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Introgression Through Rare Hybridization: A Genetic Study of a Hybrid Zone Between Red and Sika Deer (Genus Cervus) in Argyll, Scotland

Simon J. Goodman, Nick H. Barton, Graeme Swanson, Kate Abernethy and Josephine M. Pemberton
Genetics May 1, 1999 vol. 152 no. 1 355-371
Simon J. Goodman
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Nick H. Barton
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Graeme Swanson
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Kate Abernethy
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Josephine M. Pemberton
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Figures

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  • Figure 1.
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    Figure 1.

    —Map of the study site in Argyll, Scotland showing the sampled forest blocks. Sika were introduced at Carradale. In the text sample sites are referred to by number as follows: 1, South Kintyre (-25 km); 2, Carradale (0 km); 3, Achaglachach (40 km); 4, Knapdale (50 km); 5, Kilmichael (55 km); 6, Birdfield (75 km); 7, North Cowal (100 km); 8, East Cowal (105 km); 9, Glendaruel (110 km); 10, South Cowal (115 km). Values in parentheses are distances from introduction point.

  • Figure 2.
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    Figure 2.

    —The proportion of sika-like deer, plotted against distance north from the introduction point at Carradale (thick line). The gray areas bounded by dashed lines show the proportion of individuals carrying apparently introgressed alleles at nuclear or mitochondrial loci (sika-like hybrids below thick line; red-like hybrids above thick line).

  • Figure 3.
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    Figure 3.

    —Estimated relative densities (relative number of deer per square kilometer) of sika (ns) and red (nr) deer, assuming equal rates of increase (rs = rr = 9.2% yr-1) and a carrying capacity of sika β = 1.5 times greater than red (αrr = αrs = 1.5, αss = αsr = 1.5); dispersal rate σ = 3.69 km yr-1. The observed proportions of sika-like individuals in samples (dots) are compared with the estimates [p = ns/(ns + nr); top left curve]; log[L] = -10.49.

  • Figure 4.
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    Figure 4.

    —Log-likelihood contour plots for introgression into the sika-like population (a) and the red-like population (b), plotted against the current rate of hybridization H*, and past introgression I*. The rate of backcrossing into the sika-like population is assumed to be proportional to the overall proportion of red deer (H = H*q, I = I*q). The most likely values (with 2-unit support limits) are H* = 0.0121 (0.0033–0.0279) and I* = 0.00123 (0.00044–0.00193); log(L) = -168.50. For the red-like population sika alleles are assumed to have a frequency of u0 = 0.0049 in the ancestral red population. The most likely values (with 2-unit support limits) are H* = 0.0051 (0.0009–0.0149) and I* = 0.0004 (0–0.0027); log(L) = -152.71. Contours are spaced at 1 unit of log likelihood, and so the 2-unit support limits are at the second contour.

  • Figure 5.
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    Figure 5.

    —Plots of red introgression into sika (a) and sika introgression into red (b). Points show the observed frequency of red or sika alleles within the opposite taxa, compared with the predicted frequency of introgressed alleles (upper smooth curve). The lower dashed lines show the contribution to this prediction from alleles that have been present for more than four generations and are at linkage equilibrium (i.e., from ancestral polymorphism and past introgression).

Tables

  • Figures
  • TABLE 1

    Microsatellite locus primer sequences, PCR conditions, and locus reference

    LocusMgCl2 (mm)DMSOa (%)Annealing temperatureReference
    BM64382.0552–54Bishop et al. (1994)
    RM0952.0552–54Bishop et al. (l994)
    RME0252.0548–50Grosse et al. (1995)
    OarFCB0482.01052–54Buchanan et al. (1994)
    OarFCB1932.01052–54Buchanan and Crawford (1993)
    BOVIRBP2.01052–54Moore et al. (1991)
    MM0122.01048–50Mommens et al. (1994)
    VH0542.0552–54Pierson et al. (1994)
    HH0642.0552–54Henry et al. (1993)
    DRB0032.0 — 46–54Paterson and Pemberton (1997)
    TGLA3872.0550–52Georges and Massey (1992)
    d-loop2.0 — 50Cook (1993); Kocher et al. (1989); Nagata et al. (1998)
    • ↵a Percentage of dimethylsulfoxide by reaction volume.

  • TABLE 2

    For each locus, the allele sizes (in base pairs) are listed, followed by their classification as “sika” or “red” alleles and their frequency within sika-like and red-like individuals

    Locus (no. alleles)AlleleRaceFrequency in sikaFrequency in red
    BOVIRBP (9)144Sika0.60610
    146Sika0.05550.068
    150Red00.1238
    152Red00.0936
    154Red0.01730.117
    156Red0.06940.2982
    160Red00.1987
    162Red00.0146
    166Red00.0146
    Ø Red0.25170.0714
    FCB193 (14)101Red00.0635
    103Red0.01520.0076
    105Red00.0076
    107Red00.1224
    109Red00.0319
    111Red00.3035
    113Red00.0794
    115Red00.0153
    117Red00.0076
    119Red00.1411
    121Red00.1295
    127Red00.0076
    129Sika0.98480
    139Red00.0077
    Ø Red00.0751
    RM095 (11)122Red00.0379
    126Sika0.99370.0061
    128Red00.0689
    130Red00.0627
    132Red0.00630.2195
    134Red00.2985
    136Red00.106
    138Red00.0031
    140Red00.0613
    142Red00.0861
    144Red00.0153
    0Red00.0345
    REM025 (5)157Red00.0092
    171Red00.8159
    173Red00.0945
    197Sika1.0000
    209Red00.0061
    Ø Red00.0742
    BM6438 (6)251Red0.01270.4932
    253Red00.231
    255Red00.1857
    263Red00.0122
    267Sika0.32280
    277Sika0.66460
    Ø Red00.078
    VH054 (14)79Red00.012
    81Red00.043
    83Red00.0122
    85Red00.0373
    87Red00.3941
    89Red00.0994
    91Red00.147
    93Red00.0123
    96Red00.012
    97Red00.006
    102Red00.028
    106Red00.0661
    110Sika1.0000.009
    139Red00.003
    Ø Red00.1184
    HH064 (11)107Red0.01280.0482
    117Red00.003
    119Red00.018
    121Red00.0238
    123Red00.0181
    125Sika0.95510.0178
    127Red00.0239
    131Red0.02560.4132
    133Red0.00640.1634
    135Red00.0579
    137Red00.0059
    Ø Red00.2067
    TGLA387a (27)128Red00.0029
    130Red00.0059
    132Red00.0029
    134Sika0.94870.0147
    138Red00.0059
    139Red00.0029
    140Red00.0608
    141Red00.0207
    142Red00.0576
    143Red00.0059
    144Red0.00640.0724
    172Red00.0059
    198Red00.0029
    (–13) + ΩRed00
    (–12) + ΩRed00.0059
    (–11) + ΩRed00.0029
    (–10) + ΩRed00.0059
    (–9) + ΩRed00.0088
    (–8) + ΩRed0.00640.0177
    (–7) + ΩRed00.0148
    (–6) + ΩRed00.0209
    (–5) + ΩRed0.02560.0178
    (–4) + ΩRed0.00640.0179
    (–3) + ΩRed00.0089
    (–2) + ΩRed0.00640.0118
    (–1) + ΩRed00.0059
    Ω Red00.0669
    Ø Red00.5323
    DRB003 (10)151Red00.0341
    157Red0.01280.3886
    159Red00.003
    161Red00.0824
    163Red0.00640.0061
    167Red0.01280.0642
    171Red00.0061
    181Red00.003
    187Sika0.01920
    189Sika0.94870.0245
    Ø Red00.3881
    MM012 (3)89Red00.741
    91Red00.256
    93Sika10.003
    Ø Red00
    FCB048 (4)143Red0.05130.9028
    145Red00.0309
    155Sika0.79490.0063
    157Sika0.15380
    Ø Red00.0599

    The frequencies are maximum-likelihood estimates, assuming the presence of null alleles (Ø); these estimates are made without assuming that missing data are due to null homozygotes (see text).

    • ↵a At TGLA387, some alleles were very long (>250 bp) and so are scored relative to a reference allele of 250 bp, designated Ω.

  • TABLE 3

    Classification of individuals at each site into pure red or sika: heterozygotes at a single locus, introgressed mtDNA, or complex hybrids

    Site (sample size)Pure sikaSingle heterozygotemtDNA hybridComplex hybridPure redSingle heterozygotemtDNA hybridComplex hybrida
    1 (n = 2)0100000(0, 0, 1)
    1 (n = 40)2653(0, 2, 0)300(0, 5, 0)
    (1, 1, 0)
    3 (n = 33)1670(0, 5, 0)520(0, 2, 0)
    (0, 3, 0)
    4 (n = 29)750(0, 2, 0)1021(0, 0, 1)
    (0, 3, 0)
    (0, 3, 2)
    5 (n = 9)2100410(0, 0, 1)
    6 (n = 40)00003531(0, 1, 1)
    7 (n = 48)00004330(0, 0, 1)
    (0, 2, 0)
    8 (n = 12)000012000
    9 (n = 11)000010100
    10 (n = 22)00002010(0, 0, 1)
    • ↵a Classified by three numbers: whether the mtDNA is introgressed (0/1); the number of loci heterozygous for introgressed alleles; and the number homozygous for introgressed alleles. (The “homozygotes” are most likely heterozygous for null alleles; see text.)

  • TABLE 4

    The maximum-likelihood estimate for null allele frequencies (Ø), and frequency of introgessed alleles (u) for each of the loci at which apparent homozygotes for rare alleles was seen

    LocusØ freq (pooled)u freqObserved vs. expected number of each genotypelog(L) (1 d.f.)
    Ø Ø RR + ØRRSSS + ØS
    Red0.2310.01519153410.02
    TGLA3878.88153.133.801.20
    Red0.3980.024326133440.12
    DRB00326.47132.514.693.33
    Red0.1950.00606159110.46
    FCB0486.36158.641.610.40
    Sika0.0570.0331014740.66
    BOVIRBP0.260.394.7573.6
    Sika0.1170.0389115720.02
    HH0641.080.845.1971.90

    Alleles are pooled into null (Ø), red (R), and sika (S). Missing data are assumed to be null homozygotes. The last column gives the difference in log likelihood by comparing the numbers of observed and expected numbers in each genotypic class (1 d.f.). For none of the five loci is there a significant deviation from the hypothesis that missing data represent null homozygotes (see also Appendix at http://helios.bto.ed.ac.uk/evolgen/).

    • TABLE 5

      Analysis of linkage disequilibrium in red- and sika-like individuals for each site at which the phenotype was present

      Number of introgressed alleles (observed vs. expected)G-statistic (P value)Randomization test P value
      012345
      Site (sika)
          1012.00 —
      0.370.370.1573
          229610.240.480
      28.836.410.720.6225
          3167000113.620.001
      14.567.281.820.300.0380.00380.0086
          47511016.640.078
      5.525.522.760.920.230.0460.2488
          5210.38 —
      2.150.720.5386
      Site (red)
          1012.00 —
      0.370.370.1573
          230000112.840.003
      1.151.430.900.370.120.0290.0249
          352111.800.632
      4.133.221.250.320.6138
          41130.69 —
      11.302.420.4047
          5420.76 —
      4.301.430.3845
          636311.680.201
      35.304.410.280.4327
          743411.260.275
      42.365.290.330.5331
          812 — —
      12
          91010.09 —
      10.040.910.7594
          102020.18 —
      20.091.830.6649

      The observed and expected numbers of individuals with 0–5 introgressed alleles. The G-statistic tests against the null hypothesis that introgressed alleles are in linkage equilibrium (approximated by a Poisson distribution). The associated p value is calculated using the asymptotic χ2-distribution. The last column gives the number of times the observed G value was exceeded in 1000 random permutations of the dataset. Significant deviations indicate introgressing alleles are in linkage disequilibrium, suggesting recent hybridization in that site.

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      Volume 152 Issue 1, May 1999

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      Introgression Through Rare Hybridization: A Genetic Study of a Hybrid Zone Between Red and Sika Deer (Genus Cervus) in Argyll, Scotland

      Simon J. Goodman, Nick H. Barton, Graeme Swanson, Kate Abernethy and Josephine M. Pemberton
      Genetics May 1, 1999 vol. 152 no. 1 355-371
      Simon J. Goodman
      • Find this author on Google Scholar
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      Nick H. Barton
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      Graeme Swanson
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      Kate Abernethy
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      Josephine M. Pemberton
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      Introgression Through Rare Hybridization: A Genetic Study of a Hybrid Zone Between Red and Sika Deer (Genus Cervus) in Argyll, Scotland

      Simon J. Goodman, Nick H. Barton, Graeme Swanson, Kate Abernethy and Josephine M. Pemberton
      Genetics May 1, 1999 vol. 152 no. 1 355-371
      Simon J. Goodman
      • Find this author on Google Scholar
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      Nick H. Barton
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      Graeme Swanson
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      Kate Abernethy
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      Josephine M. Pemberton
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