Phylodynamics of SARS-CoV-2 in France, Europe and the world in 2020

  1. Romain Coppée  Is a corresponding author
  2. François Blanquart
  3. Aude Jary
  4. Valentin Leducq
  5. Valentine Marie Ferré
  6. Anna Maria Franco Yusti
  7. Léna Daniel
  8. Charlotte Charpentier
  9. Samuel Lebourgeois
  10. Karen Zafilaza
  11. Vincent Calvez
  12. Diane Descamps
  13. Anne-Geneviève Marcelin
  14. Benoit Visseaux
  15. Antoine Bridier-Nahmias  Is a corresponding author
  1. Université Paris Cité and Sorbonne Paris Nord, Inserm, IAME, France
  2. Collège de France, France
  3. Sorbonne Université, Inserm, iPLESP, France
  4. Hôpital Bichat-Claude-Bernard, France

Abstract

Although France was one of the most affected European countries by the COVID-19 pandemic in 2020, the dynamics of SARS-CoV-2 movement within France, but also involving France in Europe and in the world, remain only partially characterized in this timeframe. Here, we analyzed GISAID deposited sequences from 1st January to 31th December 2020 (n = 638,706 sequences at the time of writing). To tackle the challenging number of sequences without the bias of analyzing a single subsample of sequences, we produced 100 subsamples of sequences and related phylogenetic trees from the whole dataset for different geographic scales (worldwide, European countries and French administrative regions) and time periods (from 1st January to 25th July 2020, and from 26th July to 31th December 2020). We applied a maximum likelihood discrete trait phylogeographic method to date exchange events (i.e., a transition from one location to another one), to estimate the geographic spread of SARS-CoV-2 transmissions and lineages into, from and within France, Europe and the world. The results unraveled two different patterns of exchange events between the first and second half of 2020. Throughout the year, Europe was systematically associated with most of the intercontinental exchanges. SARS-CoV-2 was mainly introduced into France from North America and Europe (mostly by Italy, Spain, United Kingdom, Belgium and Germany) during the first European epidemic wave. During the second wave, exchange events were limited to neighboring countries without strong intercontinental movement, but Russia widely exported the virus into Europe during the summer of 2020. France mostly exported B.1 and B.1.160 lineages, respectively during the first and second European epidemic waves. At the level of French administrative regions, the Paris area was the main exporter during the first wave. But, for the second epidemic wave, it equally contributed to virus spread with Lyon area, the second most populated urban area after Paris in France. The main circulating lineages were similarly distributed among the French regions. To conclude, by enabling the inclusion of tens of thousands of viral sequences, this original phylodynamic method enabled us to robustly describe SARS-CoV-2 geographic spread through France, Europe and worldwide in 2020.

Data availability

All genome sequences and associated metadata in the dataset are published in GISAID's EpiCoV database. To view the contributors of each individual sequence with details such as accession number, virus name, collection date, originating lab and submitting lab and the list of authors, visit: https://doi.org/10.55876/gis8.230120zd.All the scripts developed for this study were deposited in the following GitHub repository: https://github.com/Rcoppee/PhyloCoV

Article and author information

Author details

  1. Romain Coppée

    Université Paris Cité and Sorbonne Paris Nord, Inserm, IAME, Paris, France
    For correspondence
    romain.coppee@inserm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3024-5928
  2. François Blanquart

    Centre for Interdisciplinary Research in Biology, Collège de France, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0591-2466
  3. Aude Jary

    Sorbonne Université, Inserm, iPLESP, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Valentin Leducq

    Sorbonne Université, Inserm, iPLESP, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Valentine Marie Ferré

    Service de Virologie, Hôpital Bichat-Claude-Bernard, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Anna Maria Franco Yusti

    Université Paris Cité and Sorbonne Paris Nord, Inserm, IAME, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Léna Daniel

    Université Paris Cité and Sorbonne Paris Nord, Inserm, IAME, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  8. Charlotte Charpentier

    Service de Virologie, Hôpital Bichat-Claude-Bernard, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Samuel Lebourgeois

    Université Paris Cité and Sorbonne Paris Nord, Inserm, IAME, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  10. Karen Zafilaza

    Sorbonne Université, Inserm, iPLESP, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Vincent Calvez

    Sorbonne Université, Inserm, iPLESP, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  12. Diane Descamps

    Service de Virologie, Hôpital Bichat-Claude-Bernard, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  13. Anne-Geneviève Marcelin

    Sorbonne Université, Inserm, iPLESP, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  14. Benoit Visseaux

    Service de Virologie, Hôpital Bichat-Claude-Bernard, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  15. Antoine Bridier-Nahmias

    Université Paris Cité and Sorbonne Paris Nord, Inserm, IAME, Paris, France
    For correspondence
    antoine.bridier-nahmias@inserm.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0376-6840

Funding

No external funding was received for this work.

Copyright

© 2023, Coppée et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 764
    views
  • 114
    downloads
  • 4
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Romain Coppée
  2. François Blanquart
  3. Aude Jary
  4. Valentin Leducq
  5. Valentine Marie Ferré
  6. Anna Maria Franco Yusti
  7. Léna Daniel
  8. Charlotte Charpentier
  9. Samuel Lebourgeois
  10. Karen Zafilaza
  11. Vincent Calvez
  12. Diane Descamps
  13. Anne-Geneviève Marcelin
  14. Benoit Visseaux
  15. Antoine Bridier-Nahmias
(2023)
Phylodynamics of SARS-CoV-2 in France, Europe and the world in 2020
eLife 12:e82538.
https://doi.org/10.7554/eLife.82538

Share this article

https://doi.org/10.7554/eLife.82538

Further reading

    1. Epidemiology and Global Health
    2. Genetics and Genomics
    Rashmi Sukumaran, Achuthsankar S Nair, Moinak Banerjee
    Research Article

    Burden of stroke differs by region, which could be attributed to differences in comorbid conditions and ethnicity. Genomewide variation acts as a proxy marker for ethnicity, and comorbid conditions. We present an integrated approach to understand this variation by considering prevalence and mortality rates of stroke and its comorbid risk for 204 countries from 2009 to 2019, and Genome-wide association studies (GWAS) risk variant for all these conditions. Global and regional trend analysis of rates using linear regression, correlation, and proportion analysis, signifies ethnogeographic differences. Interestingly, the comorbid conditions that act as risk drivers for stroke differed by regions, with more of metabolic risk in America and Europe, in contrast to high systolic blood pressure in Asian and African regions. GWAS risk loci of stroke and its comorbid conditions indicate distinct population stratification for each of these conditions, signifying for population-specific risk. Unique and shared genetic risk variants for stroke, and its comorbid and followed up with ethnic-specific variation can help in determining regional risk drivers for stroke. Unique ethnic-specific risk variants and their distinct patterns of linkage disequilibrium further uncover the drivers for phenotypic variation. Therefore, identifying population- and comorbidity-specific risk variants might help in defining the threshold for risk, and aid in developing population-specific prevention strategies for stroke.

    1. Epidemiology and Global Health
    2. Evolutionary Biology
    Renan Maestri, Benoît Perez-Lamarque ... Hélène Morlon
    Research Article

    Several coronaviruses infect humans, with three, including the SARS-CoV2, causing diseases. While coronaviruses are especially prone to induce pandemics, we know little about their evolutionary history, host-to-host transmissions, and biogeography. One of the difficulties lies in dating the origination of the family, a particularly challenging task for RNA viruses in general. Previous cophylogenetic tests of virus-host associations, including in the Coronaviridae family, have suggested a virus-host codiversification history stretching many millions of years. Here, we establish a framework for robustly testing scenarios of ancient origination and codiversification versus recent origination and diversification by host switches. Applied to coronaviruses and their mammalian hosts, our results support a scenario of recent origination of coronaviruses in bats and diversification by host switches, with preferential host switches within mammalian orders. Hotspots of coronavirus diversity, concentrated in East Asia and Europe, are consistent with this scenario of relatively recent origination and localized host switches. Spillovers from bats to other species are rare, but have the highest probability to be towards humans than to any other mammal species, implicating humans as the evolutionary intermediate host. The high host-switching rates within orders, as well as between humans, domesticated mammals, and non-flying wild mammals, indicates the potential for rapid additional spreading of coronaviruses across the world. Our results suggest that the evolutionary history of extant mammalian coronaviruses is recent, and that cases of long-term virus–host codiversification have been largely over-estimated.