Interplay between co-divergence and cross-species transmission in the evolutionary history of bat coronaviruses

Abstract

Coronaviruses (CoVs) have been documented in almost every species of bat sampled. Bat CoVs exhibit both extensive genetic diversity and a broad geographic range, indicative of a long-standing host association. Despite this, the respective roles of long-term virus-host co-divergence and cross-species transmission (host-jumping) in the evolution of bat coronaviruses are unclear. Using a phylogenetic approach we provide evidence that CoV diversity in bats is shaped by both species richness and their geographical distribution, and that CoVs exhibit clustering at the level of bat genera, with these genus-specific clusters largely associated with distinct CoV species. Co-phylogenetic analyses revealed that cross-species transmission has been more common than co-divergence across coronavirus evolution as a whole, and that cross-species transmission events were more likely between sympatric bat hosts. Notably, however, an analysis of the CoV RNA polymerase phylogeny suggested that many such host-jumps likely resulted in short-term spill-over infections, with little evidence for sustained onward transmission in new co-roosting host species.

Keywords: Bats; Coronaviruses; Cross-species transmission; Evolution; Phylogeny co-divergence; Virus.

Fig. 1

Host association and geographical distribution of the CoV sequences analyzed here. Countries within large-scale geographical regions are colored according to the number of CoV analyzed. Pie charts indicate the host-association of the CoV sequences included within each geographical area, with the colors indicating the different families of bat hosts. The map was built using mapchart (https://mapchart.net).

Fig. 2

Phylogenetic overview of CoV sequences analyzed here. The tree reflects a Bayesian analysis of 935 bp of the RdRp gene (data set RdRp_CoV_1), rooted using two sequences from gamma coronaviruses (GenBank accession numbers EF584911-2). Genus specific clusters identified in our study are colored based on the host genus, as indicated. Posterior probabilities >0.90 supporting each cluster are shown. Branch lengths are scaled according to the number of substitutions per site. The three bars around the tree show the frequency within each cluster of (i) host genera, (ii) host species and (iii) sampling locations, from the innermost to the most exterior. Sequences showing characters with frequency < 10%, between 10 and 50%, and >50% are colored black, grey and light grey, respectively. For the “host species” bar, only sequences belonging to the host genus characterizing the cluster (frequency > 50%) have been colored; sequences associated with hosts only characterized at the genus level are indicated in yellow. The ICTV classification of virus clusters is indicated when available. The figure was generated using iTOL.