Volume 41 Issue 6
Nov.  2020
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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

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

doi: 10.24272/j.issn.2095-8137.2020.217
#Authors contributed equally to this work
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.
More Information
  • Corresponding author: E-mail: antonio.salas@usc.es
  • Received Date: 2020-08-26
  • Accepted Date: 2020-09-16
  • Available Online: 2020-09-16
  • Publish Date: 2020-11-18
  • Spain has been one of the main global pandemic epicenters for coronavirus disease 2019 (COVID-19). Here, we analyzed >41 000 genomes (including >26 000 high-quality (HQ) genomes) downloaded from the GISAID repository, including 1 245 (922 HQ) sampled in Spain. The aim of this study was to investigate genome variation of novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and reconstruct phylogeographic and transmission patterns in Spain. Phylogeographic analysis suggested at least 34 independent introductions of SARS-CoV-2 to Spain at the beginning of the outbreak. Six lineages spread very successfully in the country, probably favored by super-spreaders, namely, A2a4 (7.8%), A2a5 (38.4%), A2a10 (2.8%), B3a (30.1%), and B9 (8.7%), which accounted for 87.9% of all genomes in the Spanish database. One distinct feature of the Spanish SARS-CoV-2 genomes was the higher frequency of B lineages (39.3%, mainly B3a+B9) than found in any other European country. While B3a, B9, (and an important sub-lineage of A2a5, namely, A2a5c) most likely originated in Spain, the other three haplogroups were imported from other European locations. The B3a strain may have originated in the Basque Country from a B3 ancestor of uncertain geographic origin, whereas B9 likely emerged in Madrid. The time of the most recent common ancestor (TMRCA) of SARS-CoV-2 suggested that the first coronavirus entered the country around 11 February 2020, as estimated from the TMRCA of B3a, the first lineage detected in the country. Moreover, earlier claims that the D614G mutation is associated to higher transmissibility is not consistent with the very high prevalence of COVID-19 in Spain when compared to other countries with lower disease incidence but much higher frequency of this mutation (56.4% in Spain vs. 82.4% in rest of Europe). Instead, the data support a major role of genetic drift in modeling the micro-geographic stratification of virus strains across the country as well as the role of SARS-CoV-2 super-spreaders.
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  • [1]
    Bandelt H-J, Forster P, Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16(1): 37−48. doi:  10.1093/oxfordjournals.molbev.a026036
    [2]
    Ceraolo C, Giorgi FM. 2020. Genomic variance of the 2019-nCoV coronavirus. Journal of Medical Virology, 92(5): 522−528. doi:  10.1002/jmv.25700
    [3]
    Colijn C, Gardy J. 2014. Phylogenetic tree shapes resolve disease transmission patterns. Evolution, Medicine, and Public Health, 2014(1): 96−108. doi:  10.1093/emph/eou018
    [4]
    Conrad O, Bechtel B, Bock M, Dietrich H, Fischer E, Gerlitz L, et al. 2015. System for automated geoscientific analyses (SAGA) v.2.1.4. Geoscientific Model Development, 8(7): 1991−2007. doi:  10.5194/gmd-8-1991-2015
    [5]
    Drummond AJ, Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7: 214. doi:  10.1186/1471-2148-7-214
    [6]
    Endo A, Abbott S, Kucharski AJ, Funk S. 2020. Estimating the overdispersion in COVID-19 transmission using outbreak sizes outside China. Wellcome Open Research, 5: 67. doi:  10.12688/wellcomeopenres.15842.3
    [7]
    Forster P, Forster L, Renfrew C, Forster M. 2020a. Phylogenetic network analysis of SARS-CoV-2 genomes. Proceedings of the National Academy of Sciences of the United States of America, 117(17): 9241−9243. doi:  10.1073/pnas.2004999117
    [8]
    Forster P, Forster L, Renfrew C, Forster M. 2020b. Reply to Sanchez-Pacheco et al., Chookajorn, and Mavian et al.: explaining phylogenetic network analysis of SARS-CoV-2 genomes. Proceedings of the National Academy of Sciences of the United States of America, 117(23): 12524−12525. doi:  10.1073/pnas.2007433117
    [9]
    Gómez-Carballa A, Bello X, Pardo-Seco J, Martinón-Torres F, Salas A. 2020. Mapping genome variation of SARS-CoV-2 worldwide highlights the impact of COVID-19 super-spreaders. Genome Research. doi:  10.1101/gr.266221.120.
    [10]
    Heled J, Drummond AJ. 2008. Bayesian inference of population size history from multiple loci. BMC Evolutionary Biology, 8: 289. doi:  10.1186/1471-2148-8-289
    [11]
    Huson DH, Bryant D. 2006. Application of phylogenetic networks in evolutionary studies. Molecular Biology and Evolution, 23(2): 254−267. doi:  10.1093/molbev/msj030
    [12]
    Kendall M, Boyd M, Colijn C. 2018-02-21. Calculating topological properties of phylogenies. https://cran.r-project.org/web/packages/phyloTop/.
    [13]
    Korber B, Fischer WM, Gnanakaran S, Yoon H, Theiler J, Abfalterer W, et al. 2020. Tracking changes in SARS-CoV-2 spike: evidence that D614G increases infectivity of the COVID-19 Virus. Cell, 182(4): 812−827. doi:  10.1016/j.cell.2020.06.043
    [14]
    Kupferschmidt K. 2020-05-19. Why do some COVID-19 patients infect many others, whereas most don’t spread the virus at all? https://www.sciencemag.org/news/2020/05/why-do-some-covid-19-patients-infect-many-others-whereas-most-don-t-spread-virus-all.
    [15]
    Leigh JW, Bryant D. 2015. POPART: full‐feature software for haplotype network construction. Methods in Ecology and Evolution, 6(9): 1110−1116. doi:  10.1111/2041-210X.12410
    [16]
    Metzig C, Ratmann O, Bezemer D, Colijn C. 2019. Phylogenies from dynamic networks. PLoS Computational Biology, 15(2): e1006761. doi:  10.1371/journal.pcbi.1006761
    [17]
    Nei M, Li WH. 1979. Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceedings of the National Academy of Sciences of the United States of America, 76(10): 5269−5273. doi:  10.1073/pnas.76.10.5269
    [18]
    Norström MM, Prosperi MCF, Gray RR, Karlsson AC, Salemi M. 2012. PhyloTempo: a set of R scripts for assessing and visualizing temporal clustering in genealogies inferred from serially sampled viral sequences. Evolutionary Bioinformatics, 8: 261−269.
    [19]
    Shen ZJ, Xiao Y, Kang L, Ma WT, Shi LS, Zhang L, et al. 2020. Genomic diversity of severe acute respiratory syndrome-coronavirus 2 in patients with coronavirus disease 2019. Clinical Infectious Diseases, 71(15): 713−720. doi:  10.1093/cid/ciaa203
    [20]
    Shu YL, McCauley J. 2017. GISAID: global initiative on sharing all influenza data - from vision to reality. Eurosurveillance, 22(13): 30494. doi:  10.2807/1560-7917.ES.2017.22.13.30494
    [21]
    Tang XL, Wu CC, Li X, Song YH, Yao XM, Wu XK, et al. 2020. On the origin and continuing evolution of SARS-CoV-2. National Science Review, 7(6): 1012−1023. doi:  10.1093/nsr/nwaa036
    [22]
    van Dorp L, Acman M, Richard D, Shaw LP, Ford CE, Ormond L, et al. 2020. Emergence of genomic diversity and recurrent mutations in SARS-CoV-2. Infection, Genetics and Evolution, 83: 104351. doi:  10.1016/j.meegid.2020.104351
    [23]
    WHO. 2020. WHO Director-General's opening remarks at the media briefing on COVID-19 – 11 March 2020.
    [24]
    Wong G, Bi YH, Wang QH, Chen XW, Zhang ZG, Yao YG. 2020. Zoonotic origins of human coronavirus 2019 (HCoV-19 / SARS-CoV-2): why is this work important?. Zoological Research, 41(3): 213−219. doi:  10.24272/j.issn.2095-8137.2020.031
    [25]
    Yu WB, Tang GD, Zhang L, Corlett RT. 2020. Decoding the evolution and transmissions of the novel pneumonia coronavirus (SARS-CoV-2 / HCoV-19) using whole genomic data. Zoological Research, 41(3): 247−257. doi:  10.24272/j.issn.2095-8137.2020.022
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