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Phylogeography of SARS-CoV-2 pandemic in Spain: a story of multiple introductions, micro-geographic stratification, founder effects, and super-spreaders

Alberto Gómez-Carballa Xabier Bello Jacobo Pardo-Seco María Luisa Pérez del Molino Federico Martinón-Torres Antonio Salas

Alberto Gómez-Carballa, Xabier Bello, Jacobo Pardo-Seco, María Luisa Pérez del Molino, Federico Martinón-Torres, Antonio Salas. Phylogeography of SARS-CoV-2 pandemic in Spain: a story of multiple introductions, micro-geographic stratification, founder effects, and super-spreaders. Zoological Research, 2020, 41(6): 605-620. doi: 10.24272/j.issn.2095-8137.2020.217
Citation: Alberto Gómez-Carballa, Xabier Bello, Jacobo Pardo-Seco, María Luisa Pérez del Molino, Federico Martinón-Torres, Antonio Salas. Phylogeography of SARS-CoV-2 pandemic in Spain: a story of multiple introductions, micro-geographic stratification, founder effects, and super-spreaders. Zoological Research, 2020, 41(6): 605-620. doi: 10.24272/j.issn.2095-8137.2020.217

西班牙SARS-CoV-2大流行的谱系地理学:关于病毒多次传入,微地理尺度分区,奠基者效应以及超级传播者的故事

doi: 10.24272/j.issn.2095-8137.2020.217

Phylogeography of SARS-CoV-2 pandemic in Spain: a story of multiple introductions, micro-geographic stratification, founder effects, and super-spreaders

Funds: This study was supported by the Instituto de Salud Carlos III: project GePEM (Instituto de Salud Carlos III(ISCIII)/PI16/01478/Cofinanciado FEDER), DIAVIR (Instituto de Salud Carlos III(ISCIII)/DTS19/00049/Cofinanciado FEDER; Proyecto de Desarrollo Tecnológico en Salud) and Resvi-Omics (Instituto de Salud Carlos III(ISCIII)/PI19/01039/Cofinanciado FEDER) and project BI-BACVIR (PRIS-3; Agencia de Conocimiento en Salud (ACIS)—Servicio Gallego de Salud (SERGAS)—Xunta de Galicia; Spain) given to A.S.; and project ReSVinext (Instituto de Salud Carlos III(ISCIII)/PI16/01569/Cofinanciado FEDER) and Enterogen (Instituto de Salud Carlos III(ISCIII)/ PI19/01090/Cofinanciado FEDER) given to F.M.-T.
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  • 摘要: 西班牙曾经是新型冠状病毒肺炎(COVID-19)全球大流行的中心之一。本研究我们分析了从GISAID数据库上获取超过4100个病毒基因组(包括超过2600个高质量的基因组),其中包含了在西班牙采样的1245个基因组(922个高质量基因组)。这项研究的主要目的是分析SARS-CoV-2病毒的基因组变异情况,并重建西班牙病毒的谱系地理和传播模式。谱系地理分析表明,从疫情爆发开始SARS-CoV-2在西班牙至少有34次独立传入事件,其中6个谱系毒株非常成功地在西班牙传播,也就是六个超级传播者,A2a4型(7.8%),A2a5型(38.4%),A2a10型(2.8%),B3a型(30.1%)和B9型(8.7%)毒株所造成,这些毒株数据占西班牙所有基因组的87.9%。西班牙流行的SARS-CoV-2基因组中有一个独特B型谱系(39.3%,主要是B3a+B9型)毒株,其发生频率远高于其它任何欧洲国家。研究推测B3a型,B9型(以及A2a5型的一个重要衍生谱系,即A2a5c型)毒株最有可能起源于西班牙,其它三个单倍型毒株可能是由从其他欧洲地区输入。B3a谱系毒株可能起源于巴斯克地区,由一个地理来源不确定的B3祖先毒株衍生而来,而B9谱系毒株则可能来源于马德里。基于估算西班牙国内检测到的第一个谱系B3a最近共同祖先(TMRCA)分化时间,推测出第一批病毒输入西班牙的时间大约在2020年2月11日。此外,对比其他疾病发病率较低但D614G突变发生率更高的国家(西班牙56.4%对比欧洲其他地区82.4%),早先的说法是D614G突变体与较高的传播能力相关,但这与西班牙COVID-19的高流行并不相符。相反,这些数据支持遗传漂变在模拟病毒株微地理尺度下分区的主要作用,以及SARS-CoV-2超级传播者在传播病毒中的作用。
    #Authors contributed equally to this work
  • Figure  1.  Skeleton of maximum parsimony tree of Spanish genomes

    Pie charts show haplogroup frequency distribution for main clades. Haplogroup labels in green refer to previously described clades (Gómez-Carballa et al, 2020), in blue are newly defined in present study. Mutations along branches are nucleotide changes against reference sequence. Mutations with a @ symbol indicate reversions. The * symbol after the name of the haplogroup in the piecharts refers to those sequences that can not be clasified into any of the sub-haplogrups included by the specified haplogroup.

    Figure  2.  Interpolation maps of haplogroup frequencies worldwide and for Iberia, and extended Bayesian skyline plots (EBSPs) for main Spanish haplogroups

    Sampling points considered for interpolation are given in map of Supplementary Figure S11.

    Figure  3.  Schematic representation of reconstructed movements of main Spanish SARS-CoV-2 clades in Iberian Peninsula according to phylogeographic information inferred from phylogenies and genome chronologies

    Areas of circles are proportional to frequencies. Note, frequency of each haplogroup in different regions should not be interpreted as a proportion of genomes received from any particular region because frequency of each haplogroup in a given region may or may not have been favored by local super-spreading events and therefore strongly depends on regional circumstances.

    Figure  4.  Origin and spread of Spanish haplogroup B3a

    We highlight arrow connecting Basque Country (Spain) with two identical SARS-CoV-2 genomes from France because these two were sampled before the Spanish ones but were derivatives of basal B3a haplotype (see main text). Question mark on B3 indicates doubts on its origin. From a likely origin of B3a in the Basque Country, B3a moved to other Spanish regions, as well as to other American, European, and Asian locations.

    Figure  5.  Networks of main Spanish super-spreader candidates by region

    BC: Basque Country; VL: Valencian Community; CT: Catalonia; MD: Madrid; NV: Navarra; and GL: Galicia. We used two political divisions in this figure, namely, cities and autochthonous communities (Galicia and Navarra); this is due to the difficulty in finding a consistent geographic/political designation that fits with sampling. For instance, most Galician cases occurred around the Santiago de Compostela city, which is in the political boundaries of several provinces of the Galician region. In Navarra, most cases were sampled in the city or area close to Pamplona.

    Figure  6.  Timeline of main episodes related to spread of SARS-CoV-2 in Spain

    Histogram in background indicates number of transmission lineages in Spain; red indicates ones generated de novo in Spain (n=64) from "domestic" mutations, green indicates lineages introduced from abroad (n=30). Indicated below schematic line representing months are dates when first genomes were sampled for main haplogroups, and TMRCA of these clades. Distribution of COVID-19 cases in Spain was built with data obtained from https://ourworldindata.org.

    Table  1.   Characteristics of SARS-CoV-2 genome database used in present study

    WorldwideSpain
    Total genomes in database
      n41 3621 259
     Ambiguities12 646553
     Indels1 37857
     MNPs76317
     Different haplotypes19 968680
     Singleton haplotypes15 934565
     Substitutions14 2911 000
     Singleton substitutions7 189746
    HQ genomes in database
     n26 506922
     Ambiguities4 936216
     Indels79540
     MNPs31812
     Different haplotypes13 559518
     Singleton haplotypes10 942438
     Substitutions10 663788
     Singleton substitutions5 313609
    LQ genomes in database
     n14 856337
     Ambiguities9 340351
     Indels87321
     MNPs4746
     Different haplotypes8 141209
     Singleton haplotypes6 709178
     Substitutions8 408353
     Singleton substitutions4 802275
    HQ: High-quality; LQ: Low-quality.
    下载: 导出CSV

    Table  2.   Regional distribution of most frequent haplotypes sampled in Spain

    IDnTnH#H1#H2#H3#H4#H5#H6
    HaplogroupB3aA2a5A2a5cA2a10B9A2a4
    Spanish region
    Andalusia13931 (22.3)4 (2.9)18 (12.9)7 (5.0)2 (1.4)
    Basque Country31 (33.3)1 (33.3)
    Balearic Island22392 (41.3)75 (33.6)10 (4.5)1 (0.4)6 (2.7)
    Catalonia339 (27.3)7 (21.2)2 (16.1)
    Canary Islands92 (22.2)1 (11.1)1 (11.1)
    Castilla Leon42 (50.0)2 (1.4)
    Castilla La Mancha31 (33.3)1 (33.3)
    Galicia3710 (27.0)8 (21.6)2 (5.4)
    La Rioja122 (16.7)2 (16.7)
    Madrid14331 (21.7)14 (9.8)16 (11.2)1 (0.7)
    Navarra4211 (26.2)5 (11.9)5 (11.9)1 (2.4)
    Valencian Community24483 (34.0)29 (11.9)16 (6.6)13 (5.3)15 (6.1)4 (1.6)7 (2.9)
    Total920277 (30.1)113 (12.3)80 (8.7)44 (4.8)16 (1.7)14 (1.5)10 (1.1)
    Continental region
    Africa18811 (5.9)11 (5.9)
    Asia2 67469 (2.6)9 (0.3)4 (0.1)2 (0.1)54 (2.0)
    Europe (excluding Spain)14 0311 068 (7.6)13 (0.1)91 (0.6)27 (0.2)8 (0.1)4 (0.0)925 (6.2)
    North America6 701108 (1.6)2 (0.0)7 (0.1)1 (0.0)3 (0.0)95 (1.4)
    Oceania1 62173 (4.5)7 (0.4)1 (0.1)1 (0.1)64 (3.9)
    South America36043 (11.9)7 (1.9)19 (5.3)2 (0.6)1 (0.3)14 (3.9)
    Total (excluding Spain)25 5751 372 (5.4)31 (0.1)128 (0.5)33 (0.1)9 (0.0)7 (0.0)1 163 (4.5)
    Total (including Spain)26 4971 485 (5.6)144 (0.5)208 (0.8)33 (0.3)25 (0.1)22 (0.1)1 173 (4.4)
    Haplotype IDs refers to: #H1=C8782T–T9477A–C14805T–G25979T–T28144C–C28657T–C28863T; #H2=C241T–C3037T–C14408T–A20268G–A23403G; #H3=C241T–C3037T–C14408T–A20268G–A23403G–G29734C; #H4=C241T–C3037T–C14408T–A23403G–C29144T; #H5=C8782T–C26088T–T28144C; and #H6=C241T–C3037T–C14408T–A23403G. Other abbreviations: nT: Total sample size; nH: Sample size of unique haplotypes. Brackets show frequency of corresponding haplotype in each region. Total samples from Spain do not match sum of values of Spanish regions because 12 sequences did not have state information. –: No sequences available.
    下载: 导出CSV

    Table  3.   Normalized phylogenetic features of potential super-spreader candidate phylogenies in Spanish COVID-19 outbreak

    HGALnn1n2ALCHCIILMHPFSISN1SN2HLH/L
    A2a4VL14771.000.141.001.001.000.211.000.920.240.990.204.92
    A2a4DN9090.430.440.710.710.750.670.910.630.550.690.561.24
    A2a5VL3215171.000.061.001.001.000.091.000.970.130.990.1010.43
    A2a5MD3913261.000.051.001.001.000.081.000.970.111.000.0812.47
    A2a5DN17980.430.240.900.870.940.180.930.880.270.820.233.61
    A2a5BC14771.000.141.001.001.000.211.000.920.240.990.204.92
    A2a5GL198110.880.210.880.880.940.160.920.890.250.900.214.36
    A2a5NV9540.570.440.750.710.880.330.890.750.470.760.421.83
    A2a5cMD2913161.000.071.001.001.000.101.000.960.140.990.109.54
    A2a5cVL2813151.000.071.001.001.000.111.000.960.140.990.119.24
    A2a5cBN9271.000.221.001.001.000.331.000.880.340.980.303.28
    A2a10VL181531.000.111.001.001.000.171.000.940.200.990.166.20
    B3aVT11773440.180.120.910.900.940.050.920.940.100.800.098.75
    B3aVL4329140.290.140.810.900.880.210.840.930.180.780.184.38
    B9DN6511.000.291.001.001.000.431.000.830.410.970.372.60
    B9VL7431.000.291.001.001.000.431.000.830.410.970.372.60
    B9MD100100.330.550.760.560.800.270.890.700.500.670.441.53
    Analysis was carried out in indicated haplogroups after subtracting corresponding nested sub-clades. n: Total sample size; n1: sample size of principal node (only for super-spreader candidate); n2: sample size of derived haplotypes (only for super-spreader candidate). For Spanish regions: BN: Barcelona (Catalonia); DN: Donostia (Basque Country); GL: Galicia; MD: Madrid; NV: Navarra; VL: Valencian Community; VT: Vitoria (Basque Country); Statistical indices: AL: Normalized average ladder; CH: Cherries; CI: Colless index; IL: IL number; MH: Maximum height; PF: Pitchforks; SC: Sackin index; SN1 and SN2: Staircase-ness 1 and 2, respectively. H: Average of AL, CI, IL, MH, and SI, SN1; L: Average of CH, PF, and SN2.
    下载: 导出CSV

    Table  4.   TMRCA of main Spanish clades

    HaplogroupnTMRCAHPDOrigin
    A2a4682020/02/202020/02/11–2020/02/27Europe
    A2a53152020/02/222020/02/12–2020/02/29Italy
    A2a5c952020/03/032020/02/28–2020/03/05Spain
    A2a10272020/03/012020/02/29–2020/03/02Portugal
    B3a2662020/02/112020/01/30–2020/02/20Spain
    B9742020/02/222020/02/15–2020/02/28Spain
    HPD: 95% highest posterior density (HPD) confidence interval. Origin refers to most likely origin of haplogroups inferred as most favorable scenario that considers both genome sampling chronology and regional genome variation. Time of the most recent common ancestor (TMRCA)
    下载: 导出CSV
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    [18] PAN Ru-Lian, Charles Oxnard.  Craniodental Variation of Macaques (Macaca):Size,Function and Phylogeny, Zoological Research.
    [19] LIN Dan-jun, YOU Yong-long, ZHONG Xiu-rong.  The Structure of The Spermatozoon of Hyla chinensis and Its Bearing on Phylogeny, Zoological Research.
    [20] KUANG Pu-ren.  Phylogeny of The Family Lernaeidae (Parasitic Copepoda), Zoological Research.
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出版历程
  • 收稿日期:  2020-08-26
  • 录用日期:  2020-09-16
  • 网络出版日期:  2020-09-16
  • 刊出日期:  2020-11-18

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