Recent evolutionary origin and localized diversity hotspots of mammalian coronaviruses

Author:

Maestri Renan12ORCID,Perez-Lamarque Benoît13ORCID,Zhukova Anna4,Morlon Hélène1

Affiliation:

1. Institut de Biologie de l'École Normale Supérieure (IBENS), École Normale Supérieure, CNRS, INSERM, Université PSL

2. Departamento de Ecologia, Instituto de Biociências, Universidade Federal do Rio Grande do Sul

3. Institut de Systématique, Évolution, Biodiversité (ISYEB), Muséum national d’histoire naturelle, CNRS, Sorbonne Université, EPHE, UA

4. Institut Pasteur, Université Paris Cité, Bioinformatics and Biostatistics Hub

Abstract

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.

Funder

GENCI-IDRIS

One Health/Make Our Planet Great Again Program

Publisher

eLife Sciences Publications, Ltd

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