Viral Co-Infection in Bats: A Systematic Review

Abstract

Co-infection is an underappreciated phenomenon in contemporary disease ecology despite its ubiquity and importance in nature. Viruses, and other co-infecting agents, can interact in ways that shape host and agent communities, influence infection dynamics, and drive evolutionary selective pressures. Bats are host to many viruses of zoonotic potential and have drawn increasing attention in their role as wildlife reservoirs for human spillover. However, the role of co-infection in driving viral transmission dynamics within bats is unknown. Here, we systematically review peer-reviewed literature reporting viral co-infections in bats. We show that viral co-infection is common in bats but is often only reported as an incidental finding. Biases identified in our study database related to virus and host species were pre-existing in virus studies of bats generally. Studies largely speculated on the role co-infection plays in viral recombination and few investigated potential drivers or impacts of co-infection. Our results demonstrate that current knowledge of co-infection in bats is an ad hoc by-product of viral discovery efforts, and that future targeted co-infection studies will improve our understanding of the role it plays. Adding to the broader context of co-infection studies in other wildlife species, we anticipate our review will inform future co-infection study design and reporting in bats. Consideration of detection strategy, including potential viral targets, and appropriate analysis methodology will provide more robust results and facilitate further investigation of the role of viral co-infection in bat reservoirs.

Keywords: chiroptera; co-infection; coinfection; review; viral co-infection; viral dynamics; wildlife.

Figure 1

PRISMA flowchart depicting each step of the literature search and screening process. Full detail of all 117 studies included from the search provided in Table S1.

Figure 2

Publication of multi-viral studies in bats over time, showing the number of papers across the full database, grouped by whether co-infection was detected or not.

Figure 3

Number of publications involving each viral and bat host family in the database, grouped by whether co-infection was detected or not. (a) Viral families. (b) Host families.

Figure 4

Boxplots depicting the median co-infected proportion and interquartile range described by the 25th and 75th percentiles of all studies in the database that detected co-infection, stratified by the continent the bats were sampled from, the viral detection strategy used (PCR, viral isolation (VI) or next-generation sequencing (NGS)), and the individual viral and host family. Co-infected proportion represents the proportion of positive individuals from each stratum that were co-infected. (a) Sampling location (continent). (b) Detection assays used. (c) Viral family. (d) Host family.

Figure 5

Heat map displaying the screening effort and detection of each pairwise viral family combination recorded in the database. The bar chart on the right displays the number of individual bats tested or infected with the viral family for each row. The heat map then displays the proportion of those individuals tested or infected with the viral family on each column. Values used to generate the plot are from Tables S3 and S4. (a) Screening effort. (b) Co-infections detected. Grey cells are combinations not tested for. Columns and rows are grouped by virus genome structure. The same viral families, in full and abbreviated form, are on the x and y axis, in identical order.

Figure 6

Heat map displaying the screening effort and detection of each pairwise host and viral family combination recorded in the database. The bar chart on the right displays the number of individual bats tested or infected from each host family for each row. The heat map then displays the proportion of those individuals tested or co-infected with the viral family on each column. Values used to generate the plot are from Tables S5 and S6. (a) Screening effort. (b) Co-infections detected. Grey cells are combinations not tested for. Columns and rows are grouped by virus genome structure. The same viral families, in abbreviated form, are present in Figure 5.

Figure 7

Network plot of themes discussed in the database. Each node is labelled with the description of a theme discussed in the publications in the database. The size of the node illustrates the number of publications discussing the corresponding theme, and the colour of the node corresponds to the broader classification the theme belongs to: drivers, mechanisms, outcomes. Themes that are discussed together in the same publication are connected by a line (edge). The thickness of the edge corresponds to the number of publications discussing the connected themes together.