Network Models: An Underutilized Tool in Wildlife Epidemiology?

Although the approach of contact network epidemiology has been increasing in popularity for studying transmission of infectious diseases in human populations, it has generally been an underutilized approach for investigating disease outbreaks in wildlife populations. In this paper we explore the differences between the type of data that can be collected on human and wildlife populations, provide an update on recent advances that have been made in wildlife epidemiology by using a network approach, and discuss why networks might have been underutilized and why networks could and should be used more in the future. We conclude with ideas for future directions and a call for field biologists and network modelers to engage in more cross-disciplinary collaboration

Genotype and sex-based host variation in behavior and susceptibility drives population disease dynamics

Host heterogeneity in pathogen transmission is widespread and presents a major hurdle to predicting and minimizing disease outbreaks. Using Drosophila melanogaster infected with Drosophila C virus as a model system, we integrated experimental measurements of social aggregation, virus shedding, and disease-induced mortality from different genetic lines and sexes into a disease modelling framework. The experimentally measured host heterogeneity produced substantial differences in simulated disease outbreaks, providing evidence for genetic and sex-specific effects on disease dynamics at a population level. While this was true for homogeneous populations of single sex/genetic line, the genetic background or sex of the index case did not alter outbreak dynamics in simulated, heterogeneous populations. Finally, to explore the relative effects of social aggregation, viral shedding and mortality, we compared simulations where we allowed these traits to vary, as measured experimentally, to simulations where we constrained variation in these traits to the population mean. In this context, variation in infectiousness, followed by social aggregation, was the most influential component of transmission. Overall, we show that host heterogeneity in three host traits dramatically affects population-level transmission, but the relative impact of this variation depends on both the susceptible population diversity and the distribution of population-level variation

Planetary Grand Challenges: A Call for Interdisciplinary Partnerships

Universities have traditionally been places where individual scholars work on individual topics, in individual disciplines, with individual funding. Even though large research institutions include all the major disciplines, faculty and students remain in their schools or colleges, rarely crossing the campus to interact. Matters do not improve once knowledge is generated. Each discipline has its own journals, its own conferences, and its own professional organizations. The academy was designed to support unparalleled expertise in specialized knowledge. However, universities are beginning to realize that the greatest challenges we face are systems problems and can only be solved by systems thinking and systems solutions. Climate change, antibiotic resistance, water scarcity, and unsustainable population growth are just a few of the planetary health crises that require interdisciplinary partnerships to solve. Fortunately, we are beginning to see early signs of a shift toward, and even normalization of, interdisciplinary collaboration. In fact, some national grants require team members from different fields as a stipulation for funding. Interdisciplinary research permits cross-field benefits in which the synergy of two or more knowledge sets is greater than the sum of its parts. Innovation increases and previously elusive solutions become possible. The field of partnership studies closely aligns with the vision and mission of interdisciplinarity and offers a philosophical framework to guide teaching and research

Investigating the Dynamics of Elk Population Size and Body Mass in a Seasonal Environment Using a Mechanistic Integral Projection Model

Environmentally mediated changes in body size often underlie population responses to environmental change, yet this is not a universal phenomenon. Understanding when phenotypic change underlies population responses to environmental change is important for obtaining insights and robust predictions of population dynamics in a changing world. We develop a dynamic integral projection model that mechanistically links environmental conditions to demographic rates and phenotypic traits (body size) via changes in resource availability and individual energetics. We apply the model to the northern Yellowstone elk population and explore population responses to changing patterns of seasonality, incorporating the interdependence of growth, demography, and density-dependent processes operating through population feedback on available resources. We found that small changes in body size distributions can have large impacts on population dynamics but need not cause population responses to environmental change. Environmental changes that altered demographic rates directly, via increasing or decreasing resource availability, led to large population impacts in the absence of substantial changes to body size distributions. In contrast, environmentally driven shifts in body size distributions could occur with little consequence for population dynamics when the effect of environmental change on resource availability was small and seasonally restricted and when strong density-dependent processes counteracted expected population responses. These findings highlight that a robust understanding of how associations between body size and demography influence population responses to environmental change will require knowledge of the shape of the relationship between phenotypic distributions and vital rates, the population status with regard to its carrying capacity, and importantly the nature of the environmentally driven change in body size and carrying capacity

Defining an epidemiological landscape that connects movement ecology to pathogen transmission and pace-of-life

Pathogen transmission depends on host density, mobility and contact. These components emerge from host and pathogen movements that themselves arise through interactions with the surrounding environment. The environment, the emergent host and pathogen movements, and the subsequent patterns of density, mobility and contact form an ‘epidemiological landscape’ connecting the environment to specific locations where transmissions occur. Conventionally, the epidemiological landscape has been described in terms of the geographical coordinates where hosts or pathogens are located. We advocate for an alternative approach that relates those locations to attributes of the local environment. Environmental descriptions can strengthen epidemiological forecasts by allowing for predictions even when local geographical data are not available. Environmental predictions are more accessible than ever thanks to new tools from movement ecology, and we introduce a ‘movement-pathogen pace of life’ heuristic to help identify aspects of movement that have the most influence on spatial epidemiology. By linking pathogen transmission directly to the environment, the epidemiological landscape offers an efficient path for using environmental information to inform models describing when and where transmission will occur

“One Health” or Three? Publication Silos Among the One Health Disciplines

The One Health initiative is a global effort fostering interdisciplinary collaborations to address challenges in human, animal, and environmental health. While One Health has received considerable press, its benefits remain unclear because its effects have not been quantitatively described. We systematically surveyed the published literature and used social network analysis to measure interdisciplinarity in One Health studies constructing dynamic pathogen transmission models. The number of publications fulfilling our search criteria increased by 14.6% per year, which is faster than growth rates for life sciences as a whole and for most biology subdisciplines. Surveyed publications clustered into three communities: one used by ecologists, one used by veterinarians, and a third diverse-authorship community used by population biologists, mathematicians, epidemiologists, and experts in human health. Overlap between these communities increased through time in terms of author number, diversity of co-author affiliations, and diversity of citations. However, communities continue to differ in the systems studied, questions asked, and methods employed. While the infectious disease research community has made significant progress toward integrating its participating disciplines, some segregation—especially along the veterinary/ecological research interface—remains

Using host traits to predict reservoir host species of rabies virus

Wildlife are important reservoirs for many pathogens, yet the role that different species play in pathogen maintenance frequently remains unknown. This is the case for rabies, a viral disease of mammals. While Carnivora (carnivores) and Chiroptera (bats) are the canonical mammalian orders known to be responsible for the maintenance and onward transmission of rabies Lyssavirus (RABV), the role of most species within these orders remains unknown and is continually changing as a result of contemporary host shifting. We combined a trait-based analytical approach with gradient boosting machine learning models to identify physiological and ecological host features associated with being a reservoir for RABV. We then used a cooperative game theory approach to determine species-specific traits associated with known RABV reservoirs. Being a carnivore reservoir for RABV was associated with phylogenetic similarity to known RABV reservoirs, along with other traits such as having larger litters and earlier sexual maturity. For bats, location in the Americas and geographic range were the most important predictors of RABV reservoir status, along with having a large litter. Our models identified 44 carnivore and 34 bat species that are currently not recognized as RABV reservoirs, but that have trait profiles suggesting their capacity to be or become reservoirs. Further, our findings suggest that potential reservoir species among bats and carnivores occur both within and outside of areas with current RABV circulation. These results show the ability of a trait-based approach to detect potential reservoirs of infection and could inform rabies control programs and surveillance efforts by identifying the types of species and traits that facilitate RABV maintenance and transmission

Cross‐species transmission and evolutionary dynamics of canine distemper virus during a spillover in African lions of Serengeti National Park

The outcome of pathogen spillover from a reservoir to a novel host population can range from a “dead‐end” when there is no onward transmission in the recipient population, to epidemic spread and even establishment in new hosts. Understanding the evolutionary epidemiology of spillover events leading to discrete outcomes in novel hosts is key to predicting risk and can lead to a better understanding of mechanisms of emergence. Here we use a Bayesian phylodynamic approach to examine cross‐species transmission and evolutionary dynamics during a canine distemper virus spillover event causing clinical disease and population decline in an African lion population (Panthera leo) in the Serengeti Ecological Region between 1993 and 1994. Using 21 near‐complete viral genomes from four species we found that this large‐scale outbreak was likely ignited by a single cross‐species spillover event from a canid reservoir to non‐canid hosts less than one year before disease detection and explosive spread of CDV in lions. Cross‐species transmission from other non‐canid species likely fueled the high prevalence of CDV across spatially structured lion prides. Multiple lines of evidence suggest that spotted hyenas (Crocuta crocuta) could have acted as the proximate source of CDV exposure in lions. We report thirteen nucleotide substitutions segregating CDV strains found in canids and non‐canids. Our results are consistent with the hypothesis that virus evolution played a role in CDV emergence in non‐canid hosts following spillover during the outbreak, and suggests that host barriers to clinical infection can limit outcomes of CDV spillover in novel host species

Transmission ecology of canine parvovirus in a multi-host, multi-pathogen system

Understanding multi-host pathogen maintenance and transmission dynamics is critical for disease control. However, transmission dynamics remain enigmatic largely because they are difficult to observe directly, particularly in wildlife. Here, we investigate the transmission dynamics of canine parvovirus (CPV) using state-space modelling of 20-years of CPV serology data from domestic dogs and African lions in the Serengeti ecosystem. We show that, although vaccination reduces the probability of infection in dogs, and despite indirect enhancement of population seropositivity as a result of vaccine shedding, the vaccination coverage achieved has been insufficient to prevent CPV from becoming widespread. CPV is maintained by the dog population and has become endemic with ~3.5-year cycles and prevalence reaching ~80%. While the estimated prevalence in lions is lower, peaks of infection consistently follow those in dogs. Dogs exposed to CPV are also more likely to become infected with a second multihost pathogen, canine distemper virus. However, vaccination can weaken this coupling raising questions about the value of monovalent versus polyvalent vaccines against these two pathogens. Our findings highlight the need to consider both pathogen- and host-level community interactions when seeking to understand the dynamics of multi-host pathogens and their implications for conservation, disease surveillance and control programmes