- Commentary
- Open access
- Published:
Revealing the complexity of vampire bat rabies “spillover transmission”
Infectious Diseases of Poverty volume 12, Article number: 10 (2023)
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).
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.
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).
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.
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.
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.
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
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.
Lucius R, Loos-Frank B, Lane RP, Poulin R, Roberts CW, Grencis RK. The biology of parasites. Weinheim: John Wiley & Sons; 2017.
Morand S, Krasnov BR, Littlewood DTJ. Parasite diversity and diversification. Cambridge: Cambridge University Press; 2015.
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.
Taylor LH, Latham SM, Woolhouse ME. Risk factors for human disease emergence. Philos Trans R Soc B. 2001;356:983–9.
Brooks DR, Boeger WA. Climate change and emerging infectious diseases: evolutionary complexity in action. Curr Opin Syst Biol. 2019;13:75–81.
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.
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.
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.
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.
Wells K, Clark NJ. Host specificity in variable environments. Trends Parasitol. 2019;35:452–65.
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.
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.
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.
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.
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.
Wang LF, Eaton BT. Bats, civets and the emergence of SARS. Curr Top Microbiol Immunol. 2007;315:325–44.
Han HJ, Yu H, Yu XJ. Evidence for zoonotic origins of Middle East respiratory syndrome coronavirus. J Gen Virol. 2016;97:274–80.
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.
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.
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.
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.
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.
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.
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.
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.
de Oliveira SV, Escobar LE, Peterson AT, Gurgel-Gonçalves R. Potential geographic distribution of hantavirus reservoirs in Brazil. PLoS ONE. 2013;8: e85137.
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.
Peterson AT. Mapping disease transmission risk. Baltimore: Johns Hopkins University Press; 2014.
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.
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.
Sunday JM, Bates AE, Dulvy NK. Thermal tolerance and the global redistribution of animals. Nat Clim Chang. 2012;2:686–90.
Thomas CD, Cameron A, Green RE, Bakkenes M, Beaumont LJ, Collingham YC, et al. Extinction risk from climate change. Nature. 2004;427:145–8.
Peterson AT, Soberón J, Sánchez-Cordero V. Conservatism of ecological niches in evolutionary time. Science. 1999;285:1265–7.
de Castro F, Bolker BM, et al. Parasite establishment and host extinction in model communities. Oikos. 2005;111:501–13.
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.
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.
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.
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.
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.
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.
Mollentze N, Biek R, Streicker DG. The role of viral evolution in rabies host shifts and emergence. Curr Opin Virol. 2014;8:68–72.
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.
Longdon B, Brockhurst MA, Russell CA, Welch JJ, Jiggins FM. The evolution and genetics of virus host shifts. PLoS Pathog. 2014;10: e1004395.
Wolfe ND, Dunavan CP, Diamond J. Origins of major human infectious diseases. Nature. 2007;447:279–83.
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.
Soberón J. Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett. 2007;10:1115–23.
Soberón J, Peterson AT. Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodivers Informatics. 2005;2:1–10.
Chave J. The problem of pattern and scale in ecology: what have we learned in 20 years? Ecol Lett. 2013;16:4.
Levin SA. The problem of pattern and scale in ecology: The Robert H. MacArthur Award Lecture. Ecology. 1992;73:1943–67.
Winter SN, Escobar LE. Chronic wasting disease modeling: An overview. J Wildl Dis. 2020;56:741–58.
Calisher C, Holmes K. Bats prove to be rich reservoirs for emerging viruses. Microbe. 2008;3:521–8.
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.
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.
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.
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.
Rupprecht CE, Hanlon CA, Hemachudha T. Rabies re-examined. Lancet Infect Dis. 2002;2:327–43.
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.
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.
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.
Fisher CR, Streicker DG, Schnell MJ. The spread and evolution of rabies virus: conquering new frontiers. Nat Rev Microbiol. 2018;16:241–55.
Brunker K, Mollentze N. Rabies virus. Trends Microbiol. 2018;26:886–7.
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.
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.
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.
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.
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.
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).
Dillon WW, Meentemeyer RK. Direct and indirect effects of forest microclimate on pathogen spillover. Ecology. 2019;100:1–12.
Krebs CJ. Ecology: the experimental analysis of distribution and abundance. New York: Longman Higer Education; 1972.
Keeling MJ, Rohani P. Modeling infectious diseases in humans and animals. Public health. New Jersey: Princetone University Press; 2007.
Peterson AT. Mapping disease transmission risk: enriching models using biology and ecology. Baltimore: Johns Hopkins University Press; 2014.
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.
Escobar LE. Ecological niche modeling: an introduction for veterinarians and epidemiologists. Front Vet Sci. 2020;7:1–15.
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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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.
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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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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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DOI: https://doi.org/10.1186/s40249-023-01062-7