Cross-Species Transmission of Bat Coronaviruses in the Americas: Contrasting Patterns between Alphacoronavirus and Betacoronavirus

Abstract

Bats harbor the largest number of coronavirus (CoV) species among mammals, serving as major reservoirs of alphaCoVs and betaCoVs, which can jump between bat species or to different mammalian hosts, including humans. Bat-CoV diversity is correlated with host taxonomic diversity, with the highest number of CoV species found in areas with the highest levels of bat species richness. Although the Americas harbor a unique and distinctive CoV diversity, no cross-species transmission (CST) or phylogeographic analysis has yet been performed. This study analyzes a large sequence data set from across the Americas through a Bayesian framework to understand how codivergence and cross-species transmission have shaped long-term bat-CoV evolution and ultimately identify bat hosts and regions where the risk of CST is the highest. Substantial levels of CST were found only among alphaCoVs. In contrast, cospeciation prevailed along the evolution of betaCoVs. Brazil is the center of diversification for both alpha and betaCoVs, with the highest levels of bat species richness. The bat family Phyllostomidae has played a key role in the evolution of American bat-CoVs, supported by the highest values of host transition rates. Although the conclusions drawn from this study are supported by biological/ecological evidence, it is likely that novel lineages will be discovered, which could also reveal undetected CSTs given that sequences are available from 11 of the 35 countries encompassing the Americas. The findings of this study can be useful for conducting targeted discovery of bat-CoVs in the region, especially in countries of the Americas with no reported sequences. IMPORTANCE Coronaviruses (CoVs) have a strong zoonotic potential due to their high rates of evolvability and their capacity for overcoming host-specific barriers. Bats harbor the largest number of CoV species among mammals, with the highest CoV diversity found in areas with the highest levels of bat species richness. Understanding their origin and patterns of cross-species transmission is crucial for pandemic preparedness. This study aims to understand how bat-CoVs diversify in the Americas, circulate among and transmit between bat families and genera, and ultimately identify bat hosts and regions where the risk of CoV spillover is the highest.

Keywords: bats; codivergence; coronavirus; cross-species transmission; host shift; phylogeny; spillover; virus.

FIG 1

American bat-CoVs in the context of global CoV diversity. Bayesian phylogeny showing global alpha, beta, delta, and gammacoronavirus. Sequences of American bat-CoVs are shown in blue (alphaCoVs) and purple (betaCoVs). Seven monophyletic American bat alphaCoVs are shown with letters A to G, and subclades of the major lineage G are shown with numbers 1 to 4. Nodes with Bayesian posterior probability >0.9 are shown in red. The scale bar is expressed in substitutions/site.

FIG 2

Ancestral host reconstruction of alphaCoVs and betaCoVs. Maximum clade credibility trees annotated using partial RdRp sequences and bat host genus as discrete character state. Branch colors correspond to the inferred ancestral bat genus with the highest posterior probability. Relevant nodes with posterior probability >0.9 are indicated with pink circles.

FIG 3

Cophylogeny plot of bat species phylogeny and alphaCoVs tree. Cyt b-based bat species phylogeny (left) and alphaCoVs phylogeny (right). Gray circles indicate bat families (M, Molossidae; V, Vespertilionidae; P, Phyllostomidae) and main alphaCoV lineages and sublineages (A to G). Bat-CoV links are colored by each bat family. Dotted lines in the alphaCoV phylogeny depict nonsupported clusterings.

FIG 4

Host transition rates among American bat genera. Strongly supported host switches between bat genera for alphaCoVs (left) and betaCoVs (right). Line color indicates the switch significance level according to the Bayes factor test. Genus color indicates host family (green, Molossidae; red, Phyllostomidae; blue, Vespertilionidae; purple, Mormoopidae).

FIG 5

Cophylogeny plot of bat species phylogeny and betaCoVs tree. Cyt b-based bat species phylogeny (left) and alphaCoVs phylogeny (right). Bat-CoV links are colored by each bat family (blue, Mormoopidae; green, Molossidae; red-yellow-brown, Phyllostomidae). Dotted lines in the betaCoV phylogeny depict nonsupported clusterings.

FIG 6

Phylogenetic reconciliation between betaCoVs and bat hosts trees. Maximum parsimony reconciliation (left) proposed for the cost region a (upper right) and its significance by randomization tests (lower left). Cospeciations and duplications/losses but not host switching took place in the evolution of betaCoVs. The MPR obtained under scheme b (not shown) was not significantly different from the randomized MPR distribution.

FIG 7

Bat species distributions. Global bat species distributions (top) and distribution of bat-CoV hosts in the Americas (bottom). Geographical ranges of bat species were obtained from the International Union for Conservation of Nature (IUCN). The plots display the number of bat species based on overlapping geographical ranges from a total of 1,317 species with IUCN range data as of March 2022.