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Comparative mitogenome phylogeography of two anteater genera (Tamandua and Myrmecophaga; Myrmecophagidae, Xenarthra): Evidence of discrepant evolutionary traits

Manuel Ruiz-García Daniel Pinilla-Beltrán Oscar E. Murillo-García Christian Miguel Pinto Jorge Brito Joseph Mark Shostell

Manuel Ruiz-García, Daniel Pinilla-Beltrán, Oscar E. Murillo-García, Christian Miguel Pinto, Jorge Brito, Joseph Mark Shostell. Comparative mitogenome phylogeography of two anteater genera (Tamandua and Myrmecophaga; Myrmecophagidae, Xenarthra): Evidence of discrepant evolutionary traits. Zoological Research, 2021, 42(5): 525-547. doi: 10.24272/j.issn.2095-8137.2020.365
Citation: Manuel Ruiz-García, Daniel Pinilla-Beltrán, Oscar E. Murillo-García, Christian Miguel Pinto, Jorge Brito, Joseph Mark Shostell. Comparative mitogenome phylogeography of two anteater genera (Tamandua and Myrmecophaga; Myrmecophagidae, Xenarthra): Evidence of discrepant evolutionary traits. Zoological Research, 2021, 42(5): 525-547. doi: 10.24272/j.issn.2095-8137.2020.365

两个食蚁兽属(TamanduaMyrmecophaga)比较线粒体组的系统地理学研究:来自不同进化特征的证据

doi: 10.24272/j.issn.2095-8137.2020.365

Comparative mitogenome phylogeography of two anteater genera (Tamandua and Myrmecophaga; Myrmecophagidae, Xenarthra): Evidence of discrepant evolutionary traits

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  • 摘要: 贫齿目Xenarthra(树懒sloths,食蚁兽anteaters和犰狳armadillos)是典型的南美洲哺乳动物。在这三个类群中,蠕舌亚目Vermilingua(食蚁兽anteaters;食蚁兽科Myrmecophagidae)是现存最少的古生物种。该研究对来自中美洲和南美洲的两种小食蚁兽(Tamandua tetradactylaT. mexicana)(n=74),以及来自南美洲的大食蚁兽Myrmecophaga tridactyla (n=41)进行采样和全线粒体组测序。在小食蚁兽Tamandua中,检测出了三种不同的单倍群。最古老的单倍群(THI)包含了许多T. tetradactyla的形态型(也包含一些T. mexicana的形态型),该单倍群起源于南美洲东南部(现在的乌拉圭),后来迁往南美洲北部,后者是THII单倍群的起源地。单倍群THII包含T. mexicana的形态型(也包含一些T. tetradactyla的形态型),主要分布于中美洲,哥伦比亚和厄瓜多尔。单倍群THI和THII之间的遗传距离达到4%。THII起源于南美洲北部或中美洲“原生”的单倍群THIII(由50%的T. mexicana和50%的T. tetradactyla组成)。THIII与THII大致分布在同一地区,如中美洲、厄瓜多尔和哥伦比亚,尽管以后者THII为主。由于三个单倍群在哥伦比亚和厄瓜多尔有重叠区,且T. tetradactylaT. mexicana没有互为单系,所以该研究认为在小食蚁兽属Tamandua内存在一个独特的新种,即T. tetradactyla。与Tamandua相比,尽管检测出两种遗传分化很大(遗传距离约为10%)的两个单倍群(MHI和MHII),但M. tridactyla在新热带地区范围内没有表现出不同的形态。基部的单倍群(MHI)起源于南美洲西北部,而地理衍生出的单倍群(MHII),虽然与MHI有重叠区,但却扩张到了南美洲中部和南部。因此,小食蚁兽属Tamandua是从北向南迁移,而大食蚁兽属Myrmecophaga从南向北迁移。该研究还发现,当前的线粒体多样性开始于晚上新世和上更新世。此外,两个类群均表现出较高的线粒体遗传多样性水平。TamanduaMyrmecophaga表现出更多的雌性种群扩张的证据。Tamandua在约0.6–0.17百万年前经历了种群扩张,Myrmecophaga在约0.3–0.2百万年前发生种群扩张。然而这两个类群在近期1–2 万年中均经历了明显的雌性数量的下降,并且它们的空间遗传结构很低。因此,TamanduaMyrmecophaga在形成它们的遗传结构过程中可能没有受到生物地理、地质或气候事件的影响。
  • Figure  1.  Map of Latin America identifying sampling locations of Tamandua and Myrmecophaga

    Numbers of individuals sampled in each country and sequenced (complete mitogenomes) are listed in parentheses.

    Figure  2.  Maximum-likelihood tree of 74 Tamandua sp. specimens based on entire mitogenomes

    Numbers in nodes are bootstrap percentages.

    Figure  3.  Maximum-likelihood tree of 41 Myrmecophaga tridactyla specimens based on entire mitogenomes

    Numbers in nodes are bootstrap percentages.

    Figure  4.  Median-joining network (MJN) with haplotypes from entire mitogenomes of Tamandua sp. sampled in Latin America

    Yellow, geographic specimens with T. tetradactyla phenotype; blue, geographic specimens with T. mexicana phenotype; black, Myrmecophaga tridactyla as outgroup. Small red circles indicate missing intermediate haplotypes. Three different haplogroups were found. Arrows indicate evolutionary trajectories of haplotypes (from ancestral to derived).

    Figure  5.  Median-joining network (MJN) with haplotypes from entire mitogenomes of Myrmecophaga tridactyla sampled in South America

    Black, specimens from MHI; yellow, specimens from MHII; green, Tamandua tetradactyla as outgroup. Small red circles indicate missing intermediate haplotypes. Two different haplogroups were found. Arrows indicate evolutionary trajectories of haplotypes (from ancestral to derived).

    Figure  6.  Monmonier’s algorithm analysis to detect three most important geographical barriers for Tamandua sp. and Myrmecophaga tridactyla specimens following mitogenome sequencing Tamandua sp. (A) and Myrmecophaga tridactyla (B)

    Table  1.   Sources of Tamandua sp. (n=74) and Myrmecophaga tridactyla (n=41) specimens collected and analyzed (mitogenomes) from Latin America and South America, respectively

    Species and Location No. of samples (n)
    Tamandua mexicana (n=30)
    Guatemala (n=4)
     Petén Department 2
     Izabal Department 1
     Jalapa Department 1
    Honduras (n=1)
     Francisco-Morazán Department 1
    Panama (n=1)
     Panama Department 1
    Colombia (n=20)
     Antioquia Department 1
     Atlántico Department 1
    Caquetá Department 1
     Córdoba Department 1
     Chocó Department 3
     Magdalena Department 4
     Nariño Department 3
     Risaralda Department 1
     Tolima Department 2
     Valle del Cauca Department 3
    Ecuador (n=4)
     Manabí Province 1
     Pichincha Province 3
    Tamandua tetradactyla (n=44)
    Colombia (n=14)
     Arauca Department 1
     Caquetá Department 2
     Cundinamarca Department 1
     Meta Department 4
     Tolima Department 2
     Vichada Department 4
    Ecuador (n=7)
     Morona-Santiago Province 1
     Napo Province 2
     Pastaza Province 2
     Sucumbíos Province 1
     Zamora Province 1
    Peru (n=2)
     Madre de Dios Department 2
    Bolivia (n=11)
     Beni Department 1
     Cochabamba Department 6
     La Paz Department 3
    Tarija Department 1
    Paraguay (n=2)
     Canindeyú Department 2
    Argentina (n=6)
     Buenos Aires Province 2
     Chaco Province 1
     Misiones Province 2
     Santa Fe Province 1
    Uruguay (n=2)
     Cerro Largo Department 1
     Treinta y Tres Department 1
    Myrmecophaga tridactyla (n=41)
    Colombia (n=20)
     Amazonas Department 1
     Arauca Department 3
     Casanare Department 4
     Cundinamarca Department 2
     Guaviare Department 1
     Meta Department 8
     Tolima Department 1
    Ecuador (n=1)
     Loja Province 1
    Peru (n=9)
     Loreto Department 3
     San Martín Department 2
     Ucayali Department 4
    Bolivia (n=4)
     Beni Department 3
     Santa Cruz Department 1
    Paraguay (n=1)
     Alto Paraná Department 1
    Argentina (n=6)
     Formosa Province 1
     Jujuy Province 1
     Santa Fe Province 1
     Tucumán Province 3
    下载: 导出CSV

    Table  2.   Genetic heterogeneity and gene flow based on mitogenomes of Tamandua sp. and Myrmecophaga tridactyla analyzed in this study

    Genetic heterogeneity and gene flow statisticsValueProbability
    Tamandua sp.
    χ2144.000 df=1340.262
    HST0.00390.0076*
    KST0.56940.00001**
    KST*0.21750.00001**
    ZS573.40730.00001**
    ZS*5.90550.00001**
    Snn0.98610.00001**
    γST0.58090.00323*
    NST0.68140.00210*
    FST0.66880.00240*
    Nm10.36
    Nm20.23
    Nm30.25
    Myrmecophaga tridactyla
    χ241.000 df=330.159
    HST0.00790.0363*
    KST0.57290.00001**
    KST*0.25670.00001**
    ZS240.6750.00001**
    ZS*5.19970.00001**
    Snn1.00000.00001**
    γST0.58150.00200*
    NST0.79550.00001**
    FST0.78750.00001**
    Nm10.36
    Nm20.13
    Nm30.13
    *: P<0.05; **: P<0.001; df: Degrees of freedom. HST, KST, KST*, ZS, ZS*, Snn, γST, NST, and FST: Genetic heterogeneity statistics; Nm: Gene flow statistic; Nm1: Gene flow estimated from γST; Nm2: Gene flow estimated from NST; Nm3: Gene flow estimated from FST.
    下载: 导出CSV

    Table  3.   Genetic diversity statistics (±standard deviation) for Tamandua sp. and Myrmecophaga tridactyla

    NHdπθ
    Tamandua sp.
    Total samples700.998±0.00030.064±0.000349.031±1.280
    THI301.000±0.00020.026±0.000232.310±1.022
    THII171.000±0.00200.018±0.002718.931±0.696
    THIII210.983±0.00170.036±0.005738.401±1.258
    Myrmecophaga tridactyla
    Total samples340.988±0.00090.051±0.000637.162±2.340
    MHI100.982±0.00460.015±0.000416.388±2.711
    MHII240.979±0.00160.024±0.000529.786±2.455
    N: Number of haplotypes; Hd: Haplotype diversity; π: Nucleotide diversity; θ: Neμ; Ne: Effective female population size; μ: Mutation rate per generation.
    下载: 导出CSV

    Table  4.   Spatial autocorrelation analyses using AIDA with five distance classes (DC), II index, and cc coefficient for Tamandua sp. and Myrmecophaga tridactyla

    Tamandua sp.1 DC=0–943 km2 DC=943–1 897 km3 DC=1 897–2 414 km4 DC=2 414–4 082 km5 DC=4 082–7 000 km
    II0.0408*0.0318*0.0024–0.083*–0.1369**
    cc0.98050.99270.95411.03241.0806
    Myrmecophaga tridactyla1 DC=0–1 066 km2 DC=1 66–1 577 km3 DC=1 577–2 683 km4 DC=2 683–3 790 km5 DC=3 790–4 510 km
    II–0.0099–0.017–0.084–0.01940.1356
    cc0.95621.15791.02850.89640.8489
    *: P<0.05; **: P<0.01.
    下载: 导出CSV
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  • 收稿日期:  2021-04-30
  • 录用日期:  2021-07-23
  • 网络出版日期:  2021-07-26
  • 刊出日期:  2021-09-18

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