The notion that certain animal groups disproportionately maintain and transmit viruses to humans due to broad-scale differences in ecology, life history, and physiology currently influences global ...health surveillance and research in disease ecology, virology, and immunology. To directly test whether such “special reservoirs” of zoonoses exist, we used literature searches to construct the largest existing dataset of virus–reservoir relationships, consisting of the avian and mammalian reservoir hosts of 415 RNA and DNA viruses along with their histories of human infection. Reservoir host effects on the propensity of viruses to have been reported as infecting humans were rare and when present were restricted to one or two viral families. The data instead support a largely host-neutral explanation for the distribution of human-infecting viruses across the animal orders studied. After controlling for higher baseline viral richness in mammals versus birds, the observed number of zoonoses per animal order increased as a function of their species richness. Animal orders of established importance as zoonotic reservoirs including bats and rodents were unexceptional, maintaining numbers of zoonoses that closely matched expectations for mammalian groups of their size. Our findings show that variation in the frequency of zoonoses among animal orders can be explained without invoking special ecological or immunological relationships between hosts and viruses, pointing to a need to reconsider current approaches aimed at finding and predicting novel zoonoses.
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BFBNIB, NMLJ, NUK, PNG, SAZU, UL, UM, UPUK
Determining which animal viruses may be capable of infecting humans is currently intractable at the time of their discovery, precluding prioritization of high-risk viruses for early investigation and ...outbreak preparedness. Given the increasing use of genomics in virus discovery and the otherwise sparse knowledge of the biology of newly discovered viruses, we developed machine learning models that identify candidate zoonoses solely using signatures of host range encoded in viral genomes. Within a dataset of 861 viral species with known zoonotic status, our approach outperformed models based on the phylogenetic relatedness of viruses to known human-infecting viruses (area under the receiver operating characteristic curve AUC = 0.773), distinguishing high-risk viruses within families that contain a minority of human-infecting species and identifying putatively undetected or so far unrealized zoonoses. Analyses of the underpinnings of model predictions suggested the existence of generalizable features of viral genomes that are independent of virus taxonomic relationships and that may preadapt viruses to infect humans. Our model reduced a second set of 645 animal-associated viruses that were excluded from training to 272 high and 41 very high-risk candidate zoonoses and showed significantly elevated predicted zoonotic risk in viruses from nonhuman primates, but not other mammalian or avian host groups. A second application showed that our models could have identified Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) as a relatively high-risk coronavirus strain and that this prediction required no prior knowledge of zoonotic Severe Acute Respiratory Syndrome (SARS)-related coronaviruses. Genome-based zoonotic risk assessment provides a rapid, low-cost approach to enable evidence-driven virus surveillance and increases the feasibility of downstream biological and ecological characterization of viruses.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Rabies is a lethal zoonotic disease that is caused by lyssaviruses, most often rabies virus. Despite control efforts, sporadic outbreaks in wildlife populations are largely unpredictable, ...underscoring our incomplete knowledge of what governs viral transmission and spread in reservoir hosts. Furthermore, the evolutionary history of rabies virus and related lyssaviruses remains largely unclear. Robust surveillance efforts combined with diagnostics and disease modelling are now providing insights into the epidemiology and evolution of rabies virus. The immune status of the host, the nature of exposure and strain differences all clearly influence infection and transmission dynamics. In this Review, we focus on rabies virus infections in the wildlife and synthesize current knowledge in the rapidly advancing fields of rabies virus epidemiology and evolution, and advocate for multidisciplinary approaches to advance our understanding of this disease.
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IZUM, KILJ, NUK, PILJ, PNG, SAZU, SBMB, UL, UM, UPUK
Urbanisation and agriculture cause declines for many wildlife, but some species benefit from novel resources, especially food, provided in human‐dominated habitats. Resulting shifts in wildlife ...ecology can alter infectious disease dynamics and create opportunities for cross‐species transmission, yet predicting host–pathogen responses to resource provisioning is challenging. Factors enhancing transmission, such as increased aggregation, could be offset by better host immunity due to improved nutrition. Here, we conduct a review and meta‐analysis to show that food provisioning results in highly heterogeneous infection outcomes that depend on pathogen type and anthropogenic food source. We also find empirical support for behavioural and immune mechanisms through which human‐provided resources alter host exposure and tolerance to pathogens. A review of recent theoretical models of resource provisioning and infection dynamics shows that changes in host contact rates and immunity produce strong non‐linear responses in pathogen invasion and prevalence. By integrating results of our meta‐analysis back into a theoretical framework, we find provisioning amplifies pathogen invasion under increased host aggregation and tolerance, but reduces transmission if provisioned food decreases dietary exposure to parasites. These results carry implications for wildlife disease management and highlight areas for future work, such as how resource shifts might affect virulence evolution.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SAZU, SBCE, SBMB, UL, UM, UPUK
Identifying the animal origins of RNA viruses requires years of field and laboratory studies that stall responses to emerging infectious diseases. Using large genomic and ecological datasets, we ...demonstrate that animal reservoirs and the existence and identity of arthropod vectors can be predicted directly from viral genome sequences via machine learning. We illustrate the ability of these models to predict the epidemiology of diverse viruses across most human-infective families of single-stranded RNA viruses, including 69 viruses with previously elusive or never-investigated reservoirs or vectors. Models such as these, which capitalize on the proliferation of low-cost genomic sequencing, can narrow the time lag between virus discovery and targeted research, surveillance, and management.
Progress in combatting zoonoses that emerge from wildlife is often constrained by limited knowledge of the biology of pathogens within reservoir hosts. We focus on the host-pathogen dynamics of four ...emerging viruses associated with bats: Hendra, Nipah, Ebola, and Marburg viruses. Spillover of bat infections to humans and domestic animals often coincides with pulses of viral excretion within bat populations, but the mechanisms driving such pulses are unclear. Three hypotheses dominate current research on these emerging bat infections. First, pulses of viral excretion could reflect seasonal epidemic cycles driven by natural variations in population densities and contact rates among hosts. If lifelong immunity follows recovery, viruses may disappear locally but persist globally through migration; in either case, new outbreaks occur once births replenish the susceptible pool. Second, epidemic cycles could be the result of waning immunity within bats, allowing local circulation of viruses through oscillating herd immunity. Third, pulses could be generated by episodic shedding from persistently infected bats through a combination of physiological and ecological factors. The three scenarios can yield similar patterns in epidemiological surveys, but strategies to predict or manage spillover risk resulting from each scenario will be different. We outline an agenda for research on viruses emerging from bats that would allow for differentiation among the scenarios and inform development of evidence-based interventions to limit threats to human and animal health. These concepts and methods are applicable to a wide range of pathogens that affect humans, domestic animals, and wildlife.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Bartonella spp. are globally distributed bacteria that cause endocarditis in humans and domestic animals. Recent work has suggested bats as zoonotic reservoirs of some human Bartonella infections; ...however, the ecological and spatiotemporal patterns of infection in bats remain largely unknown. Here we studied the genetic diversity, prevalence of infection across seasons and years, individual risk factors, and possible transmission routes of Bartonella in populations of common vampire bats (Desmodus rotundus) in Peru and Belize, for which high infection prevalence has previously been reported. Phylogenetic analysis of the gltA gene for a subset of PCR-positive blood samples revealed sequences that were related to Bartonella described from vampire bats from Mexico, other Neotropical bat species, and streblid bat flies. Sequences associated with vampire bats clustered significantly by country but commonly spanned Central and South America, implying limited spatial structure. Stable and nonzero Bartonella prevalence between years supported endemic transmission in all sites. The odds of Bartonella infection for individual bats was unrelated to the intensity of bat flies ectoparasitism, but nearly all infected bats were infested, which precluded conclusive assessment of support for vector-borne transmission. While metagenomic sequencing found no strong evidence of Bartonella DNA in pooled bat saliva and fecal samples, we detected PCR positivity in individual saliva and feces, suggesting the potential for bacterial transmission through both direct contact (i.e., biting) and environmental (i.e., fecal) exposures. Further investigating the relative contributions of direct contact, environmental, and vector-borne transmission for bat Bartonella is an important next step to predict infection dynamics within bats and the risks of human and livestock exposures.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
Preventing zoonotic emergence from bats requires integrative research
Coronavirus disease 2019 (COVID-19) is the latest in a distressing tally of viral infections—including Ebola, Nipah, rabies, ...severe acute respiratory syndrome (SARS), and Middle East respiratory syndrome (MERS)—that have evolutionary origins or epidemiological associations with bats. This seeming preponderance of zoonoses has propelled bats from biomedical obscurity to the forefront of global health. Immunological traits have been proposed to allow bats to control viruses differently from other animals. However, incomplete baselines for broader comparisons across vertebrates and extensive immunological variation among bat species casts uncertainty on their distinctiveness as viral reservoirs. Moreover, common perceptions that bats asymptomatically harbor viruses more often than other animals and that their viruses are more diverse or pose systematically heightened zoonotic risk remain unresolved. The search for answers may inspire new approaches to manage disease threats to human and animal health.
Humans have altered ecosystems worldwide, and it is important to understand how this land use change impacts infectious disease transmission in humans and animals. We conducted a systematic review ...305 scientific articles investigating how specific types of anthropogenic land use change influence infectious disease dynamics. We summarized findings, highlighted common themes, and drew attention to neglected areas of research. There was an increase in publications on this topic over the last 30 years spanning diseases of humans, livestock, and wildlife, including a large number of zoonotic pathogens. Most papers (66.9%) were observational, 30.8% were review or concept papers, and few studies (2.3%) were experimental in nature, with most studies focusing on vector-borne and/or multi-host pathogens. Common land use change types related to disease transmission were deforestation/forest fragmentation/habitat fragmentation, agricultural development/irrigation, and urbanization/suburbanization. In response to anthropogenic change, more than half of the studies (56.9%) documented increased pathogen transmission, 10.4% of studies observed decreased pathogen transmission, 30.4% had variable and complex pathogen responses, and 2.4% showed no detectable changes. Commonly reported mechanisms by which land use change altered infectious disease transmission included alteration of the vector, host, and pathogen niche, changes in host and vector community composition, changes in behavior or movement of vectors and/or hosts, altered spatial distribution of hosts and/or vectors, and socioeconomic factors, and environmental contamination. We discussed observed patterns in the literature and make suggestions for future research directions, emphasizing the importance of ecological and evolutionary theory to understand pathogen responses in changing landscapes.
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EMUNI, FIS, FZAB, GEOZS, GIS, IJS, IMTLJ, KILJ, KISLJ, MFDPS, NLZOH, NUK, OBVAL, OILJ, PNG, SAZU, SBCE, SBJE, SBMB, SBNM, UKNU, UL, UM, UPUK, VKSCE, ZAGLJ
1. Supplemental food provided to wildlife by human activities can be more abundant and predictable than natural resources, and subsequent changes in wildlife ecology can have profound impacts on ...host-parasite interactions. Identifying traits of species associated with increases or decreases in infection outcomes with resource provisioning could improve assessments of wildlife most prone to disease risks in changing environments. 2. We conducted a phylogenetic meta-analysis of 342 host-parasite interactions across 56 wildlife species and three broad taxonomic groups of parasites to identify host-level traits that influence whether provisioning is associated with increases or decreases in infection. 3. We predicted dietary generalists that capitalize on novel food would show greater infection in provisioned habitats owing to population growth and food-borne exposure to contaminants and parasite infectious stages. Similarly, species with fast life histories could experience stronger demographic and immunological benefits from provisioning that affect parasite transmission. We also predicted that wide-ranging and migratory behaviours could increase infection risks with provisioning if concentrated and non-seasonal foods promote dense aggregations that increase exposure to parasites. 4. We found that provisioning increased infection with bacteria, viruses, fungi and protozoa (i.e. microparasites) most for wide-ranging, dietary generalist host species. Effect sizes for ectoparasites were also highest for host species with large home ranges but were instead lowest for dietary generalists. In contrast, the type of provisioning was a stronger correlate of infection outcomes for helminths than host species traits. 5. Our analysis highlights host traits related to movement and feeding behaviour as important determinants of whether species experience greater infection with supplemental feeding. These results could help prioritize monitoring wildlife with particular trait profiles in anthropogenic habitats to reduce infectious disease risks in provisioned populations.
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BFBNIB, FZAB, GIS, IJS, INZLJ, KILJ, NLZOH, NMLJ, NUK, OILJ, PNG, SAZU, SBCE, SBMB, UL, UM, UPUK, ZRSKP
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