Bats unmasked: Delving into diversity and disease dynamics
We are witnessing an alarming trend of biodiversity loss and a rise of infectious diseases with human encroachment likely to blame. In 2023, at least 21 known species were declared extinct in the wild, while avian influenza A viruses rampaged through global bird populations. Yet, biodiversity loss is often a poorly suited term to describe the effects of human disturbance, because, in many cases, diversity does not decline immediately or even as steeply as one might expect. Instead, ecologists observe a change in the composition of species. Certain taxa may profit from human disturbance that removes competitors or predators, and novel, often non-native taxa can take hold. In turn, this raises the possibility that pathogens spread among biologically depauperated communities and spillover to new host species.
Understanding what is lost one requires knowing what was originally present (Figure 1). The risk of extinction becomes particularly daunting in animal groups that are poorly studied or contain many cryptic species, where morphological similarities conceal evolutionary (i.e., genetic) differences. This poses a challenge for ecologist and conservationists alike. At times, there are entire sweeps of species that form a cryptic species complex. Some bat families, for example, are known for their high cryptic diversity and among those members of the family of Hipposideridae are particularly arduous to distinguish. Bat ecologist even utilize the distinct echolocation frequencies to differentiate bat species, but to no avail in many tropical Hipposiderids.
© Marco Tschapka
Figure 1. Photos of Ghanaian hipposiderids casually hanging from the ceiling of one of the cave sites.
The cryptic Sub-Saharan Hipposideros complex
In the current paper we study Sub-Saharan Hipposiderids, loosely grouped as the morphologically cryptic Hipposideros caffer complex (Figure 2). Despite their genetic and ecological distinctiveness and varying distributions throughout Africa, their ranges overlap in Ghana, where our study took place. What drew our attention to this species complex was the fact that in earlier virus discovery studies the complex was most frequently detected positive for the two SARS-related beta-coronaviruses (CoVs) and an alpha-CoV closely related to the human common cold agent HCoV-229E. We therefore were curious whether infection likelihood differed between members of this species complex, and, if this was the case, the abundances of competent hosts, i.e., susceptible species, predicted CoV prevalence over time. Luckily, all prior sampling schemes took miniscule amounts of wing tissue to differentiate bats genetically.
© Heather J. Baldwin
Figure 2. Photos of bats belonging to the cryptic species complex Hipposideros caffer. The bats may exhibit different colors. Based solely on external features such as size, weight, or wing length, they cannot be distinguished from each other, but genetically. Each line represents a different species. A-D: Hipposideros caffer tephrus, E-H: Hipposideros caffer B, I-L: Hipposideros caffer C, M-P: Hipposideros caffer D.
Linking host species to coronavirus infection
In total, more than 2,300 bats across five caves in central Ghana were non-invasively sampled bi-monthly between August 2010 to August 2012. Employing molecular techniques, we then characterized the mitochondrial cytochrome b gene from the DNA extracted from the wing punches and sorted samples into Hipposideros caffer B to D (Figure 2, E-P). When we matched this new host species information with virus data obtained from the fecal samples collected during the same sampling period, we were intrigued to find out that the species were infected asymmetrically. Hipposideros caffer D, for example, seemed more often infected with the SARS-related beta-CoV 2b and the exclusive host species to the other SARS-related beta-CoV 2bBasal.
What determined coronavirus prevalence?
We then statistically enquired from our data whether for each sampling time point and cave site the diversity of bat species present, the relative abundance of common host species and the proportion of juvenile bats explain infection likelihood. One of the key findings of our work is that the higher the abundance of Hipposideros caffer D the more likely bats sampled were infected with one of the SARS-related beta-CoVs. By contrast, the relative abundance of Hipposideros caffer C predicted infection likelihood with the HCoV-related alpha-CoV 229E-like (Figure 3). We inferred from this that Hipposideros caffer D is a more competent host and the likely reservoir to the SARS-related beta-CoV, whereas the same was true for Hipposideros caffer C with respect to the HCoV-like alpha-CoV.
Figure 3. Infection likelihood with the alpha-CoV 229E-like increases the more Hipposideros (H.) caffer C are co-roosting with other bats and similarly, infection likelihood with the beta-CoV 2b rises when more Hipposideros caffer D are present.
More broadly, we also draw a negative relationship between the overall species diversity of the bat assemblages at each time point and the prevalence of each virus. However, this relationship is to be interpreted in the context of the community assemblage. Incorporating the relative abundance of each host species improved the performance and variance explained by each model suggesting that the enrichment of competent hosts at the expense of non-competent hosts in less species diverse bat communities is a driving factor in this relationship. In a nutshell, in species poor bat communities more susceptible hosts seem to dominate and, hence, increase coronavirus prevalence.
Protecting bat diversity is a pandemic prevention strategy
Our findings underscore the importance of deciphering the taxonomy of putative virus reservoirs, may that be bats or other animal groups. Our study therefore aligns itself with recent calls to standardize sampling and reporting in virus discovery studies and we add that high taxonomic resolution of host taxa should be the gold standard. The implications of our research extend to both conservation efforts and disease management strategies. Understanding how species assemblages influence disease dynamics enhances our ability to predict and mitigate infectious disease spread. This safeguards both wildlife and humans.
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