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Review
. 2022 May;20(5):299-314.
doi: 10.1038/s41579-021-00652-2. Epub 2021 Nov 19.

Ecology, evolution and spillover of coronaviruses from bats

Manuel Ruiz-Aravena #  1 , Clifton McKee #  2 , Amandine Gamble  3 , Tamika Lunn  4 , Aaron Morris  5 , Celine E Snedden  3 , Claude Kwe Yinda  6 , Julia R Port  6 , David W Buchholz  7 , Yao Yu Yeo  7 , Christina Faust  8 , Elinor Jax  5 , Lauren Dee  5 , Devin N Jones  1 , Maureen K Kessler  1   9 , Caylee Falvo  1 , Daniel Crowley  1 , Nita Bharti  8 , Cara E Brook  10 , Hector C Aguilar  7 , Alison J Peel  4 , Olivier Restif  5 , Tony Schountz  11 , Colin R Parrish  7 , Emily S Gurley  2 , James O Lloyd-Smith  3 , Peter J Hudson  8 , Vincent J Munster  6 , Raina K Plowright  12
Affiliations
Review

Ecology, evolution and spillover of coronaviruses from bats

Manuel Ruiz-Aravena et al. Nat Rev Microbiol. 2022 May.

Erratum in

  • Author Correction: Ecology, evolution and spillover of coronaviruses from bats.
    Ruiz-Aravena M, McKee C, Gamble A, Lunn T, Morris A, Snedden CE, Yinda CK, Port JR, Buchholz DW, Yeo YY, Faust C, Jax E, Dee L, Jones DN, Kessler MK, Falvo C, Crowley D, Bharti N, Brook CE, Aguilar HC, Peel AJ, Restif O, Schountz T, Parrish CR, Gurley ES, Lloyd-Smith JO, Hudson PJ, Munster VJ, Plowright RK. Ruiz-Aravena M, et al. Nat Rev Microbiol. 2022 May;20(5):315. doi: 10.1038/s41579-022-00691-3. Nat Rev Microbiol. 2022. PMID: 35027705 Free PMC article. No abstract available.

Abstract

In the past two decades, three coronaviruses with ancestral origins in bats have emerged and caused widespread outbreaks in humans, including severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Since the first SARS epidemic in 2002-2003, the appreciation of bats as key hosts of zoonotic coronaviruses has advanced rapidly. More than 4,000 coronavirus sequences from 14 bat families have been identified, yet the true diversity of bat coronaviruses is probably much greater. Given that bats are the likely evolutionary source for several human coronaviruses, including strains that cause mild upper respiratory tract disease, their role in historic and future pandemics requires ongoing investigation. We review and integrate information on bat-coronavirus interactions at the molecular, tissue, host and population levels. We identify critical gaps in knowledge of bat coronaviruses, which relate to spillover and pandemic risk, including the pathways to zoonotic spillover, the infection dynamics within bat reservoir hosts, the role of prior adaptation in intermediate hosts for zoonotic transmission and the viral genotypes or traits that predict zoonotic capacity and pandemic potential. Filling these knowledge gaps may help prevent the next pandemic.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Geographical and taxonomic distribution of reported bat hosts of coronaviruses.
a | Biogeographical patterns of bat families, sampling and coronavirus host status. b | Bat taxonomic diversity and coronavirus testing results. Data were compiled from field studies involving sequencing of coronaviruses in wild bats. A list of all reported bat coronavirus hosts based on the reviewed studies can be found in Supplementary Table 1 and Supplementary data. ‘Named’ refers to the number of taxonomically described bat species per family based on the expert-curated Bat Species of the World database. Bat Species of the World database. CoVs, coronaviruses.
Fig. 2
Fig. 2. Geographical distribution of reported bat hosts of coronaviruses.
Data on bat hosts were compiled from field studies involving sequencing of coronaviruses in wild bats. Where phylogenetic analysis was included in studies, key Alphacoronavirus and Betacoronavirus subgenera of bats associated with human or domestic animal infections or well characterized in bats (for example, Hibecovirus and Nobecovirus) are summarized (see Supplementary data). Geographical ranges of reported bat host species for any coronaviruses or key subgenera were obtained from the International Union for Conservation of Nature (IUCN). The plots display the number of bat species based on overlapping geographical ranges. The plots of bat species include 1,317 species with IUCN range data as of September 2021. Patterns in the left-hand maps indicate that sampling of bat species largely reflects the biogeographical patterns of bat diversity, with hotspots in Central America, South America, equatorial Africa and South-East Asia. However, hotspots of bat hosts of coronaviruses display important differences: lower than expected diversity of hosts in South America and higher diversity of hosts in South-East Asia. Although biological differences in bat coronavirus interactions with certain bat families (for example, Rhinolophidae) might explain some of these patterns, small sample sizes in some species in the Americas and more intensive sampling in China and South-East Asia likely contribute as well.
Fig. 3
Fig. 3. Coronavirus taxonomy and host distribution.
The proposed phylogeny has been compiled from analyses of full genomes and/or gene segments. Branch lengths do not reflect evolutionary distance between taxa and are drawn only to clearly illustrate relationships between and within genera. The distribution of bat species hosting highlighted subgenera is given in Fig. 2. The associated table summarizes a selection of important pathogenic virus species within genera and the host species or taxa with reported infections of a virus within a genus. BCoV, bovine coronavirus; CCoV, canine coronavirus; CRCoV, canine respiratory coronavirus; FCoV, feline coronavirus; HCoV, human coronavirus; IBV, infectious bronchitis virus (avian coronavirus); MCoV, murine coronavirus; MERS, Middle East respiratory syndrome; Myl-CoV, Myotis lucifugus coronavirus; PEDV, porcine epidemic diarrhoea virus: PorCoV, porcine coronavirus; SADS-CoV, swine acute diarrhoea syndrome coronavirus; SARS-CoV, severe acute respiratory syndrome coronavirus; TGEV, transmissible gastroenteritis virus.
Fig. 4
Fig. 4. Prevalence of detection of bat coronaviruses in field samples.
Data were obtained from published studies that included two or more sampling events with at least ten samples collected and that reported the virological status of samples (positive and negative). While the data show that prevalence varies in space and time and by bat species (each plot), few studies provide insights into the drivers of prevalence. No field studies have yet combined longitudinal sampling of individuals with collection of extensive metadata on bat ecology, bat health and environmental conditions. Sampling designs differed across studies. Most studies conducted cross-sectional sampling over multiple years. One field study sampled individual bats at multiple sites over time, although data were pooled across three sites (panel a). Other studies sampled the same bat species over time across multiple sites or sampled multiple species and individuals in pooled samples across time within a site. These sampling approaches reflect the purpose of the studies — most were focused on characterizing viral diversity, not infection dynamics. Details are presented in Supplementary information. Each plot represents the prevalence of detections per bat species: Pteropus lylei (panel a); Eonycteris spelaea (panel b); Rousettus leschenaultii (panel c); Chaerephon pumilus (panel d); Eidolon helvum (panel e); Myonycteris angolensis (panel f); Rhinolophus cf. clivosus (panel g); Myotis daubentonii (panel h); Rhinolophus sinicus (panel i); Rhinolophus sinicus, Rhinolophus ferrumequinum, Rhinolophus affinis and Aselliscus stoliczkanus (panel j); and Myotis myotis (panel k). Colours in the plots represent different years within the study: year 1, red; year 2, blue; year 3, green; year 4, purple; and year 5, orange. Black asterisks show sampling events in which no coronavirus was detected. Circles show the mean prevalence, and bars show the 95% confidence intervals estimated by the Wilson method.
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