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Revealing the complexity of vampire bat rabies “spillover transmission”

Infectious Diseases of Poverty volume 12, Article number: 10 (2023) Cite this article

Abstract

Background

The term virus ‘spillover’ embodies a highly complex phenomenon and is often used to refer to viral transmission from a primary reservoir host to a new, naïve yet susceptible and permissive host species. Spillover transmission can result in a virus becoming pathogenic, causing disease and death to the new host if successful infection and transmission takes place.

Main text

The scientific literature across diverse disciplines has used the terms virus spillover, spillover transmission, cross-species transmission, and host shift almost indistinctly to imply the complex process of establishment of a virus from an original host (source/donor) to a naïve host (recipient), which have close or distant taxonomic or evolutionary ties. Spillover transmission may result in unsuccessful onward transmission, if the virus dies off before propagation. Alternatively, successful viral establishment in the new host can occur if subsequent secondary transmission among individuals of the same novel species and among other sympatric susceptible species occurred. As such, virus spillover transmission is a common yet highly complex phenomenon that encompasses multiple subtle stages that can be deconstructed to be studied separately to better understand the drivers of disease emergence. Rabies virus (RABV) is a well-documented viral pathogen which still inflicts heavy impact on humans, companion animals, wildlife, and livestock throughout Latin America due substantial spatial temporal and ecological—natural and expansional—overlap with several virus reservoir hosts. Thereby, the rabies disease system represents a robust avenue through which the drivers and uncertainties surrounding spillover transmission can be unravel at its different subtle stages to better understand how they may be affected by coarse, medium, and fine scale variables.

Conclusions

The continued study of viral spillover transmission necessitates the elucidation of its complexities to better assess the cross-scale impacts of ecological forces linked to the propensity of spillover success. Improving capacities to reconstruct and predict spillover transmission would prevent public health impacts on those most at risk populations across the globe.

Graphical Abstract:

Background

Viruses have interacted with their hosts for at least thousands of years [1]. Indeed, most viruses are expected to be host-specialists—infecting a single host species, instead of host-generalists—infecting multiple host species [2]. This long-term host-virus relationship allows the virus to induce negligible damage to its host in a process-termed co-evolution [3]. Thus, host-virus co-evolution facilitates coexistence by reducing reciprocal harm: viruses modulate their virulence against the host and hosts modulate their immune response against the virus [4]. A stable host-virus relationship, however, can be disrupted by external forces, causing the manifestation of disease (i.e., detrimental effect of the virus over the host). Cross-species virus transmission, from the original host to a new host, occurs in fish, plants, and wildlife, which has also been referred as spillover transmission. Using an ecological framework, this comment article reveals the inherent complexities of spillover transmission, strictly defined as the processes that allow cross-species transmission of viruses causing disease (i.e., pathogens) in humans (i.e., zoonotic pathogens; Box 1). Nevertheless, the rationale could be useful for non-zoonotic and non-directly transmitted viruses and other infectious agents.

More than 75% of emerging infectious diseases in humans have originated from spillover transmission events between hosts that do not share obvious evolutionary histories [5]. Thus, it has been proposed that evolutionary biology alone has failed to anticipate emerging infectious diseases [6]. This failure could be due in part to the confirmation bias of spillover transmission studies which have been historically focused on (1) viruses that had successfully established in a naïve host causing the emergence of novel transmission cycles, (2) viruses that are virulent to a naïve yet susceptible host causing conspicuous disease, and (3) zoonotic viruses [7,8,9,10]. Nevertheless, during spillover transmission events wildlife viruses are not guaranteed to establish in a naïve host, and may or may not affect humans in a negative way [10]. Thus, identifying or revealing factors at different scales of complexity associated with spillover transmission is key for the better understanding and forecasting of disease emergence.

Defining spillover transmission

The transmission of a virus from one species to another is termed “spillover transmission” [10, 11]. As such, “virus spillover” is a correct term commonly used in epidemiology of zoonoses to refer to cross-species or interspecies transmission events. “Disease spillover”, in contrast, is an incorrect term commonly used in the gray literature, to refer to the same phenomenon. Disease spillover is an erroneous use of the spillover term because diseases per se cannot be transmitted, only their causative agents (e.g., viruses). Many emerging infectious diseases have originated via spillover transmission of viruses from an original or primary wildlife hosts (i.e., reservoir host) to new, naïve domestic animal hosts followed by successful onward intraspecific transmission (Fig. 1). In some instances, wide host-range viruses transmitted from wildlife to domestic animals can reach humans through a secondary spillover transmission event (i.e., spillover transmission from new hosts, instead of the original host). For example, outbreaks from spillover transmission in the last two decades include: rabies virus (RABV; Lyssavirus) from vampire bats to cattle in Latin America [12, 13], swine acute diarrhea syndrome coronavirus (SADS-CoV; Alphacoronavirus) from Rhinolophus spp. bats to pigs in China [14], Nipah virus (Henipavirus) from flying-fox bats to pigs in Bangladesh [15, 16], Marburg virus from the African fruit bat (Rousettus aegyptiacus) to primates in Africa, severe acute respiratory syndrome coronavirus (SARS-CoV or SARS-CoV-1; Betacoronavirus) from bats to palm civets [17], Middle-East respiratory syndrome (MERS-CoV; Betacoronavirus) from bats to camels in the Middle East [18,19,20], Hendra virus (HeV; Henipavirus) from flying-fox bats to horses in Australia [21], and severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2; Betacoronavirus) from bats to a yet unknown secondary host in Southeast Asia [22,23,24,25] (Fig. 1).

Fig. 1
figure 1

Recent spillover transmission events. A native reservoir serves as the source of a virus to other host species, in which it could be virulent. This accidental cross-species transmission (i.e., spillover transmission) (red arrows), occurs between host species without evolutionary relatedness. Spillover transmission between two genetically unrelated species has been documented in recent emerging infectious where a pathogen from an original wildlife host (left) is transmitted (primary spillover; red arrows on the left) to another wildlife or domestic species (middle), and from them to a human (secondary spillover; right). SADS-CoV: swine acute diarrhea syndrome coronavirus. SARS-CoV: severe acute respiratory syndrome coronavirus. MERS-CoV: Middle-East respiratory syndrome. SARS-CoV-2: severe acute respiratory syndrome coronavirus 2

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Strikingly, there are no known empirical indicators for predicting the likelihood of spillover events. Nevertheless, spillover transmission events are better characterized for some viruses, such as bat-borne rabies in Latin America, which offers opportunities to better understand spillover transmission and successful onward transmission to secondary susceptible hosts. A series of factors could contribute to the likelihood of spillover transmission and successful virus establishment across scales, from micro to macro. At the fine scale, susceptibility, immune status, genetics, population density, availability of resources (e.g., diet), sex, and age of the host reservoir could be linked to higher levels of viral shedding or higher contact rates to increase spillover transmission and successful virus establishment in a new species (Fig. 2). At an intermediate scale, biodiversity composition, expansion of agriculture, and intensification of livestock production could play a role in the likelihood of spillover transmission by facilitating interactions between species. Finally, at coarse scales, global climate and landscape change or expansion of species ranges could also influence the risk of spillover transmission.

Fig. 2
figure 2

Factors potentially related to spillover transmission across scales. Different biological process act at different spatial scales and may have variables impacts across those scales. Which scale is appropriate to study specific patterns and parameters is still an unresolved question in disease ecology. Studies at fine scale provide high-detail and specificity, but cover small areas while coarse-scale studies cover large geographic areas at the cost of detail

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Furthermore, factors facilitating spillover transmission may act across scales and be interconnected. For example, paleontological evidence suggests that extinctions of large mammals due to climate change increased the endemicity of pathogens in the remaining wildlife community, which may conduce to increased spillover transmissions from wildlife to humans [26]. Furthermore, climate and landscape variation modulate mammal species composition, which shapes virus speciation and endemism altering viral spillover rates between primary hosts and sympatric naïve hosts [27,28,29]. As such, biodiversity losses due to global change could influence the propensity of viral spillover transmission [30], evidenced by previous studies on the influence of potential changes in wildlife species assemblages due to environmental change [31,32,33,34].

Spillover transmission versus disease emergence

Pathogen virulence and pathogen-induced extinction risks are generally considered to be low in reservoir hosts [35]. Nevertheless, in the new host spillover transmission can have two different outcomes: successful and unsuccessful establishment (Fig. 3). In unsuccessful virus establishment, the virus fails to establish in the new host due to factors such as the new host having no cell receptor affinity [36], low intracellular compatibility (e.g., no compatible codon usage) [37], a robust immune response that clears the infection, or having behaviors which reduce exposure to the virus (e.g., solitary vs. social species) [38]. Similarly, the virus could fail to establish due to high virulence in the new host species, which results in the death of the infected host before sustained propagation or onward transmission among conspecifics can occur. New hosts which do not generate secondary infections or onward transmission among conspecifics during spillover transmission are termed “end hosts.” Alternatively, viruses may successfully establish and generate brief or sustained onward transmission, resulting in a “new” reservoir host. For example, new hosts could have an immune response which is insufficient to clear the infection, allowing the virus to multiply and be transmitted onward to new individuals of the same species before the death of the new individual host. Establishment of the virus can be achieved without the need for viral evolution or adaptation—“virulence conservatism”—or reflected as evolutionary change in the virus—“host shift”. Secondary onward transmission resulting from successful viral establishment, either with or without viral evolution, is the prelude to disease emergence [10, 39,40,41,42,43,44,45,46]. An important knowledge gap that has not yet been fully explored with regard to disease emergence includes the role of habitat conditions or biodiversity gradients that may limit or facilitate secondary onward transmission (Box 1).

Fig. 3
figure 3

Diagram of spillover transmission events with successful and unsuccessful virus establishment in the new host. A geographical range shift of a host species may cause contact with a novel host species. This disturbance in host species assemblages may cause transmission of viruses from the primary host to a new, naïve host, resulting in the expression of disease or death of the new host. Alternatively, the new host infected with the virus could show complete innocuity due to the incompetence of the host to interact with the novel virus. a Pathogens generally fail to successfully establish in a naïve host (orange) due to the virus removal (e.g., the immune system clears the infection or there is no cell tropism compatibility to lack of affinity with cell receptors). b Pathogens could also fail to establish in a new host due to the host’s death (e.g., pathogen kills the naïve host). Failure of the pathogen to establish in a new host, also known as ‘end hosts’ (orange), will not generate secondary transmission. c In rare spillover transmission events, pathogens successfully establish in a naïve host in the absence of pathogen’s adaptation (Pathogen does not change; i.e., pathogen’s complete genome highly conserved, without adaptative mutations. Under this scenario pathogens mainly present neutral evolution). e Alternatively, the pathogen could develop adaptation (i.e., mutations) to modulate its virulence and escape or overcome the host’s immunity or increase cell receptor affinity (Pathogen change, i.e., host-shift). Successful pathogen establishment in a naïve host, also known as ‘new host’ is the prelude for disease emergence

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Spatial scale

Different biological process act at different spatial scales [47]. For example, while behavior may be relevant to explain transmission patterns at the local level, climate could be more important to explain transmission at the continental level [48]. The appropriate scale to study specific patterns and parameters is still an unresolved question in disease ecology [49, 50]. Studies at fine scale provide high-detail and specificity but cover small areas, while coarse-scale studies cover large geographic areas at the cost of detail (Fig. 4). Spillover and onward transmission from an original host to a naïve host has been studied at the molecular, individual, and population level. Nevertheless, there is a need for spillover-transmission research at coarser scales to untangle the biogeographic elements of cross-species transmission [51]. Different spatial scales allow for the use of data with different information and at different levels of detail (i.e., grain; Fig. 4). At fine spatial scales, spillover studies can analyze host-level data (e.g., sex, age, genetic variation, body size, etc.) to assess the role of reservoir features on spillover risk. At medium spatial scales, researchers should assess landscape-level data (e.g., land cover change, intensity of urbanization, livestock density) to understand these features’ impact on spillover propensity. At coarse spatial scales, future investigations should explore how biogeographic factors (e.g., temperature, precipitation, evapotranspiration) explain why virus spillover transmission occurs in some areas but not others and when onward transmission is more likely.

Fig. 4
figure 4

Multiscale framework of spillover research. a Pathogen spillover studies across fine, medium, and coarse scales allow bottom-up and top-down assessments. b Different scales allow to cover different study area extents, from individuals, to ecosystems. Modified from [74]

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Bats and spillover

Bats are known to be major reservoirs hosts for many viruses, and consequently the primary source (donor or source host) of microorganisms that can successfully establish in naïve species (recipient host) [52, 53]. The high number of bat species (~ 1200) inherently generates a proportionally high amount and diversity of viruses (virosphere) with the potential to infect humans and other mammals [54]. That is, more bat-borne viruses are expected to be discovered as research effort increases [55]. As such, global hotspots of bat diversity are expected to harbor a larger and more diverse plethora of microorganisms with pandemic potential.

Viral establishment in the new host is dependent upon the frequency of spillover transmission events and demography of the new host [35]. Intermediate levels of virulence are also highly suitable for successful establishment in a naïve host species [35]. Pathogen virulence generally dependents upon the host affected [36] (Fig. 3). That is, a virus could be highly virulent for some host species or individuals, but not virulent for others. Molecular-level mechanisms of infection are well understood for many emerging diseases originated from spillover [3]; thus, one next frontier on spillover transmission research is a focus on the drivers of the spillover events themselves to understand why spillover occurs, which is neglected in many spillover transmission studies.

Rabies as a model of spillover transmission

Rabies is caused by all members of the Lyssavirus genus, and ranks among the best-understood and best-surveyed disease systems [56, 57]. RABV is the most widespread agent within the genus and its detection and identification are achieved with high certainty by continent-wide comprehensive surveillance systems [58]. RABV is distributed across the globe, with hotspots of viral diversity along the Neotropics [59, 60]. Rabies virus transmission requires direct contact, through bites and scratches [61], and distinct viral lineages have become established in different species and populations within the Carnivora and Chiroptera orders [55]. Furthermore, the study of rabies was foundational to the development of the idea of vaccination (i.e., by Louis Pasteur); modern molecular epidemiology; disease eradication under One Health approaches; development of oral vaccination strategies; and for understanding disease persistence, natural immunity, abortive infections, spillover transmission, disease ecology, and evolution [57, 61]. Rabies is also almost 100% fatal for infected individuals, killing ~ 59,000 people annually, and causes at least USD 8.6 billion in economic losses annually [62]. In summary, rabies is a well understood, data-rich disease with a high degree of host plasticity and a demonstrated history of viral conservatism across host lineages, resulting in disease persistence. These elements make the rabies system a unique opportunity for advancing the global understanding of spillover transmission across regions, host taxa, and periods.

Spillover transmission of rabies virus

While canine-rabies has been almost eradicated in the Americas, bat-borne rabies is now an emerging public health and agricultural problem [56, 63]. In Latin America, most rabies cases in humans and domestic animals originate from bites inflicted by the common vampire bat (Desmodus rotundus) (Fig. 5), one of the only three mammal species 100% dependent on blood to survive [56, 63]. The species has a broad geographic range, and feeds on the blood of a variety of prey species, including wildlife, livestock, pets, and humans [64]. Some of the southernmost D. rotundus populations in South America even feed on marine mammals (e.g., sea lions) and birds (e.g., penguins). During feeding, D. rotundus can transmit rabies virus to their prey (Fig. 5), which may result in primary spillover transmission or even secondary spillover to other species (e.g., rabies from D. rotundus to cats and then from cats to humans). Vampire bat-borne rabies virus (VB-RABV) outbreaks in humans suggest that mortality mainly occurs in tropical and subtropical regions. For example, Brazil reports about two cases of human rabies annually caused by bat-borne rabies viruses that have been laboratory-confirmed as antigenic variant 3, a RABV variant associated with D. rodundus. However, underreported cases that are not laboratory confirmed are probably much more common. Documenting how VB-RABV can spill from D. rotundus over to other species can inform and guide strategies to prevent VB-RABV spillover transmission to humans and domestic animals, and help prevent the potential spread of D. rotundus rabies from Latin America into the United States.

Fig. 5
figure 5

Desmodus rotundus rabies virus spillover and onward transmission. Rabies virus is transmitted accidentally from one infected vampire to its prey Rabies virus is transmitted from an infected vampire bat (i.e., reservoir host) to other species, which may or may not maintain transmission (i.e., end host vs. new host; Fig. 3). Primary spillover transmission events are common in Latin America. Secondary spillover transmission also occurs and result in zoonotic spillover (i.e., human infections)

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In summary, VB-RABV has been documented for over a century [65], and as a system displays many interesting elements of spillover transmission. VB-RABV from wildlife species is regularly transmitted to domestic animals and humans [64, 66], has a conservative virus for which dramatic viral genomic change has not been observed during some spillover events [61], and possesses an original reservoir host species (bats from the New World) which is often times evolutionary distant from its receptor hosts (e.g., herbivores from the Old World) [60]. Furthermore, D. rotundus is one of the most well studied mammals in the Americas [57, 58, 64, 67] (Fig. 6; considerable availability of specimens of the species), and is distributed across tropical regions where well-studied species are scarce. Comprehensive documentation and available data on rabies virus and the vampire bat geographic distribution across the Neotropics is reasonably well collected in a continuous and standardized form. That is, bat hosts and virus detection and identification are attained with high certainty by a continent-wide comprehensive surveillance system. In Latin America alone, at least 23,536 outbreaks of VB-RABV spillover to cattle were reported between 1970 and 2021 [68]. For example, VB-RABV lineage antigenic variant 3, specific to D. rotundus, shows failure to establish onward transmission after spillover transmission to livestock. These elements make vampire bat borne rabies an extraordinarily unique wildlife-disease system for advancing the understanding of spillover transmission across large study areas.

Fig. 6
figure 6

Large vampire bat records. Unpublished records of Desmodus rotundus and specimens are available across Latin America. For example, specimens are stored in biological collections in Latin America and available for future research to study spillover transmission and disease emergence

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Conclusions

Virus spillover transmission, as the prelude for disease emergence, is a poorly understood highly complex phenomenon [10]. Although spillover transmission is expected to increase in incidence and geographic range in the future years as a result of global change [6], the role of environmental factors at different scales of complexity has been rarely studied quantitatively [69]. As a result of these uncertainties, there is a poor mechanistic understanding of spillover transmission inherent processes (subtle stages) that limits humanity’s ability to predict virus spillover transmission across different regions. A persistently unsolved question in disease ecology, therefore, is the extent to which spillover transmission can be quantified and predicted at the local, regional, and continental levels (i.e., across spatial scales). Research is still needed on the ecological and biogeographic drivers leading to cross-species viral transmission to determine the mechanisms that facilitate host-virus dynamics across regions and environmental gradients [70,71,72]. Understanding where spillover transmission events are more likely to occur is the crucial first step where focused surveillance should take place, to anticipate effective early prevention and control programs before virus spillover transmission ends in disease emergence. The status quo in spillover transmission research reveals predictive limitations that fail to determine when a spillover transmission event could result in outbreaks, epidemics, and pandemics such as the COVID-19 pandemic caused by SARS-CoV-2.

Vampire-bat-borne rabies (VB-RABV) is an ideal biological system to study spillover transmission. For instance, RABV is well understood and there is an effective vaccine to reduce biosecurity risks for researchers. Additionally, VB-RABV spillover from D. rotundus to livestock is frequent and widespread in Latin America. Finally, VB-RABV primary spillover transmission to cattle results in end hosts, so that there are immense opportunities to better understand actual spillover transmission events that do not necessarily result in the establishment of new transmission cycles that may end up in long-lasting epidemics.

Future research in this field should focus on five key questions. (1) What landscape conditions are needed for a spillover transmission event to occur in the first place? (2) How can biodiversity composition modulate the likelihood of spillover transmission? and (3) What type of mutations in viral genomes facilitate spillover transmission and subsequent disease spread across different species? (4) Are there any climatic drivers favoring or limiting spillover transmission? (5) How do landscape changes, such as changes due to emergent commodity or natural resources exploitation (e.g., lithium) or massive destruction after armed conflicts impact spillover transmission of wildlife viruses? These research lines are of critical public interest considering that the circulation of zoonotic viruses in wildlife is, in general, a threat to human health and social/economic development [73]. By understanding the specific drivers of zoonotic virus spillover transmission from wildlife, and by forecasting areas suitable for successful spillover transmission, health professionals could implement early detection, control, and elimination strategies for effective outbreak containment that will reduce economic impacts.

Availability of data and materials

Not applicable.

Abbreviations

RABV:

Rabies virus

VB-RABV:

Vampire Bat Rabies or Vampire Bat-borne Rabies

US:

United States

References

  1. Molina-Cruz A, Zilversmit MM, Neafsey DE, Hartl DL, Barillas-Mury C. Mosquito vectors and the globalization of Plasmodium falciparum malaria. Annu Rev Genet. 2016;50:447–65.

    Article  CAS  PubMed  Google Scholar 

  2. Lucius R, Loos-Frank B, Lane RP, Poulin R, Roberts CW, Grencis RK. The biology of parasites. Weinheim: John Wiley & Sons; 2017.

    Google Scholar 

  3. Morand S, Krasnov BR, Littlewood DTJ. Parasite diversity and diversification. Cambridge: Cambridge University Press; 2015.

    Book  Google Scholar 

  4. Molina-Cruz A, Canepa GE, Barillas-Mury C. Plasmodium P47: a key gene for malaria transmission by mosquito vectors. Curr Opin Microbiol. 2017;40:168–74.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Taylor LH, Latham SM, Woolhouse ME. Risk factors for human disease emergence. Philos Trans R Soc B. 2001;356:983–9.

    Article  CAS  Google Scholar 

  6. Brooks DR, Boeger WA. Climate change and emerging infectious diseases: evolutionary complexity in action. Curr Opin Syst Biol. 2019;13:75–81.

    Article  Google Scholar 

  7. Allen T, Murray KA, Zambrana-Torrelio C, Morse SS, Rondinini C, Di Marco M, et al. Global hotspots and correlates of emerging zoonotic diseases. Nat Commun. 2017;8:1124.

    Article  PubMed Central  PubMed  Google Scholar 

  8. Olival KJ, Hosseini PR, Zambrana-Torrelio C, Ross N, Bogich TL, Daszak P. Host and viral traits predict zoonotic spillover from mammals. Nature. 2017;546:646–50.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Plowright RK, Foley P, Field HE, Dobson AP, Foley JE, Eby P, et al. Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proc Biol Sci. 2011;278:3703–12.

    PubMed Central  PubMed  Google Scholar 

  10. Plowright RK, Parrish CR, McCallum H, Hudson PJ, Ko AI, Graham AL, et al. Pathways to zoonotic spillover. Nat Rev Microbiol. 2017;15:502–10.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Wells K, Clark NJ. Host specificity in variable environments. Trends Parasitol. 2019;35:452–65.

    Article  PubMed  Google Scholar 

  12. Schneider MC, Romijn P, Uieda W, Tamayo H, Silva D, Belotto A, et al. Rabies transmitted by vampire bats to humans: an emerging zoonotic disease in Latin America? Am J Public Heal. 2009;25:260–9.

    Google Scholar 

  13. Meske M, Fanelli A, Rocha F, Awada L, Soto PC, Mapitse N, et al. Evolution of rabies in south America and inter-species dynamics (2009–2018). Trop Med Infect Dis. 2021;6:2–18.

    Google Scholar 

  14. Zhou P, Fan H, Lan T, Yang X Lou, Shi WF, Zhang W, et al. Fatal swine acute diarrhoea syndrome caused by an HKU2-related coronavirus of bat origin. Nature. 2018;556:255–9.

  15. Hsu VP, Hossain MJ, Parashar UD, Ali MM, Ksiazek TG, Kuzmin I, et al. Nipah virus encephalitis reemergence, Bangladesh. Emerg Infect Dis. 2004;10:2082–7.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Epstein JH, Anthony SJ, Islam A, Marm Kilpatrick A, Khan SA, Balkey MD, et al. Nipah virus dynamics in bats and implications for spillover to humans. Proc Natl Acad Sci USA. 2020;117:29190–201.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Wang LF, Eaton BT. Bats, civets and the emergence of SARS. Curr Top Microbiol Immunol. 2007;315:325–44.

    CAS  PubMed Central  PubMed  Google Scholar 

  18. Han HJ, Yu H, Yu XJ. Evidence for zoonotic origins of Middle East respiratory syndrome coronavirus. J Gen Virol. 2016;97:274–80.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Memish ZA, Mishra N, Olival KJ, Fagbo SF, Kapoor V, Epstein JH, et al. Middle east respiratory syndrome coronavirus in bats, Saudi Arabia. Emerg Infect Dis. 2013;19:1819–23.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Meyer B, Müller MA, Corman VM, Reusken CBEM, Ritz D, Godeke GJ, et al. Antibodies against MERS coronavirus in dromedaries, United Arab Emirates, 2003 and 2013. Emerg Infect Dis. 2014;20:552–9.

    Article  PubMed Central  PubMed  Google Scholar 

  21. Mahalingam S, Herrero LJ, Playford EG, Spann K, Herring B, Rolph MS, et al. Hendra virus: an emerging paramyxovirus in Australia. Lancet Infect Dis. 2012;12:799–807.

    Article  PubMed  Google Scholar 

  22. Latinne A, Hu B, Olival KJ, Zhu G, Zhang L, Li H, et al. Origin and cross-species transmission of bat coronaviruses in China. Nat Commun. 2020;11: e4235.

    Article  Google Scholar 

  23. Xiao K, Zhai J, Feng Y, Zhou N, Zhang X, Zou JJ, et al. Isolation of SARS-CoV-2-related coronavirus from Malayan pangolins. Nature. 2020;583:286–9.

    Article  CAS  PubMed  Google Scholar 

  24. Lau SKP, Luk HKH, Wong ACP, Li KSM, Zhu L, He Z, et al. Possible bat origin of severe acute respiratory syndrome coronavirus 2. Emerg Infect Dis. 2020;26:1542–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  25. Holmes EC, Goldstein SA, Rasmussen AL, Robertson DL, Crits-Christoph A, Wertheim JO, et al. The origins of SARS-CoV-2: a critical review. Cell. 2021;184:4848–56.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Doughty CE, Prys-Jones TO, Faurby S, Abraham AJ, Hepp C, Leshyk V, et al. Megafauna decline have reduced pathogen dispersal which may have increased emergent infectious diseases. Ecography. 2020;43:1107–17.

    Article  Google Scholar 

  27. de Oliveira SV, Escobar LE, Peterson AT, Gurgel-Gonçalves R. Potential geographic distribution of hantavirus reservoirs in Brazil. PLoS ONE. 2013;8: e85137.

    Article  PubMed Central  PubMed  Google Scholar 

  28. Astorga F, Escobar LE, Poo-Muñoz D, Escobar-Dodero J, Rojas-Hucks S, Alvarado-Rybak M, et al. Distributional ecology of Andes hantavirus: a macroecological approach. Int J Health Geogr. 2018;17:22.

    Article  PubMed Central  PubMed  Google Scholar 

  29. Peterson AT. Mapping disease transmission risk. Baltimore: Johns Hopkins University Press; 2014.

    Book  Google Scholar 

  30. Civitello DJ, Cohen J, Fatima H, Halstead NT, Liriano J, McMahon TA, et al. Biodiversity inhibits parasites: broad evidence for the dilution effect. Proc Natl Acad Sci USA. 2015;112:8667–71.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Williams JE, Blois JL. Range shifts in response to past and future climate change: can climate velocities and species’ dispersal capabilities explain variation in mammalian range shifts? J Biogeogr. 2018;45:2175–89.

    Article  Google Scholar 

  32. Sunday JM, Bates AE, Dulvy NK. Thermal tolerance and the global redistribution of animals. Nat Clim Chang. 2012;2:686–90.

    Article  Google Scholar 

  33. Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, et al. Extinction risk from climate change. Nature. 2004;427:145–8.

    Article  CAS  PubMed  Google Scholar 

  34. Peterson AT, Soberón J, Sánchez-Cordero V. Conservatism of ecological niches in evolutionary time. Science. 1999;285:1265–7.

    Article  CAS  PubMed  Google Scholar 

  35. de Castro F, Bolker BM, et al. Parasite establishment and host extinction in model communities. Oikos. 2005;111:501–13.

    Article  Google Scholar 

  36. Damas J, Hughes GM, Keough KC, Painter CA, Persky NS, Corbo M, et al. Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates. Proc Natl Acad Sci USA. 2020;117:22311–22.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  37. Escobar LE, Pritzkow S, Winter SN, Grear DA, Kirchgessner MS, Dominguez-Villegas E, et al. The ecology of chronic wasting disease in wildlife. Biol Rev. 2020;95:393–408.

    Article  PubMed  Google Scholar 

  38. Robles-Fernández ÁL, Santiago-Alarcon D, Lira-Noriega A. Wildlife susceptibility to infectious diseases at global scales. Proc Natl Acad Sci USA. 2022;119:1–12.

    Article  Google Scholar 

  39. Streicker DG, Turmelle AS, Vonhof MJ, Kuzmin IV, McCracken GF, Rupprecht CE. Host phylogeny constrains cross-species emergence and establishment of rabies virus in bats. Science. 2010;329:676–9.

    Article  CAS  PubMed  Google Scholar 

  40. Lloyd-Smith JO, George D, Pepin KM, Pitzer VE, Pulliam JRC, Dobson AP, et al. Epidemic dynamics at the human-animal interface. Science. 2009;326:1362–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  41. Plowright RK, Eby P, Hudson PJ, Smith IL, Westcott D, Bryden WL, et al. Ecological dynamics of emerging bat virus spillover. Proc R Soc B. 2014;282:1798.

    Google Scholar 

  42. Mollentze N, Biek R, Streicker DG. The role of viral evolution in rabies host shifts and emergence. Curr Opin Virol. 2014;8:68–72.

    Article  PubMed Central  PubMed  Google Scholar 

  43. De Roode JC, Yates AJ, Altizer S. Virulence-transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc Natl Acad Sci USA. 2008;105:7489–94.

    Article  PubMed Central  PubMed  Google Scholar 

  44. Longdon B, Brockhurst MA, Russell CA, Welch JJ, Jiggins FM. The evolution and genetics of virus host shifts. PLoS Pathog. 2014;10: e1004395.

    Article  PubMed Central  PubMed  Google Scholar 

  45. Wolfe ND, Dunavan CP, Diamond J. Origins of major human infectious diseases. Nature. 2007;447:279–83.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  46. Mollentze N, Streicker DG, Murcia PR, Hampson K, Biek R. Virulence mismatches in index hosts shape the outcomes of cross-species transmission. Proc Natl Acad Sci USA. 2020;117:28859–66.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Soberón J. Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett. 2007;10:1115–23.

    Article  PubMed  Google Scholar 

  48. Soberón J, Peterson AT. Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodivers Informatics. 2005;2:1–10.

    Article  Google Scholar 

  49. Chave J. The problem of pattern and scale in ecology: what have we learned in 20 years? Ecol Lett. 2013;16:4.

    Article  PubMed  Google Scholar 

  50. Levin SA. The problem of pattern and scale in ecology: The Robert H. MacArthur Award Lecture. Ecology. 1992;73:1943–67.

    Article  Google Scholar 

  51. Winter SN, Escobar LE. Chronic wasting disease modeling: An overview. J Wildl Dis. 2020;56:741–58.

    Article  PubMed  Google Scholar 

  52. Calisher C, Holmes K. Bats prove to be rich reservoirs for emerging viruses. Microbe. 2008;3:521–8.

    Google Scholar 

  53. Calisher CH, Holmes KKV, Dominguez SR, Schountz T, Cryan P, Childs JE, et al. Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev. 2006;19:531–45.

    Article  PubMed Central  PubMed  Google Scholar 

  54. Mollentze N, Streicker DG. Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proc Natl Acad Sci USA. 2020;117:9423–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Escobar LE, Peterson AT, Favi M, Yung V, Medina-Vogel G. Bat-borne rabies in Latin America. Rev Inst Med Trop Sao Paulo. 2015;57:63–72.

    Article  PubMed Central  PubMed  Google Scholar 

  56. Velasco-Villa A, Escobar LE, Sanchez A, Shi M, Streicker DG, Gallardo-Romero NF, et al. Successful strategies implemented towards the elimination of canine rabies in the Western Hemisphere. Antiviral Res. 2017;143:1–12.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  57. Rupprecht CE, Hanlon CA, Hemachudha T. Rabies re-examined. Lancet Infect Dis. 2002;2:327–43.

    Article  PubMed  Google Scholar 

  58. Streicker DG, Winternitzc JC, Satterfield DA, Condori-Condori RE, Broos A, Tello C, et al. Host-pathogen evolutionary signatures reveal dynamics and future invasions of vampire bat rabies. Proc Natl Acad Sci USA. 2016;113:10926–31.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  59. Streicker DG, Lemey P, Velasco-Villa AA, Rupprecht CE. Rates of viral evolution are linked to host geography in bat rabies. PLoS Pathog. 2012;8: e1002720.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  60. Stoner-Duncan B, Streicker DG, Tedeschi CM. Vampire bats and rabies: toward an ecological solution to a public health problem. PLoS Negl Trop Dis. 2014;8: e2867.

    Article  PubMed Central  PubMed  Google Scholar 

  61. Fisher CR, Streicker DG, Schnell MJ. The spread and evolution of rabies virus: conquering new frontiers. Nat Rev Microbiol. 2018;16:241–55.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  62. Brunker K, Mollentze N. Rabies virus. Trends Microbiol. 2018;26:886–7.

    Article  CAS  PubMed  Google Scholar 

  63. Velasco-Villa A, Mauldin MR, Shi M, Escobar LE, Gallardo-Romero NF, Damon I, et al. The history of rabies in the Western Hemisphere. Antiviral Res. 2017;146:221–32.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Benavides JA, Valderrama W, Recuenco S, Uieda W, Suzán G, Avila-Flores R, et al. Defining new pathways to manage the ongoing emergence of bat rabies in Latin America. Viruses. 2020;12:1–13.

    Article  Google Scholar 

  65. Pawan JL. The transmission of paralytic rabies in Trinidad by the vampire bat (Desmodus rotundus murinus Wagner, 1840). Ann Trop Med Parasitol. 1936;30:101–30.

    Article  Google Scholar 

  66. Anderson A, Shwiff S, Gebhardt K, Ramírez AJ, Shwiff S, Kohler D, et al. Economic evaluation of vampire bat (Desmodus rotundus) rabies prevention in Mexico. Transbound Emerg Dis. 2014;61:140–6.

    Article  CAS  PubMed  Google Scholar 

  67. Blackwood JC, Streicker DG, Altizer S, Rohani P. Resolving the roles of immunity, pathogenesis, and immigration for rabies persistence in vampire bats. Proc Natl Acad Sci USA. 2013;110:20837–42.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. PAHO/PANAFTOSA. SIRVERA [Internet]. Sist. Inf. Reg. para la Vigil. Epidemiológica la Rabia. 2022 [cited 2022 Oct 21]. Available from: http://sirvera.panaftosa.org.br/search/public (Spanish).

  69. Dillon WW, Meentemeyer RK. Direct and indirect effects of forest microclimate on pathogen spillover. Ecology. 2019;100:1–12.

    Article  Google Scholar 

  70. Krebs CJ. Ecology: the experimental analysis of distribution and abundance. New York: Longman Higer Education; 1972.

    Google Scholar 

  71. Keeling MJ, Rohani P. Modeling infectious diseases in humans and animals. Public health. New Jersey: Princetone University Press; 2007.

    Google Scholar 

  72. Peterson AT. Mapping disease transmission risk: enriching models using biology and ecology. Baltimore: Johns Hopkins University Press; 2014.

    Book  Google Scholar 

  73. Brandão PE, Scheffer K, Villarreal LY, Achkar S, Oliveira RN, Fahl WO, et al. A coronavirus detected in the vampire bat Desmodus rotundus. Braz J Infect Dis. 2008;12:466–8.

    Article  PubMed  Google Scholar 

  74. Escobar LE. Ecological niche modeling: an introduction for veterinarians and epidemiologists. Front Vet Sci. 2020;7:1–15.

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank Diego Soler-Tovar, Shariful Islam, and Mariana Castaneda Guzman for their support on the development and review of this manuscript. The opinions and conclusions expressed in this commentary article are those of the authors and do not necessarily represent the official position of the CDC or the US Department of Health and Human Services.

Funding

This study was supported by the National Science Foundation award: Human–Environment and Geographical Sciences Program 2116748 and Institute for Critical Technology and Applied Science, Virginia Tech: ICTAS-JFP-2022-2023. The publication was supported by the VT Open Access Subvention Fund.

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Authors and Affiliations

  1. Department of Fish and Wildlife Conservation, Virginia Tech, Blacksburg, VA, USA

    Luis E. Escobar & Paige Van de Vuurst

  2. Virginia Tech Graduate School, Translational Biology, Medicine, and Health Program, Blacksburg, VA, USA

    Luis E. Escobar & Paige Van de Vuurst

  3. Global Change Center, Virginia Tech, Blacksburg, VA, USA

    Luis E. Escobar

  4. Center for Emerging Zoonotic and Arthropod-Borne Pathogens, Virginia Tech, Blacksburg, VA, USA

    Luis E. Escobar & Paige Van de Vuurst

  5. Facultad de Ciencias Agropecuarias, Universidad de La Salle, Bogotá, Colombia

    Luis E. Escobar

  6. Poxvirus and Rabies Branch, Centers for Disease Control and Prevention, 1600 Clifton Rd. NE, Atlanta, GA, 30333, USA

    Andres Velasco-Villa, Panayampalli S. Satheshkumar & Yoshinori Nakazawa

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  1. Luis E. Escobar
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  4. Yoshinori Nakazawa
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  5. Paige Van de Vuurst
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Contributions

LEE designed and wrote the first draft of this commentary. All authors contributed to the development, review, and approval of the last version of this article. All authors read and approved the final manuscript.

Authors’ information

Dr. Luis Escobar is faculty and principal investigator at the Department of Fish and Wildlife Conservation in Virginia Tech, Blacksburg, Virginia, US. His research interests are global change and zoonotic diseases of fish and wildlife origin.

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Correspondence to Luis E. Escobar.

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Escobar, L.E., Velasco-Villa, A., Satheshkumar, P.S. et al. Revealing the complexity of vampire bat rabies “spillover transmission”. Infect Dis Poverty 12, 10 (2023). https://doi.org/10.1186/s40249-023-01062-7

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Keywords

Infectious Diseases of Poverty

ISSN: 2049-9957

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