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Cranial variation in allactagine jerboas (Allactaginae, Dipodidae, Rodentia): a geometric morphometric study

Bader H. Alhajeri

Bader H. Alhajeri. Cranial variation in allactagine jerboas (Allactaginae, Dipodidae, Rodentia): a geometric morphometric study. Zoological Research, 2021, 42(2): 182-194. doi: 10.24272/j.issn.2095-8137.2020.302
Citation: Bader H. Alhajeri. Cranial variation in allactagine jerboas (Allactaginae, Dipodidae, Rodentia): a geometric morphometric study. Zoological Research, 2021, 42(2): 182-194. doi: 10.24272/j.issn.2095-8137.2020.302

跳鼠的头骨变异:基于几何形态学研究

doi: 10.24272/j.issn.2095-8137.2020.302

Cranial variation in allactagine jerboas (Allactaginae, Dipodidae, Rodentia): a geometric morphometric study

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  • 摘要: 五趾跳鼠亚科(Allactaginae)是跳鼠科的一个亚科,包括四趾和五趾跳鼠(五趾跳鼠属Allactaga, 沙漠跳鼠属Allactodipus, 东方五趾跳鼠属Orientallactaga, 肥尾跳鼠属Pygeretmus, 小五趾跳鼠属Scarturus),栖息于亚洲和北非的开阔地带。近期已有的分子系统发育研究颠覆了人们对这个类群的分类认识。为此,基于修订后的分类观点,该研究使用头骨几何形态学方法检测了该亚科14个物种219号标本的头骨变异 (Allactaga major, A. severtzovi, Orientallactaga balikunica, O. bullata, O. sibirica, Pygeretmus platyurus, P. pumilio, P. shitkovi, Scarturus aralychensis, S. euphraticus, S. hotsoni, S. indicus, S. tetradactylus, S. williamsi)。结果显示没有头骨具有显著的大小和形状性二型,但物种的头骨大小和形状在总体和物种对上存在显著差异,且物种自身对头骨大小和形状有很大影响。没有证据表明具有独特的物种异速生长模式,大多数样本都符合常见的异速生长回归向量,只有一小部分头骨形状的变化呈现出异速生长。五趾跳鼠属Allactaga体型最大,其后依次是东方五趾跳鼠属Orientallactaga,小五趾跳鼠属Scarturus, 与肥尾跳鼠属Pygeretmus。以听泡膨大、颧骨弓和吻部缩小为主要特征的主成分1(PC1)可将O. bullata+O. balikunica+S. hotsoni与A. major+A. severtzovi+O. sibirica分开,以颅底和吻部增大,颧弓和枕骨大孔减少为主要特征的主成分2(PC2)可将东方五趾跳鼠属Orientallactaga与小五趾跳鼠属Scarturus+肥尾跳鼠属Pygeretmus分开。而基于非加权组平均法(UPGMA)的聚类分析发现该亚科仅包含4个属,但是,S. hotsoniO. bullata+O. balikunica聚为一支,O. sibiricaA. major+A. severtzovi聚为一支,可能是分别缘于趋同进化和异速生长。
  • Figure  1.  Allactagine relationships based on several molecular phylogenies published in the last decade (Dianat et al., 2013; Hamidi et al., 2016; Lebedev et al., 2013; Moore et al., 2015; Pisano et al., 2015; Upham et al., 2019; Wu et al., 2012; Zhang et al., 2013)

    Relationships are shown as cladograms (with arbitrary branch lengths), with conspecific clades of individuals (based on authors of each study) collapsed into a single tip (see notes). For most studies, the allactagine clade was extracted from a larger phylogeny, and whenever available, the tree based on concatenation of all genes was used. Taxonomy of species names was updated following Michaux & Shenbrot (2017). Cladograms were constructed using R library ape (Paradis & Schliep, 2019).

    Figure  2.  Map of localities sampled in this study

    Genera are designated with different colors, and species are designated with different symbols; darker tones are more heavily sampled localities. The x- and y-axes are longitude and latitude, respectively (using geographic WGS84 CRS). Supplementary Data S1 lists geographic coordinates of localities. Locality of a single specimen (A. major, AMNH 227) was unknown and does not appear in this map. Map was generated using ggplot2 (Wickham, 2016), rnaturalearth (South, 2017), and ggspatial (Dunnington, 2020).

    Figure  3.  Digitized landmarks on ventral cranial view of a small five-toed jerboa (S. indicus; FMNH 103883) from Herāt, Afghanistan (Landmarks are described in Supplementary Table S1)

    Figure  4.  Boxplot of recorded cranial sizes

    For each box, inner line is the median, hinges are the first and third quartiles, whiskers extend from each hinge to the maximum/minimum value (not exceeding 1.5 times the interquartile range), and outliers are plotted as points. Plot was generated using ggplot2.

    Figure  5.  Scatterplot of Procrustes shape coordinates based on PCA of 219 specimens

    Axes show principal components (PC) 1–2 and percentage of total shape variation explained by each. Genera are designated with different colors, and species are designated with different symbols (following legend in Figure 2). Quadrants are demarcated by dotted lines passing through PC origins. TPS deformation grids show shapes at PC extremes (compared to sample mean). To aid visualization, landmarks (in same order and orientation as Figure 3) are linked, and deformations are magnified two-fold. Plot was generated using geomorph.

    Figure  6.  UPGMA dendrogram showing similarity in species-mean shapes (based on Procrustes shape coordinates) along with associated TPS deformation grid for each species (compared to average of all 14 species-mean shapes)

    To aid visualization, landmarks (in same order and orientation as Figure 3) are linked, and deformations are magnified two-fold. Node ‘height’ is indicated below dendrogram. Figure was generated using base R functions and geomorph.

    Figure  7.  Scatterplot of shape-size covariation of 219 specimens

    Logged centroid sizes and common allometric component (CAC) are on x- and y-axes, respectively. Genera are designated with different colors, and species are designated with different symbols (following Figure 2). TPS deformation grids show shapes at CAC extremes (compared to sample mean). To aid visualization, landmarks (in same order and orientation as Figure 3) are linked, and deformations are magnified four-fold. Plot was generated using geomorph.

    Table  1.   ANOVA table for linear model of effect of species identity (‘Species’) on logged cranial size (A) and logged cranial size (‘Size’), species identity, and their interaction on cranial shape (Procrustes shape coordinates) (B)

    dfSSMSR2FZP
    (A) Centroid size (log)
    Species133.81170.29320.8754110.8810.6580.001
    Residuals2050.54210.00260.1245
    Total2184.3537
    (B) Procrustes shape
    Size10.00710.00710.01286.815.4190.001
    Species130.25520.01960.459418.7316.9660.001
    Size×species120.01510.00120.02731.201.6020.061
    Residuals1920.20120.00100.3622
    Total2180.5555
    df: Degrees of freedom; SS: Sum of squares—hierarchical (type-II) was used for (multifactorial) Procrustes shape model; MS: Mean squares; R2: R-squared value; F: F-value; Z: Effect size (standard deviation of F sampling distribution); P: P-values based on 999 permutations. Fit of each linear model was evaluated using randomized residual permutation procedure (RRPP). Model coefficients were estimated using ordinary least squares (OLS). Significant model terms are in bold. All 219 specimens are included in these models.
    下载: 导出CSV

    Table  2.   Pairwise distances between species means and associated statistics based on logged centroid size (A), Procrustes shape coordinates (B), and size-corrected Procrustes shape coordinates (least squares means with logged centroid size as a covariate and no interaction) (C)

    (A) Size (B) Shape (no correction) (C) Shape (size correction)
    dUCLZPdUCLZPdUCLZP
    A. major — A. severtzovi0.160.191.40.1050.030.05–0.30.5930.030.05–0.30.573
    A. major — O. balikunica0.460.206.20.0010.100.057.10.0010.080.063.30.008
    A. major — O. bullata0.350.137.30.0010.090.0311.10.0010.080.045.90.001
    A. major — O. sibirica0.220.124.50.0020.050.035.80.0010.050.034.50.003
    A. major — P. pumilio0.630.1511.40.0010.050.044.00.0020.060.071.30.105
    A. major — P. shitkovi0.540.236.30.0010.050.061.10.1330.080.072.40.029
    A. major — S. aralychensis0.560.178.70.0010.080.046.40.0010.070.062.20.031
    A. major — S. euphraticus0.400.166.60.0010.070.044.70.0010.060.052.60.015
    A. major — S. hotsoni0.480.1310.30.0010.100.0312.00.0010.080.054.60.002
    A. major — S. indicus0.510.1311.20.0010.070.037.60.0010.060.062.20.030
    A. major — S. tetradactylus0.460.1210.30.0010.070.038.30.0010.060.052.50.017
    A. major — S. williamsi0.350.127.30.0010.060.035.80.0010.050.042.50.020
    A. severtzovi — O. balikunica0.300.232.80.0140.090.064.80.0010.070.063.10.007
    A. severtzovi — O. bullata0.190.162.40.0210.080.046.80.0010.070.046.10.001
    A. severtzovi — O. sibirica0.060.16–0.30.5210.040.041.90.0490.040.042.20.032
    A. severtzovi — P. pumilio0.460.186.50.0010.050.052.70.0130.060.061.90.047
    A. severtzovi — P. shitkovi0.380.243.70.0020.060.061.00.1450.070.072.40.024
    A. severtzovi — S. aralychensis0.390.205.00.0010.070.053.60.0030.060.062.10.039
    A. severtzovi — S. euphraticus0.240.192.60.0190.060.052.40.0210.050.052.00.038
    A. severtzovi — S. hotsoni0.320.164.90.0010.080.047.10.0010.070.054.20.002
    A. severtzovi — S. indicus0.350.165.50.0010.060.044.10.0010.050.052.40.032
    A. severtzovi — S. tetradactylus0.290.174.40.0010.060.044.50.0020.050.052.70.017
    A. severtzovi — S. williamsi0.190.172.30.0290.050.042.20.0270.040.041.50.077
    O. balikunica — O. bullata0.110.170.70.2220.040.041.50.0770.040.041.60.070
    O. balikunica — O. sibirica0.240.173.30.0090.080.046.40.0010.070.044.60.002
    O. balikunica — P. pumilio0.170.191.60.0810.080.056.10.0010.090.057.50.001
    O. balikunica — P. shitkovi0.080.27–0.30.5120.100.074.60.0010.100.066.00.001
    O. balikunica — S. aralychensis0.090.220.20.3580.060.053.10.0060.070.054.00.004
    O. balikunica — S. euphraticus0.060.20–0.30.5360.060.053.20.0060.060.053.50.004
    O. balikunica — S. hotsoni0.020.17–0.90.8220.040.040.80.1890.040.041.30.098
    O. balikunica — S. indicus0.050.17–0.40.5580.060.044.00.0020.060.044.90.002
    O. balikunica — S. tetradactylus0.000.17–1.20.9750.070.045.00.0010.070.045.80.001
    O. balikunica — S. williamsi0.110.180.80.2050.060.044.40.0010.060.044.40.003
    O. bullata — O. sibirica0.130.074.70.0010.080.0216.60.0010.070.0214.80.001
    O. bullata — P. pumilio0.270.116.70.0010.080.0312.70.0010.100.0410.90.001
    O. bullata — P. shitkovi0.190.191.70.0640.090.056.30.0010.100.058.00.001
    O. bullata — S. aralychensis0.200.143.40.0030.070.038.40.0010.080.048.70.001
    O. bullata — S. euphraticus0.050.13–0.10.4800.070.038.00.0010.070.039.50.001
    O. bullata — S. hotsoni0.130.083.90.0010.050.0210.60.0010.050.029.80.001
    O. bullata — S. indicus0.160.075.30.0010.070.0214.10.0010.070.0213.80.001
    O. bullata — S. tetradactylus0.100.073.50.0040.080.0216.10.0010.080.0217.00.001
    O. bullata — S. williamsi0.000.08–1.20.9220.070.0213.20.0010.070.0214.80.001
    O. sibirica — P. pumilio0.410.1011.10.0010.070.0311.20.0010.080.056.00.001
    O. sibirica — P. shitkovi0.320.194.10.0010.080.054.70.0010.090.055.60.001
    O. sibirica — S. aralychensis0.340.146.80.0010.070.037.80.0010.070.044.90.001
    O. sibirica — S. euphraticus0.180.123.50.0040.050.035.30.0010.050.034.80.002
    O. sibirica — S. hotsoni0.260.0710.60.0010.070.0216.10.0010.060.038.50.001
    O. sibirica — S. indicus0.290.0711.90.0010.060.0213.60.0010.060.036.40.001
    O. sibirica — S. tetradactylus0.240.0610.70.0010.070.0216.30.0010.060.039.70.001
    O. sibirica — S. williamsi0.130.074.60.0010.050.0210.20.0010.040.028.40.001
    P. pumilio — P. shitkovi0.090.210.10.3950.050.060.80.1920.040.050.50.261
    P. pumilio — S. aralychensis0.070.150.20.3630.050.043.60.0020.050.044.60.002
    P. pumilio — S. euphraticus0.230.153.70.0040.060.045.30.0010.070.045.60.001
    P. pumilio — S. hotsoni0.150.113.10.0070.080.0311.40.0010.080.0312.40.001
    P. pumilio — S. indicus0.120.102.40.0240.040.035.50.0010.050.036.40.001
    P. pumilio — S. tetradactylus0.170.104.10.0030.040.034.80.0010.050.035.80.001
    P. pumilio — S. williamsi0.280.116.80.0010.060.037.30.0010.060.046.30.001
    P. shitkovi — S. aralychensis0.010.22–1.10.9030.070.062.90.0120.070.053.40.004
    P. shitkovi — S. euphraticus0.140.210.80.2000.060.062.40.0250.070.063.60.002
    P. shitkovi — S. hotsoni0.060.19–0.30.5570.090.056.30.0010.090.057.60.001
    P. shitkovi — S. indicus0.030.19–0.80.7600.060.053.40.0060.070.054.10.002
    P. shitkovi — S. tetradactylus0.080.190.10.4070.060.053.20.0070.070.054.40.001
    P. shitkovi — S. williamsi0.190.201.80.0580.060.052.90.0100.070.054.30.002
    S. aralychensis — S. euphraticus0.150.171.60.0800.040.041.20.1240.040.041.30.107
    S. aralychensis — S. hotsoni0.070.130.50.2890.040.043.50.0010.050.034.50.002
    S. aralychensis — S. indicus0.040.13–0.20.4890.020.03–0.20.5180.020.030.00.432
    S. aralychensis — S. tetradactylus0.100.131.10.1430.020.030.20.3680.030.030.80.187
    S. aralychensis — S. williamsi0.200.133.60.0030.040.042.70.0100.040.042.40.020
    S. euphraticus — S. hotsoni0.080.120.70.2240.050.034.90.0010.050.034.90.002
    S. euphraticus — S. indicus0.110.131.50.0920.030.032.20.0400.030.032.40.024
    S. euphraticus — S. tetradactylus0.060.120.10.4010.040.033.40.0060.040.034.00.003
    S. euphraticus — S. williamsi0.050.120.00.4410.020.03–0.50.6400.020.030.00.461
    S. hotsoni — S. indicus0.030.08–0.10.4710.040.029.00.0010.050.0210.40.001
    S. hotsoni — S. tetradactylus0.020.07–0.20.5130.050.0211.50.0010.050.0212.60.001
    S. hotsoni — S. williamsi0.130.084.10.0010.050.0210.40.0010.050.028.60.001
    S. indicus — S. tetradactylus0.050.061.40.1150.030.024.90.0010.030.025.80.001
    S. indicus — S. williamsi0.160.075.60.0010.030.025.90.0010.030.025.00.001
    S. tetradactylus — S. williamsi0.110.073.70.0030.040.029.00.0010.040.027.90.001
    d: Distance between (least squares) means; UCL: 95% upper confidence limit for d (one-tailed); Z: Effect size; P: P-values based on 999 permutations. Significantly different pairs are in bold. P. platyurus consists of a single specimen, and thus could not be included in these pairwise comparisons.
    下载: 导出CSV
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  • 收稿日期:  2020-10-15
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