Structural network characteristics affect epidemic severity and prediction in social contact networks.

Understanding and mitigating epidemic spread in complex networks requires the measurement of structural network properties associated with epidemic risk. Classic measures of epidemic thresholds like the basic reproduction number (R0) have been adapted to account for the structure of social contact networks but still may be unable to capture epidemic potential relative to more recent measures based on spectral graph properties. Here, we explore the ability of R0 and the spectral radius of the social contact network to estimate epidemic susceptibility. To do so, we simulate epidemics on a series of constructed (small world, scale-free, and random networks) and a collection of over 700 empirical biological social contact networks. Further, we explore how other network properties are related to these two epidemic estimators (R0 and spectral radius) and mean infection prevalence in simulated epidemics. Overall, we find that network properties strongly influence epidemic dynamics and the subsequent utility of R0 and spectral radius as indicators of epidemic risk.

Vector communities under global change may exacerbate and redistribute infectious disease risk.

Vector-borne parasites may be transmitted by multiple vector species, resulting in an increased risk of transmission, potentially at larger spatial scales compared to any single vector species. Additionally, the different abilities of patchily distributed vector species to acquire and transmit parasites will lead to varying degrees of transmission risk. Investigation of how vector community composition and parasite transmission change over space due to variation in environmental conditions may help to explain current patterns in diseases but also informs our understanding of how patterns will change under climate and land-use change. We developed a novel statistical approach using a multi-year, spatially extensive case study involving a vector-borne virus affecting white-tailed deer transmitted by Culicoides midges. We characterized the structure of vector communities, established the ecological gradient controlling change in structure, and related the ecology and structure to the amount of disease reporting observed in host populations. We found that vector species largely occur and replace each other as groups, rather than individual species. Moreover, community structure is primarily controlled by temperature ranges, with certain communities being consistently associated with high levels of disease reporting. These communities are essentially composed of species previously undocumented as potential vectors, whereas communities containing putative vector species were largely associated with low levels, or even absence, of disease reporting. We contend that the application of metacommunity ecology to vector-borne infectious disease ecology can greatly aid the identification of transmission hotspots and an understanding of the ecological drivers of parasite transmission risk both now and in the future.

Epidemic time series similarity is related to geographic distance and age structure.

Objective: More similar locations may have similar infectious disease dynamics. There is clear overlap in putative causes for epidemic similarity, such as geographic distance, age structure, and population size. We compare the effects of these potential drivers on epidemic similarity compared to a baseline assumption that differences in the basic reproductive number (R 0) will translate to differences in epidemic trajectories. Methods: Using COVID-19 case counts from United States counties, we explore the importance of geographic distance, population size differences, and age structure dissimilarity on resulting epidemic similarity. Results: We find clear effects of geographic space, age structure, population size, and R 0 on epidemic similarity, but notably the effect of age structure was stronger than the baseline assumption that differences in R 0 would be most related to epidemic similarity. Conclusions: Together, this highlights the role of spatial and demographic processes on SARS-CoV2 epidemics in the United States.

Effects of occupancy estimation on abundance-occupancy relationships.

Abundance-occupancy relationships predict that species that occupy more sites are also more locally abundant, where occupancy is usually estimated following the assumption that species can occupy all sampled sites. Here we use the National Ecological Observatory Network small-mammal data to assess whether this assumption affects abundance-occupancy relationships. We estimated occupancy considering all sampled sites (traditional occupancy) and only the sites found within the species geographic range (spatial occupancy) and realized environmental niche (environmental occupancy). We found that when occupancy was estimated considering only sites possible for the species to colonize (spatial and environmental occupancy) weaker abundance-occupancy relationships were observed. This shows that the assumption that the species can occupy all sampled sites directly affects the assessment of abundance-occupancy relationships. Estimating occupancy considering only sites that are possible for the species to colonize will consequently lead to a more robust assessment of abundance-occupancy relationships.

The Global Virome in One Network (VIRION): an Atlas of Vertebrate-Virus Associations.

Data that catalogue viral diversity on Earth have been fragmented across sources, disciplines, formats, and various degrees of open sharing, posing challenges for research on macroecology, evolution, and public health. Here, we solve this problem by establishing a dynamically maintained database of vertebrate-virus associations, called The Global Virome in One Network (VIRION). The VIRION database has been assembled through both reconciliation of static data sets and integration of dynamically updated databases. These data sources are all harmonized against one taxonomic backbone, including metadata on host and virus taxonomic validity and higher classification; additional metadata on sampling methodology and evidence strength are also available in a harmonized format. In total, the VIRION database is the largest open-source, open-access database of its kind, with roughly half a million unique records that include 9,521 resolved virus "species" (of which 1,661 are ICTV ratified), 3,692 resolved vertebrate host species, and 23,147 unique interactions between taxonomically valid organisms. Together, these data cover roughly a quarter of mammal diversity, a 10th of bird diversity, and ∼6% of the estimated total diversity of vertebrates, and a much larger proportion of their virome than any previous database. We show how these data can be used to test hypotheses about microbiology, ecology, and evolution and make suggestions for best practices that address the unique mix of evidence that coexists in these data. IMPORTANCE Animals and their viruses are connected by a sprawling, tangled network of species interactions. Data on the host-virus network are available from several sources, which use different naming conventions and often report metadata in different levels of detail. VIRION is a new database that combines several of these existing data sources, reconciles taxonomy to a single consistent backbone, and reports metadata in a format designed by and for virologists. Researchers can use VIRION to easily answer questions like "Can any fish viruses infect humans?" or "Which bats host coronaviruses?" or to build more advanced predictive models, making it an unprecedented step toward a full inventory of the global virome.

Improved chromosome-level genome assembly of the Glanville fritillary butterfly (Melitaea cinxia) integrating Pacific Biosciences long reads and a high-density linkage map.

BACKGROUND: The Glanville fritillary (Melitaea cinxia) butterfly is a model system for metapopulation dynamics research in fragmented landscapes. Here, we provide a chromosome-level assembly of the butterfly's genome produced from Pacific Biosciences sequencing of a pool of males, combined with a linkage map from population crosses. RESULTS: The final assembly size of 484 Mb is an increase of 94 Mb on the previously published genome. Estimation of the completeness of the genome with BUSCO indicates that the genome contains 92-94% of the BUSCO genes in complete and single copies. We predicted 14,810 genes using the MAKER pipeline and manually curated 1,232 of these gene models. CONCLUSIONS: The genome and its annotated gene models are a valuable resource for future comparative genomics, molecular biology, transcriptome, and genetics studies on this species.

Optimising predictive models to prioritise viral discovery in zoonotic reservoirs.

Despite the global investment in One Health disease surveillance, it remains difficult and costly to identify and monitor the wildlife reservoirs of novel zoonotic viruses. Statistical models can guide sampling target prioritisation, but the predictions from any given model might be highly uncertain; moreover, systematic model validation is rare, and the drivers of model performance are consequently under-documented. Here, we use the bat hosts of betacoronaviruses as a case study for the data-driven process of comparing and validating predictive models of probable reservoir hosts. In early 2020, we generated an ensemble of eight statistical models that predicted host-virus associations and developed priority sampling recommendations for potential bat reservoirs of betacoronaviruses and bridge hosts for SARS-CoV-2. During a time frame of more than a year, we tracked the discovery of 47 new bat hosts of betacoronaviruses, validated the initial predictions, and dynamically updated our analytical pipeline. We found that ecological trait-based models performed well at predicting these novel hosts, whereas network methods consistently performed approximately as well or worse than expected at random. These findings illustrate the importance of ensemble modelling as a buffer against mixed-model quality and highlight the value of including host ecology in predictive models. Our revised models showed an improved performance compared with the initial ensemble, and predicted more than 400 bat species globally that could be undetected betacoronavirus hosts. We show, through systematic validation, that machine learning models can help to optimise wildlife sampling for undiscovered viruses and illustrates how such approaches are best implemented through a dynamic process of prediction, data collection, validation, and updating.

Temporal variability in population and community dynamics.

Populations and communities fluctuate in their overall numbers through time, and the magnitude of fluctuations in individual species may scale to communities. However, the composite variability at the community scale is expected to be tempered by opposing fluctuations in individual populations, a phenomenon often called the portfolio effect. Understanding population variability, how it scales to community variability, and the spatial scaling in this variability are pressing needs given shifting environmental conditions and community composition. We explore evidence for portfolio effects using null community simulations and a large collection of empirical community time series from the BioTIME database. Additionally, we explore the relative roles of habitat type and geographic location on population and community temporal variability. We find strong portfolio effects in our theoretical community model, but weak effects in empirical data, suggesting a role for shared environmental responses, interspecific competition, or a litany of other factors. Furthermore, we observe a clear latitudinal signal - and differences among habitat types - in population and community variability. Together, this highlights the need to develop realistic models of community dynamics, and hints at spatial, and underlying environmental, gradients in variability in both population and community dynamics.

Estimating R 0 from early exponential growth: parallels between 1918 influenza and 2020 SARS-CoV-2 pandemics.

The large spatial scale, geographical overlap, and similarities in transmission mode between the 1918 H1N1 influenza and 2020 SARS-CoV-2 pandemics together provide a novel opportunity to investigate relationships between transmission of two different diseases in the same location. To this end, we use initial exponential growth rates in a Bayesian hierarchical framework to estimate the basic reproductive number, R 0, of both disease outbreaks in a common set of 43 cities in the United States. By leveraging multiple epidemic time series across a large spatial area, we are able to better characterize the variation in R 0 across the United States. Additionally, we provide one of the first city-level comparisons of R 0 between these two pandemics and explore how demography and outbreak timing are related to R 0. Despite similarities in transmission modes and a common set of locations, R 0 estimates for COVID-19 were uncorrelated with estimates of pandemic influenza R 0 in the same cities. Also, the relationships between R 0 and key population or epidemic traits differed between diseases. For example, epidemics that started later tended to be less severe for COVID-19, while influenza epidemics exhibited an opposite pattern. Our results suggest that despite similarities between diseases, epidemics starting in the same location may differ markedly in their initial progression.

The science of the host-virus network.

Better methods to predict and prevent the emergence of zoonotic viruses could support future efforts to reduce the risk of epidemics. We propose a network science framework for understanding and predicting human and animal susceptibility to viral infections. Related approaches have so far helped to identify basic biological rules that govern cross-species transmission and structure the global virome. We highlight ways to make modelling both accurate and actionable, and discuss the barriers that prevent researchers from translating viral ecology into public health policies that could prevent future pandemics.

The future of zoonotic risk prediction.

In the light of the urgency raised by the COVID-19 pandemic, global investment in wildlife virology is likely to increase, and new surveillance programmes will identify hundreds of novel viruses that might someday pose a threat to humans. To support the extensive task of laboratory characterization, scientists may increasingly rely on data-driven rubrics or machine learning models that learn from known zoonoses to identify which animal pathogens could someday pose a threat to global health. We synthesize the findings of an interdisciplinary workshop on zoonotic risk technologies to answer the following questions. What are the prerequisites, in terms of open data, equity and interdisciplinary collaboration, to the development and application of those tools? What effect could the technology have on global health? Who would control that technology, who would have access to it and who would benefit from it? Would it improve pandemic prevention? Could it create new challenges? This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Spatial variation in species' roles in host-helminth networks.

Species interactions may vary considerably across space as a result of spatial and environmental gradients. With respect to host-parasite interactions, this suggests that host and parasite species may play different functional roles across the different networks they occur in. Using a global occurrence database of helminth parasites, we examine the conservation of species' roles using data on host-helminth interactions from 299 geopolitical locations. Defining species' roles in a two-dimensional space which captures the tendency of species to be more densely linked within species subgroups than between subgroups, we quantified species' roles in two ways, which captured if and which species' roles are conserved by treating species' utilization of this two-dimensional space as continuous, while also classifying species into categorical roles. Both approaches failed to detect the conservation of species' roles for a single species out of over 38 000 host and helminth parasite species. Together, our findings suggest that species' roles in host-helminth networks may not be conserved, pointing to the potential role of spatial and environmental gradients, as well as the importance of the context of the local host and helminth parasite community. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Forecasting parasite sharing under climate change.

Species are shifting their distributions in response to climate change. This geographic reshuffling may result in novel co-occurrences among species, which could lead to unseen biotic interactions, including the exchange of parasites between previously isolated hosts. Identifying potential new host-parasite interactions would improve forecasting of disease emergence and inform proactive disease surveillance. However, accurate predictions of future cross-species disease transmission have been hampered by the lack of a generalized approach and data availability. Here, we propose a framework to predict novel host-parasite interactions based on a combination of niche modelling of future host distributions and parasite sharing models. Using the North American ungulates as a proof of concept, we show this approach has high cross-validation accuracy in over 85% of modelled parasites and find that more than 34% of the host-parasite associations forecasted by our models have already been recorded in the literature. We discuss potential sources of uncertainty and bias that may affect our results and similar forecasting approaches, and propose pathways to generate increasingly accurate predictions. Our results indicate that forecasting parasite sharing in response to shifts in host geographic distributions allow for the identification of regions and taxa most susceptible to emergent pathogens under climate change. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

The ghost of hosts past: impacts of host extinction on parasite specificity.

A growing body of research is focused on the extinction of parasite species in response to host endangerment and declines. Beyond the loss of parasite species richness, host extinction can impact apparent parasite host specificity, as measured by host richness or the phylogenetic distances among hosts. Such impacts on the distribution of parasites across the host phylogeny can have knock-on effects that may reshape the adaptation of both hosts and parasites, ultimately shifting the evolutionary landscape underlying the potential for emergence and the evolution of virulence across hosts. Here, we examine how the reshaping of host phylogenies through extinction may impact the host specificity of parasites, and offer examples from historical extinctions, present-day endangerment, and future projections of biodiversity loss. We suggest that an improved understanding of the impact of host extinction on contemporary host-parasite interactions may shed light on core aspects of disease ecology, including comparative studies of host specificity, virulence evolution in multi-host parasite systems, and future trajectories for host and parasite biodiversity. This article is part of the theme issue 'Infectious disease macroecology: parasite diversity and dynamics across the globe'.

Species-area and network-area relationships in host-helminth interactions.

The scaling relationship observed between species richness and the geographical area sampled (i.e. the species-area relationship (SAR)) is a widely recognized macroecological relationship. Recently, this theory has been extended to trophic interactions, suggesting that geographical area may influence the structure of species interaction networks (i.e. network-area relationships (NARs)). Here, we use a global dataset of host-helminth parasite interactions to test existing predictions from macroecological theory. Scaling between single locations to the global host-helminth network by sequentially adding networks together, we find support that geographical area influences species richness and the number of species interactions in host-helminth networks. However, species-area slopes were larger for host species relative to their helminth parasites, counter to theoretical predictions. Lastly, host-helminth network modularity-capturing the tendency of the network to form into separate subcommunities-decreased with increasing area, also counter to theoretical predictions. Reconciling this disconnect between existing theory and observed SAR and NAR will provide insight into the spatial structuring of ecological networks, and help to refine theory to highlight the effects of network type, species distributional overlap, and the specificity of trophic interactions on NARs.

Initial abundance and stochasticity influence competitive outcome in communities.

Predicting competitive outcomes in communities frequently involves inferences based on deterministic population models since these provide clear criteria for exclusion (e.g. R* rule) or long-term coexistence (e.g. mutual invasibility). However, incorporating stochasticity into population- or community-level processes into models is necessary if the goal is to explain variation in natural systems, which are inherently stochastic. Similarly, in systems with demographic or environmental stochasticity, weaker competitors have the potential to exclude superior competitors, contributing to what is known as 'competitive indeterminacy'. The importance of such effects for natural communities is unknown, in part because it is difficult to demonstrate that multiple forms of stochasticity are present in these communities. Moreover, the effects of multiple forms of stochasticity on competitive outcomes are largely untested, even in theory. Here, we address these issues by examining the role of stochasticity in replicated communities of flour beetles (Tribolium sp.). To do so, we developed a set of two-species stochastic Ricker models incorporating four distinct forms of stochasticity: environmental stochasticity, demographic stochasticity, demographic heterogeneity and stochastic sex determination. By fitting models to experimental data, and simulating fit models to examine long- term behaviour, we found that both the duration of transient coexistence and the degree of competitive indeterminacy were sensitive to the forms of stochasticity included in our models. These findings suggest the current estimates of extinction risk, coexistence and time until competitive exclusion in communities may not be accurate when based on models that exclude relevant forms of stochasticity.

Taxonomic resolution affects host-parasite association model performance.

Identifying the factors that structure host­parasite interactions is fundamental to understand the drivers of species distributions and to predict novel cross-species transmission events. More phylogenetically related host species tend to have more similar parasite associations, but parasite specificity may vary as a function of transmission mode, parasite taxonomy or life history. Accordingly, analyses that attempt to infer host−parasite associations using combined data on different parasite groups may perform quite differently relative to analyses on each parasite subset. In essence, are more data always better when predicting host−parasite associations, or does parasite taxonomic resolution matter? Here, we explore how taxonomic resolution affects predictive models of host−parasite associations using the London Natural History Museum's database of host­helminth interactions. Using boosted regression trees, we demonstrate that taxon-specific models (i.e. of Acanthocephalans, Nematodes and Platyhelminthes) consistently outperform full models in predicting mammal-helminth associations. At finer spatial resolutions, full and taxon-specific model performance does not vary, suggesting tradeoffs between phylogenetic and spatial scales of analysis. Although all models identify similar host and parasite covariates as important to such patterns, our results emphasize the importance of phylogenetic scale in the study of host­parasite interactions and suggest that using taxonomic subsets of data may improve predictions of parasite distributions and cross-species transmission. Predictive models of host­pathogen interactions should thus attempt to encompass the spatial resolution and phylogenetic scale desired for inference and prediction and potentially use model averaging or ensemble models to combine predictions from separately trained models.

What would it take to describe the global diversity of parasites?

How many parasites are there on Earth? Here, we use helminth parasites to highlight how little is known about parasite diversity, and how insufficient our current approach will be to describe the full scope of life on Earth. Using the largest database of host-parasite associations and one of the world's largest parasite collections, we estimate a global total of roughly 100 000-350 000 species of helminth endoparasites of vertebrates, of which 85-95% are unknown to science. The parasites of amphibians and reptiles remain the most poorly described, but the majority of undescribed species are probably parasites of birds and bony fish. Missing species are disproportionately likely to be smaller parasites of smaller hosts in undersampled countries. At current rates, it would take centuries to comprehensively sample, collect and name vertebrate helminths. While some have suggested that macroecology can work around existing data limitations, we argue that patterns described from a small, biased sample of diversity aren't necessarily reliable, especially as host-parasite networks are increasingly altered by global change. In the spirit of moonshots like the Human Genome Project and the Global Virome Project, we consider the idea of a Global Parasite Project: a global effort to transform parasitology and inventory parasite diversity at an unprecedented pace.

Community context and dispersal stochasticity drive variation in spatial spread.

Dispersal is a key process in shaping species spatial distributions. Species interactions and variation in dispersal probabilities may jointly influence species spatial dynamics. However, many studies examine dispersal as a neutral process, independent of community context or intraspecific variation in dispersal behaviour. Here, we use controlled, replicated communities of two Tribolium species (T. castaneum and T. confusum) to examine how intraspecific variation in dispersal behaviour and community context influence dispersal dynamics in simple experimental landscapes composed of homogeneous habitat patches. We found considerable individual-level variation in dispersal probability that was unrelated to body size variation. Further, the context of dispersal mattered, as T. castaneum dispersal was reduced in two-species communities, while T. confusum dispersal was unaffected by community composition. Incorporating individual-level variation into a two-species stochastic spatial Ricker model, we provide evidence that individual-level variability in dispersal behaviour results in more variable spatial spread than assuming individuals have the same dispersal probability. Further, interspecific competition resulted in more variable spatial spread. The variability in spatial spread observed in our tightly controlled and replicated experimental system and in our stochastic model simulations points to potential fundamental limitations in forecasting species shifting ranges without considering potential interspecific interactions and demographic variability in dispersal behaviour.

What determines parasite species richness across host species?

IN FOCUS: Dáttilo, W., Barrozo-Chávez, N., Lira-Noriega, A., Guevara, R., Villalobos, F., Santiago-Alarcon, D., Neves, F. S., Izzo, T., & Ribeiro, S. P. (2020). Species-level drivers of mammalian ectoparasite faunas. Journal of Animal Ecology. https://doi.org/10.1111/1365-2656.13216. The question of what drives the number of parasite species able to infect a given host species is still a largely open question, despite decades of research. Dáttilo and colleagues examine the potential drivers of ectoparasite species across a large set of host species to explore the taxonomic and trait drivers of host-parasite interactions. Here, we contextualize their findings, explore what is known about parasite species richness, and identify some potential next steps towards answers.