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PMID: 16322515 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

A scan of molecular variation leads to the narrow localization of a selective sweep affecting both Afrotropical and cosmopolitan populations of Drosophila melanogaster.

Genetics ·Vol. 172 ·No. 2 ·2006-02-00 ·Pages 1093-105

Pool JE, Bauer DuMont V, Mueller JL, Aquadro CF

Abstract

Drosophila melanogaster originated in tropical Africa but has achieved a cosmopolitan distribution in association with human habitation. Cosmopolitan populations of D. melanogaster are known to have reduced genetic variation, particularly on the X chromosome. However, the relative importance of population bottlenecks and selective sweeps in explaining this reduction is uncertain. We surveyed variation at 31 microsatellites across a 330-kb section of the X chromosome located between the white and kirre genes. Two linked clusters of loci were observed with reduced variation and a skew toward rare alleles in both an Ecuador and a Zimbabwe population sample. Examining Zimbabwe DNA sequence polymorphism within one of these regions allowed us to localize a selective sweep to a 361-bp window within the 5' regulatory region of the roughest gene, with one nucleotide substitution representing the best candidate for the target of selection. Estimates of sweep age suggested that this fixation event occurred prior to the expansion of D. melanogaster from sub-Saharan Africa. For both putative sweep regions in our data set, cosmopolitan populations showed wider footprints of selection compared to those in Zimbabwe. This pattern appears consistent with the demographic amplification of preexisting sweep signals due to one or more population bottlenecks.

MeSH Terms
Animals Dinucleotide Repeats Drosophila melanogaster/genetics Ecuador Genetic Variation Genetics, Population Molecular Sequence Data Polymorphism, Genetic Zimbabwe
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Pool John E
Department of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853, USA. jep36@cornell.edu
Bauer DuMont Vanessa
Mueller Jacob L
Aquadro Charles F
References (51)
51 references, click to expand
  1. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.
    Genetics. 1989 Nov;123(3):585-95 PMID: 2513255
  2. Molecular variation at the In(2L)t proximal breakpoint site in natural populations of Drosophila melanogaster and D. simulans.
    Genetics. 2000 Apr;154(4):1681-91 PMID: 10747062
  3. Requirement of the roughest gene for differentiation and time of death of interommatidial cells during pupal stages of Drosophila compound eye development.
    Mech Dev. 2003 May;120(5):537-47 PMID: 12782271
  4. Temporal patterns of fruit fly (Drosophila) evolution revealed by mutation clocks.
    Mol Biol Evol. 2004 Jan;21(1):36-44 PMID: 12949132
  5. Multilocus patterns of nucleotide variability and the demographic and selection history of Drosophila melanogaster populations.
    Genome Res. 2005 Jun;15(6):790-9 PMID: 15930491
  6. The hitch-hiking effect of a favourable gene.
    Genet Res. 1974 Feb;23(1):23-35 PMID: 4407212
  7. Statistical tests of neutrality of mutations.
    Genetics. 1993 Mar;133(3):693-709 PMID: 8454210
  8. Demography and natural selection have shaped genetic variation in Drosophila melanogaster: a multi-locus approach.
    Genetics. 2003 Nov;165(3):1269-78 PMID: 14668381
  9. 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
  10. Analyzing the repressive function of ultraspiracle, the Drosophila RXR, in Drosophila eye development.
    Mech Dev. 2002 Feb;111(1-2):89-98 PMID: 11804781
  11. Inferring the effects of demography and selection on Drosophila melanogaster populations from a chromosome-wide scan of DNA variation.
    Mol Biol Evol. 2005 Oct;22(10):2119-30 PMID: 15987874
  12. Hitchhiking mapping: a population-based fine-mapping strategy for adaptive mutations in Drosophilamelanogaster.
    Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12949-54 PMID: 12351680
  13. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis.
    Bioinformatics. 1999 Feb;15(2):174-5 PMID: 10089204
  14. Inferences about human demography based on multilocus analyses of noncoding sequences.
    Genetics. 2002 Jul;161(3):1209-18 PMID: 12136023
  15. African and North American populations of Drosophila melanogaster are very different at the DNA level.
    Nature. 1993 Oct 7;365(6446):548-50 PMID: 8413609
  16. Power of neutrality tests to detect bottlenecks and hitchhiking.
    J Mol Evol. 2003;57 Suppl 1:S190-200 PMID: 15008416
  17. Non-African populations of Drosophila melanogaster have a unique origin.
    Mol Biol Evol. 2004 Aug;21(8):1482-91 PMID: 15014160
  18. Detecting the footprint of positive selection in a european population of Drosophila melanogaster: multilocus pattern of variation and distance to coding regions.
    Genetics. 2004 Aug;167(4):1759-66 PMID: 15342514
  19. Haldane's sieve and adaptation from the standing genetic variation.
    Genetics. 2001 Feb;157(2):875-84 PMID: 11157004
  20. Detecting a local signature of genetic hitchhiking along a recombining chromosome.
    Genetics. 2002 Feb;160(2):765-77 PMID: 11861577
  21. Maximum-likelihood methods for detecting recent positive selection and localizing the selected site in the genome.
    Genetics. 2005 Sep;171(1):377-84 PMID: 15972464
  22. Estimation of average heterozygosity and genetic distance from a small number of individuals.
    Genetics. 1978 Jul;89(3):583-90 PMID: 17248844
  23. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster.
    Nature. 1983 Aug 4-10;304(5925):412-7 PMID: 6410283
  24. A pseudohitchhiking model of X vs. autosomal diversity.
    Genetics. 2004 Dec;168(4):2261-9 PMID: 15611190
  25. DNA variability and divergence at the notch locus in Drosophila melanogaster and D. simulans: a case of accelerated synonymous site divergence.
    Genetics. 2004 May;167(1):171-85 PMID: 15166145
  26. Identification of regulatory modules mediating specific expression of the roughest gene in Drosophila melanogaster.
    Dev Genes Evol. 2004 Sep;214(9):453-9 PMID: 15278452
  27. 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
  28. Hitchhiking under positive Darwinian selection.
    Genetics. 2000 Jul;155(3):1405-13 PMID: 10880498
  29. Different forces drive the evolution of the Acp26Aa and Acp26Ab accessory gland genes in the Drosophila melanogaster species complex.
    Genetics. 1998 Nov;150(3):1079-89 PMID: 9799260
  30. Reduced natural selection associated with low recombination in Drosophila melanogaster.
    Mol Biol Evol. 1993 Nov;10(6):1239-58 PMID: 8277853
  31. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms.
    Genetics. 1995 Jun;140(2):783-96 PMID: 7498754
  32. 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
  33. A microsatellite-based multilocus screen for the identification of local selective sweeps.
    Genetics. 2002 Feb;160(2):753-63 PMID: 11861576
  34. Approximate Bayesian inference reveals evidence for a recent, severe bottleneck in a Netherlands population of Drosophila melanogaster.
    Genetics. 2006 Mar;172(3):1607-19 PMID: 16299396
  35. Libsequence: a C++ class library for evolutionary genetic analysis.
    Bioinformatics. 2003 Nov 22;19(17):2325-7 PMID: 14630667
  36. Evolutionary inferences from DNA variation at the 6-phosphogluconate dehydrogenase locus in natural populations of drosophila: selection and geographic differentiation.
    Genetics. 1994 Jan;136(1):155-71 PMID: 8138153
  37. A role for ultraspiracle, the Drosophila RXR, in morphogenetic furrow movement and photoreceptor cluster formation.
    Development. 1997 Jul;124(13):2499-506 PMID: 9216992
  38. Estimating the time since the fixation of a beneficial allele.
    Genetics. 2003 Aug;164(4):1667-76 PMID: 12930770
  39. A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population.
    Genet Res. 1973 Oct;22(2):201-4 PMID: 4777279
  40. Evidence of a high rate of selective sweeps in African Drosophila melanogaster.
    Genetics. 2003 Feb;163(2):599-609 PMID: 12618399
  41. Chromosomal patterns of microsatellite variability contrast sharply in African and non-African populations of Drosophila melanogaster.
    Genetics. 2002 Jan;160(1):247-56 PMID: 11805060
  42. Genetic variation of Drosophila melanogaster natural populations.
    Trends Genet. 1988 Apr;4(4):106-11 PMID: 3149056
  43. Distinguishing between selective sweeps and demography using DNA polymorphism data.
    Genetics. 2005 Jul;170(3):1401-10 PMID: 15911584
  44. Multiple signatures of positive selection downstream of notch on the X chromosome in Drosophila melanogaster.
    Genetics. 2005 Oct;171(2):639-53 PMID: 16020794
  45. Properties of statistical tests of neutrality for DNA polymorphism data.
    Genetics. 1995 Sep;141(1):413-29 PMID: 8536987
  46. Evidence for a selective sweep in the wapl region of Drosophila melanogaster.
    Genetics. 2006 Jan;172(1):265-74 PMID: 16204208
  47. SelSim: a program to simulate population genetic data with natural selection and recombination.
    Bioinformatics. 2004 Dec 12;20(18):3673-5 PMID: 15271777
  48. MatInspector and beyond: promoter analysis based on transcription factor binding sites.
    Bioinformatics. 2005 Jul 1;21(13):2933-42 PMID: 15860560
  49. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data.
    Genetics. 1996 Dec;144(4):2001-14 PMID: 8978083
  50. Generating samples under a Wright-Fisher neutral model of genetic variation.
    Bioinformatics. 2002 Feb;18(2):337-8 PMID: 11847089
  51. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations.
    Genetics. 1991 Oct;129(2):555-62 PMID: 1743491
Article Info
Journal
Genetics
Abbr.
Genetics
ISSN
0016-6731
DOI
10.1534/genetics.105.049973
Email
jep36@cornell.edu
Published
2006-02-00
Epub
2005-00-01
Pages
1093-105
Language
English
Region
United States
NLM ID
0374636
PMCID
PMC1456208
Subset
IM
Grants
NIGMS NIH HHS · R01 GM036431 · United States
NIGMS NIH HHS · GM36431 · United States
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PubMed source DOI: 10.1534/genetics.105.049973 PMC Full Text View journal details
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