3):119-22 PMID: 16430990
  124. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection.
    Genetics. 2004 Nov;168(3):1457-65 PMID: 15579698
  125. Analysis of a shift in codon usage in Drosophila.
    J Mol Evol. 2003;57 Suppl 1:S214-25 PMID: 15008418
Article Info
Journal
PLoS biology
Abbr.
PLoS Biol
ISSN
1545-7885
Published
2007-11-06
Pages
e310
Language
English
Region
United States
NLM ID
101183755
PMCID
PMC2062478
Subset
IM
Grants
NHGRI NIH HHS · R01 HG002942 · United States
NHGRI NIH HHS · R01HG2107-3 · United States
NIGMS NIH HHS · R01 GM071926 · United States
NHGRI NIH HHS · R01-HG02362-03 · United States
NHGRI NIH HHS · R01 HG002107 · United States
NHGRI NIH HHS · HG02942-01A1 · United States
NHGRI NIH HHS · R01 HG002362 · United States
Databases
GENBANK
AAEU01000000
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]