Using host species traits to understand the consequences of resource provisioning for host–parasite interactions

1.Supplemental food provided to wildlife by human activities can be more abundant and predictable than natural resources, and subsequent changes to 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 that 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 behaviors 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 behavior 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

Spatial expansions and travelling waves of rabies in vampire bats

A major obstacle to anticipating the cross-species transmission of zoonotic diseases and developing novel strategies for their control is the scarcity of data informing how these pathogens circulate within natural reservoir populations. Vampire bats are the primary reservoir of rabies in Latin America, where the disease remains among the most important viral zoonoses affecting humans and livestock. Unpredictable spatiotemporal dynamics of rabies within bat populations have precluded anticipation of outbreaks and undermined widespread bat culling programs. By analysing 1146 vampire bat-transmitted rabies (VBR) outbreaks in livestock across 12 years in Peru, we demonstrate that viral expansions into historically uninfected zones have doubled the recent burden of VBR. Viral expansions are geographically widespread, but severely constrained by high elevation peaks in the Andes mountains. Within Andean valleys, invasions form wavefronts that are advancing towards large, unvaccinated livestock populations that are heavily bitten by bats, which together will fuel high transmission and mortality. Using spatial models, we forecast the pathways of ongoing VBR epizootics across heterogeneous landscapes. These results directly inform vaccination strategies to mitigate impending viral emergence, reveal VBR as an emerging rather than an enzootic disease and create opportunities to test novel interventions to manage viruses in bat reservoirs

Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts

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

Are all hosts created equal? Partitioning host species contributions to parasite persistence in multihost communities

Many parasites circulate endemically within communities of multiple host species. To understand disease persistence within these communities, it is essential to know the contribution each host species makes to parasite transmission and maintenance. However, quantifying those contributions is challenging. We present a conceptual framework for classifying multihost sharing, based on key thresholds for parasite persistence. We then develop a generalized technique to quantify each species’ contribution to parasite persistence, allowing natural systems to be located within the framework. We illustrate this approach using data on gastrointestinal parasites circulating within rodent communities and show that, although many parasites infect several host species, parasite persistence is often driven by just one host species. In some cases, however, parasites require multiple host species for maintenance. Our approach provides a quantitative method for differentiating these cases using minimal reliance on system-specific parameters, enabling informed decisions about parasite management within poorly understood multihost communities

Contextualizing bats as viral reservoirs

No abstract available

Genetic diversity, infection prevalence, and possible transmission routes of Bartonella spp. in vampire bats

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

The role of viral evolution in rabies host shifts and emergence

Despite its ability to infect all mammals, Rabies virus persists in numerous species-specific cycles that rarely sustain transmission in alternative species. The determinants of these species-associations and the adaptive significance of genetic divergence between host-associated viruses are poorly understood. One explanation is that epidemiological separation between reservoirs causes neutral genetic differentiation. Indeed, recent studies attributed host shifts to ecological factors and selection of ‘preadapted’ viral variants from the existing viral community. However, phenotypic differences between isolates and broad scale comparative and molecular evolutionary analyses indicate multiple barriers that Rabies virus must overcome through adaptation. This review assesses various lines of evidence and proposes a synthetic hypothesis for the respective roles of ecology and evolution in Rabies virus host shifts

Vampire Bats and Rabies: Toward an Ecological Solution to a Public Health Problem

In the first half of 2011, 21 school-age children and two adults died of rabies transmitted by the common vampire bat (Desmodus rotundus) in and around the small rural village of Yupicusa in the Peruvian Amazon (Figure 1) [1]. This is only one of many such outbreaks occurring throughout the greater Amazon Basin (Figure 2), which, despite efforts at increasing education, vaccination, and bat population control, seem to have escalated over the last three decades—a timeline concurrent with major social and ecological changes in the area [2]. The remote and impoverished nature of communities affected by these outbreaks and the unique niche of vampire bats in a changing socioecological landscape create challenges beyond those faced in previous rabies control efforts and require new strategies to address this public health menace through ecosystem-level intervention. Here we examine this complex system and offer perspectives from a field expedition to Imaza following the 2011 outbreak

Predicting reservoir hosts and arthropod vectors from evolutionary signatures in RNA virus genomes

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

Predicting spatial spread of rabies in skunk populations using surveillance data reported by the public

Background: Prevention and control of wildlife disease invasions relies on the ability to predict spatio-temporal dynamics and understand the role of factors driving spread rates, such as seasonality and transmission distance. Passive disease surveillance (i.e., case reports by public) is a common method of monitoring emergence of wildlife diseases, but can be challenging to interpret due to spatial biases and limitations in data quantity and quality. Methodology/Principal findings: We obtained passive rabies surveillance data from dead striped skunks (Mephitis mephitis) in an epizootic in northern Colorado, USA. We developed a dynamic patch-occupancy model which predicts spatio-temporal spreading while accounting for heterogeneous sampling. We estimated the distance travelled per transmission event, direction of invasion, rate of spatial spread, and effects of infection density and season. We also estimated mean transmission distance and rates of spatial spread using a phylogeographic approach on a subsample of viral sequences from the same epizootic. Both the occupancy and phylogeographic approaches predicted similar rates of spatio-temporal spread. Estimated mean transmission distances were 2.3 km (95% Highest Posterior Density (HPD95): 0.02, 11.9; phylogeographic) and 3.9 km (95% credible intervals (CI95): 1.4, 11.3; occupancy). Estimated rates of spatial spread in km/year were: 29.8 (HPD95: 20.8, 39.8; phylogeographic, branch velocity, homogenous model), 22.6 (HPD95: 15.3, 29.7; phylogeographic, diffusion rate, homogenous model) and 21.1 (CI95: 16.7, 25.5; occupancy). Initial colonization probability was twice as high in spring relative to fall. Conclusions/Significance: Skunk-to-skunk transmission was primarily local (< 4 km) suggesting that if interventions were needed, they could be applied at the wave front. Slower viral invasions of skunk rabies in western USA compared to a similar epizootic in raccoons in the eastern USA implies host species or landscape factors underlie the dynamics of rabies invasions. Our framework provides a straightforward method for estimating rates of spatial spread of wildlife diseases