Interconnecting global threats: climate change, biodiversity loss, and infectious diseases.

The concurrent pressures of rising global temperatures, rates and incidence of species decline, and emergence of infectious diseases represent an unprecedented planetary crisis. Intergovernmental reports have drawn focus to the escalating climate and biodiversity crises and the connections between them, but interactions among all three pressures have been largely overlooked. Non-linearities and dampening and reinforcing interactions among pressures make considering interconnections essential to anticipating planetary challenges. In this Review, we define and exemplify the causal pathways that link the three global pressures of climate change, biodiversity loss, and infectious disease. A literature assessment and case studies show that the mechanisms between certain pairs of pressures are better understood than others and that the full triad of interactions is rarely considered. Although challenges to evaluating these interactions-including a mismatch in scales, data availability, and methods-are substantial, current approaches would benefit from expanding scientific cultures to embrace interdisciplinarity and from integrating animal, human, and environmental perspectives. Considering the full suite of connections would be transformative for planetary health by identifying potential for co-benefits and mutually beneficial scenarios, and highlighting where a narrow focus on solutions to one pressure might aggravate another.

Network embedding unveils the hidden interactions in the mammalian virome.

Predicting host-virus interactions is fundamentally a network science problem. We develop a method for bipartite network prediction that combines a recommender system (linear filtering) with an imputation algorithm based on low-rank graph embedding. We test this method by applying it to a global database of mammal-virus interactions and thus show that it makes biologically plausible predictions that are robust to data biases. We find that the mammalian virome is under-characterized anywhere in the world. We suggest that future virus discovery efforts could prioritize the Amazon Basin (for its unique coevolutionary assemblages) and sub-Saharan Africa (for its poorly characterized zoonotic reservoirs). Graph embedding of the imputed network improves predictions of human infection from viral genome features, providing a shortlist of priorities for laboratory studies and surveillance. Overall, our study indicates that the global structure of the mammal-virus network contains a large amount of information that is recoverable, and this provides new insights into fundamental biology and disease emergence.

Using phylogeographic link-prediction in primates to prioritize human parasite screening.

Objectives: The ongoing risk of emerging infectious disease has renewed calls for understanding the origins of zoonoses and identifying future zoonotic disease threats. Given their close phylogenetic relatedness and geographic overlap with humans, non-human primates (NHPs) have been the source of many infectious diseases throughout human evolution. NHPs harbor diverse parasites, with some infecting only a single host species while others infect species from multiple families. Materials and Methods: We applied a novel link-prediction method to predict undocumented instances of parasite sharing between humans and NHPs. Our model makes predictions based on phylogenetic distances and geographic overlap among NHPs and humans in six countries with high NHP diversity: Columbia, Brazil, Democratic Republic of Congo, Madagascar, China and Indonesia. Results: Of the 899 human parasites documented in the Global Infectious Diseases and Epidemiology Network (GIDEON) database for these countries, 12% were shared with at least one other NHP species. The link prediction model identified an additional 54 parasites that are likely to infect humans but were not reported in GIDEON. These parasites were mostly host generalists, yet their phylogenetic host breadth varied substantially. Discussion: As human activities and populations encroach on NHP habitats, opportunities for parasite sharing between human and non-human primates will continue to increase. Our study identifies specific infectious organisms to monitor in countries with high NHP diversity, while the comparative analysis of host generalism, parasite taxonomy, and transmission mode provides insights to types of parasites that represent high zoonotic risk.

Past and future uses of text mining in ecology and evolution.

Ecology and evolutionary biology, like other scientific fields, are experiencing an exponential growth of academic manuscripts. As domain knowledge accumulates, scientists will need new computational approaches for identifying relevant literature to read and include in formal literature reviews and meta-analyses. Importantly, these approaches can also facilitate automated, large-scale data synthesis tasks and build structured databases from the information in the texts of primary journal articles, books, grey literature, and websites. The increasing availability of digital text, computational resources, and machine-learning based language models have led to a revolution in text analysis and natural language processing (NLP) in recent years. NLP has been widely adopted across the biomedical sciences but is rarely used in ecology and evolutionary biology. Applying computational tools from text mining and NLP will increase the efficiency of data synthesis, improve the reproducibility of literature reviews, formalize analyses of research biases and knowledge gaps, and promote data-driven discovery of patterns across ecology and evolutionary biology. Here we present recent use cases from ecology and evolution, and discuss future applications, limitations and ethical issues.

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.

Predicting missing links in global host-parasite networks.

1. Parasites that infect multiple species cause major health burdens globally, but for many, the full suite of susceptible hosts is unknown. Predicting undocumented host-parasite associations will help expand knowledge of parasite host specificities, promote the development of theory in disease ecology and evolution, and support surveillance of multi-host infectious diseases. The analysis of global species interaction networks allows for leveraging of information across taxa, but link prediction at this scale is often limited by extreme network sparsity and lack of comparable trait data across species. 2. Here we use recently developed methods to predict missing links in global mammal-parasite networks using readily available data: network properties and evolutionary relationships among hosts. We demonstrate how these link predictions can efficiently guide the collection of species interaction data and increase the completeness of global species interaction networks. 3. We amalgamate a global mammal host-parasite interaction network (>29,000 interactions) and apply a hierarchical Bayesian approach for link prediction that leverages information on network structure and scaled phylogenetic distances among hosts. We use these predictions to guide targeted literature searches of the most likely yet undocumented interactions, and identify empirical evidence supporting many of the top 'missing' links. 4. We find that link prediction in global host-parasite networks can successfully predict parasites of humans, domesticated animals and endangered wildlife, representing a combination of published interactions missing from existing global databases, and potential but currently undocumented associations. 5. Our study provides further insight into the use of phylogenies for predicting host-parasite interactions, and highlights the utility of iterated prediction and targeted search to efficiently guide the collection of information on host-parasite interactions. These data are critical for understanding the evolution of host specificity, and may be used to support disease surveillance through a process of predicting missing links, and targeting research towards the most likely undocumented interactions.

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.

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'.

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'.

Opposing macroevolutionary and trait-mediated patterns of threat and naturalisation in flowering plants.

Due to expanding global trade and movement of people, new plant species are establishing in exotic ranges at increasing rates while the number of native species facing extinction from multiple threats grows. Yet, how species losses and gains globally may, together, be linked to traits and macroevolutionary processes is poorly understood. Here, we show that, adjusting for diversification rate and clade age, the proportion of threatened species across flowering plant families is negatively related to the proportion of naturalised species per family. Moreover, naturalisation is positively associated with range size, short generation time, autonomous seed production and interspecific hybridisation, but negatively with age and diversification, whereas threat is negatively associated with range size and hybridisation, and positively with biotic pollination, age and diversification rate. That we find such a pronounced signature of naturalisation and threat across plant families suggests that both trait syndromes have coexisted over deep evolutionary time and counter to intuition, that neither strategy is necessarily superior to the other over long evolutionary timespans.

Ecological indicators of mammal exposure to Ebolavirus.

Much of the basic ecology of Ebolavirus remains unresolved despite accumulating disease outbreaks, viral strains and evidence of animal hosts. Because human Ebolavirus epidemics have been linked to contact with wild mammals other than bats, traits shared by species that have been infected by Ebolavirus and their phylogenetic distribution could suggest ecological mechanisms contributing to human Ebolavirus spillovers. We compiled data on Ebolavirus exposure in mammals and corresponding data on life-history traits, movement, and diet, and used boosted regression trees (BRT) to identify predictors of exposure and infection for 119 species (hereafter hosts). Mapping the phylogenetic distribution of presumptive Ebolavirus hosts reveals that they are scattered across several distinct mammal clades, but concentrated among Old World fruit bats, primates and artiodactyls. While sampling effort was the most important predictor, explaining nearly as much of the variation among hosts as traits, BRT models distinguished hosts from all other species with greater than 97% accuracy, and revealed probable Ebolavirus hosts as large-bodied, frugivorous, and with slow life histories. Provisionally, results suggest that some insectivorous bat genera, Old World monkeys and forest antelopes should receive priority in Ebolavirus survey efforts. This article is part of the theme issue 'Dynamic and integrative approaches to understanding pathogen spillover'.

Disease mortality in domesticated animals is predicted by host evolutionary relationships.

Infectious diseases of domesticated animals impact human well-being via food insecurity, loss of livelihoods, and human infections. While much research has focused on parasites that infect single host species, most parasites of domesticated mammals infect multiple species. The impact of multihost parasites varies across hosts; some rarely result in death, whereas others are nearly always fatal. Despite their high ecological and societal costs, we currently lack theory for predicting the lethality of multihost parasites. Here, using a global dataset of >4,000 case-fatality rates for 65 infectious diseases (caused by microparasites and macroparasites) and 12 domesticated host species, we show that the average evolutionary distance from an infected host to other mammal host species is a strong predictor of disease-induced mortality. We find that as parasites infect species outside of their documented phylogenetic host range, they are more likely to result in lethal infections, with the odds of death doubling for each additional 10 million years of evolutionary distance. Our results for domesticated animal diseases reveal patterns in the evolution of highly lethal parasites that are difficult to observe in the wild and further suggest that the severity of infectious diseases may be predicted from evolutionary relationships among hosts.

Bacterial diversity in the waterholes of the Kruger National Park: an eDNA metabarcoding approach 1.

Bacteria are essential components of natural environments. They contribute to ecosystem functioning through roles as mutualists and pathogens for larger species, and as key components of food webs and nutrient cycles. Bacterial communities respond to environmental disturbances, and the tracking of these communities across space and time may serve as indicators of ecosystem health in areas of conservation concern. Recent advances in DNA sequencing of environmental samples allow for rapid and culture-free characterization of bacterial communities. Here we conduct the first metabarcoding survey of bacterial diversity in the waterholes of the Kruger National Park, South Africa. We show that eDNA can be amplified from waterholes and find strongly structured microbial communities, likely reflecting local abiotic conditions, animal ecology, and anthropogenic disturbance. Over timescales from days to weeks we find increased turnover in community composition, indicating bacteria may represent host-associated taxa of large vertebrates visiting the waterholes. Through taxonomic annotation we also identify pathogenic taxa, demonstrating the utility of eDNA metabarcoding for surveillance of infectious diseases. These samples serve as a baseline survey of bacterial diversity in the Kruger National Park, and in the future, spatially distinct microbial communities may be used as markers of ecosystem disturbance, or biotic homogenization across the park.

Global Mammal Parasite Database version 2.0.

Illuminating the ecological and evolutionary dynamics of parasites is one of the most pressing issues facing modern science, and is critical for basic science, the global economy, and human health. Extremely important to this effort are data on the disease-causing organisms of wild animal hosts (including viruses, bacteria, protozoa, helminths, arthropods, and fungi). Here we present an updated version of the Global Mammal Parasite Database, a database of the parasites of wild ungulates (artiodactyls and perissodactyls), carnivores, and primates, and make it available for download as complete flat files. The updated database has more than 24,000 entries in the main data file alone, representing data from over 2700 literature sources. We include data on sampling method and sample sizes when reported, as well as both "reported" and "corrected" (i.e., standardized) binomials for each host and parasite species. Also included are current higher taxonomies and data on transmission modes used by the majority of species of parasites in the database. In the associated metadata we describe the methods used to identify sources and extract data from the primary literature, how entries were checked for errors, methods used to georeference entries, and how host and parasite taxonomies were standardized across the database. We also provide definitions of the data fields in each of the four files that users can download.

Tongues on the EDGE: language preservation priorities based on threat and lexical distinctiveness.

Languages are being lost at rates exceeding the global loss of biodiversity. With the extinction of a language we lose irreplaceable dimensions of culture and the insight it provides on human history and the evolution of linguistic diversity. When setting conservation goals, biologists give higher priority to species likely to go extinct. Recent methods now integrate information on species evolutionary relationships to prioritize the conservation of those with a few close relatives. Advances in the construction of language trees allow us to use these methods to develop language preservation priorities that minimize loss of linguistic diversity. The evolutionarily distinct and globally endangered (EDGE) metric, used in conservation biology, accounts for a species' originality (evolutionary distinctiveness-ED) and its likelihood of extinction (global endangerment-GE). Here, we use a similar framework to inform priorities for language preservation by generating rankings for 350 Austronesian languages. Kavalan, Tanibili, Waropen and Sengseng obtained the highest EDGE scores, while Xârâcùù (Canala), Nengone and Palauan are among the most linguistically distinct, but are not currently threatened. We further provide a way of dealing with incomplete trees, a common issue for both species and language trees.

The macroecology of infectious diseases: a new perspective on global-scale drivers of pathogen distributions and impacts.

Identifying drivers of infectious disease patterns and impacts at the broadest scales of organisation is one of the most crucial challenges for modern science, yet answers to many fundamental questions remain elusive. These include what factors commonly facilitate transmission of pathogens to novel host species, what drives variation in immune investment among host species, and more generally what drives global patterns of parasite diversity and distribution? Here we consider how the perspectives and tools of macroecology, a field that investigates patterns and processes at broad spatial, temporal and taxonomic scales, are expanding scientific understanding of global infectious disease ecology. In particular, emerging approaches are providing new insights about scaling properties across all living taxa, and new strategies for mapping pathogen biodiversity and infection risk. Ultimately, macroecology is establishing a framework to more accurately predict global patterns of infectious disease distribution and emergence.

Response to Strona & Fattorini: are generalist parasites being lost from their hosts?

We respond to criticism of our recent paper by examining assumptions about the structure of host-parasite networks, and discuss the implications of host extinction on our perception of parasite specificity.

The path to host extinction can lead to loss of generalist parasites.

Host extinction can alter disease transmission dynamics, influence parasite extinction and ultimately change the nature of host-parasite systems. While theory predicts that single-host parasites are among the parasite species most susceptible to extinction following declines in their hosts, documented parasite extinctions are rare. Using a comparative approach, we investigate how the richness of single-host and multi-host parasites is influenced by extinction risk among ungulate and carnivore hosts. Host-parasite associations for free-living carnivores (order Carnivora) and terrestrial ungulates (orders Perissodactyla + Cetartiodactyla minus cetaceans) were merged with host trait data and IUCN Red List status to explore the distribution of single-host and multi-host parasites among threatened and non-threatened hosts. We find that threatened ungulates harbour a higher proportion of single-host parasites compared to non-threatened ungulates, which is explained by decreases in the richness of multi-host parasites. However, among carnivores threat status is not a significant predictor of the proportion of single-host parasites, or the richness of single-host or multi-host parasites. The loss of multi-host parasites from threatened ungulates may be explained by decreased cross-species contact as hosts decline and habitats become fragmented. Among carnivores, threat status may not be important in predicting patterns of parasite specificity because host decline results in equal losses of both single-host parasites and multi-host parasites through reduction in average population density and frequency of cross-species contact. Our results contrast with current models of parasite coextinction and highlight the need for updated theories that are applicable across host groups and account for both inter- and intraspecific contact.