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The Role of Natural Selection in Genetic Differentiation of Worldwide Populations of Drosophila ananassae

John F. Baines, Aparup Das, Sylvain Mousset and Wolfgang Stephan
Genetics December 1, 2004 vol. 168 no. 4 1987-1998; https://doi.org/10.1534/genetics.104.027482
John F. Baines
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Aparup Das
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Sylvain Mousset
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Wolfgang Stephan
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Article Figures & Data

Figures

  • Tables
  • Figure 1.—
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    Figure 1.—

    Restriction map of furrowed and location of the region sequenced in this study. R1–R42 are EcoRI restriction fragments described by Chen et al. (2000). The R1 fragment covers part of the 5′-untranslated region (UTR) and exons 1–9; R9/R42 covers exon 12, the 3′-UTR, and 3′ flanking region. A 5.1-kb region (1.2 kb of R1 and 3.9 kb of R9 and R42) corresponding to the 5.7-kb fw fragment of Chen et al. (2000)(−600 bp of 5′ sequence) was amplified in three separate PCR reactions and subjected to direct sequencing.

  • Figure 2.—
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    Figure 2.—

    Representative polymorphism at fw. Length polymorphisms are not shown. The standard sequence is based on the inferred ancestral sequence as determined by D. pallidosa. All nucleotides shown as letters represent the derived state of the polymorphism. Polymorphisms distinguishing the northern haplotype class (sites 1504 of R1 and 687, 969, 3994, and 4106 of R9/R42) are highlighted in blue. Note that site 1004 of R1 is not diagnostic of this haplotype class because it is not completely linked to these sites (see CH population). Polymorphisms distinguishing the southern haplotype class (sites 1854 and 2961 of R9/R42) are highlighted in red. Coordinates of the R1, and R9 and R42 (combined), fragments correspond to those given by the accession nos. AF185289 and AF185290, respectively.

  • Figure 3.—
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    Figure 3.—

    Geographic distribution of fw haplotype frequencies.

  • Figure 4.—
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    Figure 4.—

    Relationship of nontransformed haplotype frequency and population latitude (measured as distance from the equator). Regressions (r2) and slopes (m) are based on transformed frequencies: northern r2 = 0.841 (P < 0.0001), m = 10.224; southern r2 = 0.669 (P < 0.001), m = −10.115.

  • Figure 5.—
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    Figure 5.—

    Summary of clinal variation at fw for all populations. Only sites with significant clinal variation are shown (see Table 4). Shaded boxes refer to significant clinal variation at site Y that cannot be explained by linkage to site X.

  • Figure 6.—
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    Figure 6.—

    Comparison of the migration-drift parameter, ΘP (Vogl et al. 2003), at fw and 10 neutral loci.

Tables

  • Figures
  • TABLE 1

    Population samples of D. ananassae used in this study

    Sampling locationCountryAbbreviationNo. of
 isofemale linesCollection
 date
    ChennaiIndia  CH 92000
    PuriIndia  PUR 82000
    BhubaneswarIndia  BBS 92000
    KathmanduNepal  KATH102000
    MandalayMyanmar  MAN101994
    Chiang MaiThailand  CNX102002
    BangkokThailand  BKK 82002
    Kota Kinabalu, BorneoMalaysia  KK 82002
    Bogor, JavaIndonesia  BOG162001
    Darwin and KakaduAustralia  DAR 91995
    CebuPhilippines  CEB 92002
    ManilaPhilippines  MNL102002
    Kumejima, OkinawaJapan  KMJ102000
  • TABLE 2

    Summary of polymorphism at fw

    PopulationDiversity, π̂Diversity, θ̂Tajima's DDivergence
    CH0.001400.001320.320.00563
    PUR0.000680.000650.260.00556
    BBS0.000490.00070−1.360.00574
    KATH00—0.00591
    MAN0.000230.000220.100.00585
    CNX0.001100.000891.040.00563
    BKK0.001320.001140.800.00541
    KK0.000770.00098−1.070.00507
    BOG0.000340.00082−2.28**0.00502
    DAR0.000770.00093−0.800.00530
    CEB0.000530.00077−1.490.00511
    MNL0.000770.00112−1.440.00585
    KMJ0.000130.00022−1.560.00592
    • ↵** P < 0.01.

    • Nucleotide diversity π̂ was estimated accordting to Nei (1987), and θ̂ according to Watterson (1975). The value of D was obtained by Tajima's (1989) method.

  • TABLE 3

    Results of pairwise HKA tests between fw and 10 neutral loci

    PopulationSignificant
 comparisons
 with fwTotal
 significant
 comparisonsP
    CH 0 41
    PUR 5 57.2E-05
    BBS 4 40.00062
    KATH10103.4E-11
    MAN 9161.6E-05
    CNX 1 10.18
    BKK 2 30.08
    KK 2 20.0303
    BOG 0 01
    DAR 3 30.00457
    CEB 4 40.00062
    MNL 1 10.18
    KMJ 7 91.9E-05
    • The HKA test was performed for all pairwise comparisons between loci [11 loci (fw + 10 neutral loci) → 55 comparisons], for each of the 13 sampled populations. For each population, the probability of observing at least i significant tests at the fw locus given that n paired tests were performed and k were significant between the l loci was calculated using Equation 1 (see materials and methods). Populations in italics indicate that the number of comparisons deviating from the neutral expectation was significantly higher than expected for this population.

  • TABLE 4

    Summary of clinal variation of polymorphic sites at fw and 10 neutral loci

    r2
    LocusSiteFrequency  SlopeAll populationsIndiaSE AsiaEasternmost
    fw 8340.07 9.79NS—— 0.821*
    (25)10040.53 8.84  0.782***NS0.886* 0.812*
    15040.49 10.46  0.857***0.929*0.886* 0.812*
     6870.49 10.46  0.857***0.929*0.886* 0.812*
     9690.49 10.46  0.857***0.929*0.886* 0.812*
    10690.19 8.9  0.305*NSNS—
    18540.44 −10.57  0.693***—0.987**NS
    22920.06  −6.05NS0.589*——
    29610.44 −10.57  0.693***—0.987**NS
    39940.49 10.46  0.857***0.929*0.886* 0.812*
    40230.05 −11.8NS0.948*——
    41060.49 10.46  0.857***0.929*0.886* 0.812*
    1   40.07 −22.65NSNSNS 0.808*
    (35)  100.14 6.81NSNSNS 0.850*
      140.19 5.74NSNSNS 0.825*
      530.14 −20.91  0.335*NSNSNS
    2  280.05 21.56NS—— 0.890*
    (63)  470.12 −23.67  0.283*NSNSNS
      480.10 −48.77  0.424*—NSNS
      800.78 5.46NS—0.933**NS
      830.88 10.27  0.290*—0.857*NS
      890.02 −94.96  0.270*—0.852*—
      900.05  −5.48NS—0.852*NS
      940.02 77.84  0.308*NS——
    3   30.31 5.35NS0.928*NSNS
    (60)   80.01114.99  0.280*———
       90.01104.11  0.251*———
      110.15 3.96NS0.994*NSNS
      130.05 10.80NS—0.840*NS
      180.01114.99  0.280*———
      470.01114.99  0.280*———
      520.81  −1.16NSNSNS 0.802*
      530.80  −2.78NSNSNS 0.802*
    4  720.07 23.81NS—NS 0.795*
    (34)
    5   20.18 −18.56NS0.936*NSNS
    (27)  130.05 −57.94  0.343*—NSNS
    6   70.18 28.16  0.398*NSNSNS
    (10)
    7  100.10 8.36NSNSNS 0.821*
    (19)  200.01−126.33  0.370**———
    8  80.03 −50.13  0.305*—NS—
    (15)
    9  220.91 18.28  0.454**—NS 0.959**
    (29)  250.33  −4.82NS0.931*NSNS
    10   70.01−129.66  0.356*—0.852*—
    (34)  210.25 12.62  0.315*0.943*NSNS
      230.86 4.74NS0.935*NSNS
      390.27 13.13  0.303*NSNSNS
      460.16 10.41NSNSNS 0.874*
      580.37 −10.48  0.313*NSNSNS
    • ↵* P < 0.05;

    • ↵** P < 0.01;

    • ↵*** P < 0.001.

    • The numbers of polymorphic sites analyzed for clinal variation (singletons were eliminated) at each locus are indicated in parentheses in column 1. Only sites displaying significant clinal variation in one or more subsets (see below) are shown. The frequency of individual sites is calculated for the entire pooled sample, on the basis of the derived state of the polymorphism as determined by the outgroup D. pallidosa. The slopes are computed from transformed data based on the entire pooled sample. Regressions (r2) of transformed allele frequencies on latitude were performed for all the populations combined, as well as the following subsets: India (KATH, BBS, PUR, and CH), SE Asia (MAN, CNX, BKK, and BOG), and Easternmost (KMJ, MNL, CEB, KK, BOG, and DAR). Polymorphic sites monomorphic or occurring only once in individual subsets are indicated by dashes. NS, no significant clinal variation.

  • TABLE 5

    Probability of obtaining the observed or lower values of FST under the background selection model

    k = 100k = 500
    Population 1Population 2Region of
 comparisonR = 0R = 0.1R = 0R = 0.1
    KATH  MAN  N-N0.0680.0570.0700.032
    KATH  BBS  N-N0.0390.0270.0390.012
    KATH  KMJ  N-N0.0800.0770.0800.078
    MAN  BBS  N-N0.0250.0290.0250.005
    MAN  KMJ  N-N0.0510.0350.0500.019
    KATH  BOG  N-S0.5220.5360.5250.556
    MAN  DAR  N-S0.4560.4580.4610.437
    BBS  DAR  N-S0.5160.4980.5090.473
    BBS  BOG  N-S0.7470.7660.7370.770
    KMJ  KK  N-S0.3420.3220.3320.299
    DAR  BOG  S-S0.1070.0740.1070.030
    DAR  CEB  S-S0.0480.0340.0450.017
    DAR  KK  S-S0.0650.0460.0650.019
    BOG  CEB  S-S0.0560.0380.0570.013
    BOG  KK  S-S0.0640.0390.0690.012
    • Significant comparisons are shown in italics. N, North; S, South.

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Volume 168 Issue 4, December 2004

Genetics: 168 (4)

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The Role of Natural Selection in Genetic Differentiation of Worldwide Populations of Drosophila ananassae

John F. Baines, Aparup Das, Sylvain Mousset and Wolfgang Stephan
Genetics December 1, 2004 vol. 168 no. 4 1987-1998; https://doi.org/10.1534/genetics.104.027482
John F. Baines
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Aparup Das
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Sylvain Mousset
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Wolfgang Stephan
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The Role of Natural Selection in Genetic Differentiation of Worldwide Populations of Drosophila ananassae

John F. Baines, Aparup Das, Sylvain Mousset and Wolfgang Stephan
Genetics December 1, 2004 vol. 168 no. 4 1987-1998; https://doi.org/10.1534/genetics.104.027482
John F. Baines
  • Find this author on Google Scholar
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Aparup Das
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Sylvain Mousset
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Wolfgang Stephan
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