The coevolutionary mosaic of bat betacoronavirus emergence risk.

Pathogen evolution is one of the least predictable components of disease emergence, particularly in nature. Here, building on principles established by the geographic mosaic theory of coevolution, we develop a quantitative, spatially explicit framework for mapping the evolutionary risk of viral emergence. Driven by interest in diseases like Severe Acute Respiratory Syndrome (SARS), Middle East Respiratory Syndrome (MERS), and Coronavirus disease 2019 (COVID-19), we examine the global biogeography of bat-origin betacoronaviruses, and find that coevolutionary principles suggest geographies of risk that are distinct from the hotspots and coldspots of host richness. Further, our framework helps explain patterns like a unique pool of merbecoviruses in the Neotropics, a recently discovered lineage of divergent nobecoviruses in Madagascar, and-most importantly-hotspots of diversification in southeast Asia, sub-Saharan Africa, and the Middle East that correspond to the site of previous zoonotic emergence events. Our framework may help identify hotspots of future risk that have also been previously overlooked, like West Africa and the Indian subcontinent, and may more broadly help researchers understand how host ecology shapes the evolution and diversity of pandemic threats.

Comparative approaches in social network ecology.

Social systems vary enormously across the animal kingdom, with important implications for ecological and evolutionary processes such as infectious disease dynamics, anti-predator defence, and the evolution of cooperation. Comparing social network structures between species offers a promising route to help disentangle the ecological and evolutionary processes that shape this diversity. Comparative analyses of networks like these are challenging and have been used relatively little in ecology, but are becoming increasingly feasible as the number of empirical datasets expands. Here, we provide an overview of multispecies comparative social network studies in ecology and evolution. We identify a range of advancements that these studies have made and key challenges that they face, and we use these to guide methodological and empirical suggestions for future research. Overall, we hope to motivate wider publication and analysis of open social network datasets in animal ecology.

How behavioural ageing affects infectious disease.

Ageing is associated with profound changes in behaviour that could influence exposure and susceptibility to infectious disease. As well as determining emergent patterns of infection across individuals of different ages, behavioural ageing could interact with, confound, or counteract age-related changes in other traits. Here, we examine how behavioural ageing can manifest and influence patterns of infection in wild animals. We discuss a range of age-related changes that involve interactions between behaviour and components of exposure and susceptibility to infection, including social ageing and immunosenescence, acquisition of novel parasites and pathogens with age, changes in spatial behaviours, and age-related hygiene and sickness behaviours. Overall, most behavioural changes are expected to result in a reduced exposure rate, but there is relatively little evidence for this phenomenon, emerging largely from a rarity of explicit tests of exposure changes over the lifespan. This review offers a framework for understanding how ageing, behaviour, immunity, and infection interact, providing a series of hypotheses and testable predictions to improve our understanding of health in ageing societies.

Novel pathogen introduction triggers rapid evolution in animal social movement strategies.

Animal sociality emerges from individual decisions on how to balance the costs and benefits of being sociable. Novel pathogens introduced into wildlife populations should increase the costs of sociality, selecting against gregariousness. Using an individual-based model that captures essential features of pathogen transmission among social hosts, we show how novel pathogen introduction provokes the rapid evolutionary emergence and coexistence of distinct social movement strategies. These strategies differ in how they trade the benefits of social information against the risk of infection. Overall, pathogen-risk-adapted populations move more and have fewer associations with other individuals than their pathogen-risk-naive ancestors, reducing disease spread. Host evolution to be less social can be sufficient to cause a pathogen to be eliminated from a population, which is followed by a rapid recovery in social tendency. Our conceptual model is broadly applicable to a wide range of potential host-pathogen introductions and offers initial predictions for the eco-evolutionary consequences of wildlife pathogen spillover scenarios and a template for the development of theory in the ecology and evolution of animals' movement decisions.

Social responses to a hurricane drive greater epidemic risk.

The increasing frequency and intensity of extreme weather events due to climate change has the potential to alter ecosystem dynamics and wildlife health. Here we show that increasing social connections in response to a hurricane enhanced disease transmission risk for years after the event in a population of rhesus macaques. Our findings reveal that behavioural responses to natural disasters can elevate epidemic risk, thereby threatening wildlife health, population viability, and spillover to humans.

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.

Ecological drivers of sustained enzootic yellow fever virus transmission in Brazil, 2017-2021.

Beginning December 2016, sylvatic yellow fever (YF) outbreaks spread into southeastern Brazil, and Minas Gerais state experienced two sylvatic YF waves (2017 and 2018). Following these massive YF waves, we screened 187 free-living non-human primate (NHPs) carcasses collected throughout the state between January 2019 and June 2021 for YF virus (YFV) using RTqPCR. One sample belonging to a Callithrix, collected in June 2020, was positive for YFV. The viral strain belonged to the same lineage associated with 2017-2018 outbreaks, showing the continued enzootic circulation of YFV in the state. Next, using data from 781 NHPs carcasses collected in 2017-18, we used generalized additive mixed models (GAMMs) to identify the spatiotemporal and host-level drivers of YFV infection and intensity (an estimation of genomic viral load in the liver of infected NHP). Our GAMMs explained 65% and 68% of variation in virus infection and intensity, respectively, and uncovered strong temporal and spatial patterns for YFV infection and intensity. NHP infection was higher in the eastern part of Minas Gerais state, where 2017-2018 outbreaks affecting humans and NHPs were concentrated. The odds of YFV infection were significantly lower in NHPs from urban areas than from urban-rural or rural areas, while infection intensity was significantly lower in NHPs from urban areas or the urban-rural interface relative to rural areas. Both YFV infection and intensity were higher during the warm/rainy season compared to the cold/dry season. The higher YFV intensity in NHPs in warm/rainy periods could be a result of higher exposure to vectors and/or higher virus titers in vectors during this time resulting in the delivery of a higher virus dose and higher viral replication levels within NHPs. Further studies are needed to better test this hypothesis and further compare the dynamics of YFV enzootic cycles between different seasons.

Social Familiarity and Spatially Variable Environments Independently Determine Reproductive Fitness in a Wild Bird.

AbstractThe social interactions that an individual experiences are a key component of its environment and can have important consequences for reproductive success. The dear enemy effect posits that having familiar neighbors at a territory boundary can reduce the need for territory defense and competition and potentially increase cooperation. Although fitness benefits of reproducing among familiar individuals are documented in many species, it remains unclear to what extent these relationships are driven by direct benefits of familiarity itself versus other socioecological covariates of familiarity. We use 58 years of great tit (Parus major) breeding data to disentangle the relationship between neighbor familiarity, partner familiarity, and reproductive success while simultaneously considering individual and spatiotemporal effects. We find that neighbor familiarity was positively associated with reproductive success for females but not males, while an individual's familiarity with their breeding partner was associated with fitness benefits for both sexes. There was strong spatial heterogeneity in all investigated fitness components, but our findings were robust and significant over and above these effects. Our analyses are consistent with direct effects of familiarity on individuals' fitness outcomes. These results suggest that social familiarity can yield direct fitness benefits, potentially driving the maintenance of long-term bonds and evolution of stable social systems.

Host phylogeny and ecological associations best explain Wolbachia host shifts in scale insects.

Wolbachia are among the most prevalent and widespread endosymbiotic bacteria on Earth. Wolbachia's success in infecting an enormous number of arthropod species is attributed to two features: the range of phenotypes they induce in their hosts, and their ability to switch between host species. Whilst much progress has been made in elucidating their induced phenotypes, our understanding of Wolbachia host-shifting is still very limited: we lack answers to even fundamental questions concerning Wolbachia's routes of transfer and the importance of factors influencing host shifts. Here, we investigate the diversity and host-shift patterns of Wolbachia in scale insects, a group of arthropods with intimate associations with other insects that make them well suited to studying host shifts. Using Illumina multitarget amplicon sequencing of Wolbachia-infected scale insects and their direct associates we determined the identity of all Wolbachia strains. We then fitted a generalized additive mixed model to our data to estimate the influence of host phylogeny and the geographical distribution on Wolbachia strain sharing among scale insect species. The model predicts no significant contribution of host geography but strong effects of host phylogeny, with high rates of Wolbachia sharing among closely related species and a sudden drop-off in sharing with increasing phylogenetic distance. We also detected the same Wolbachia strain in scale insects and several intimately associated species (ants, wasps and flies). This indicates putative host shifts and potential routes of transfers via these associates and highlights the importance of ecological connectivity in Wolbachia host-shifting.

Behavioural ecology at the spatial-social interface.

Spatial and social behaviour are fundamental aspects of an animal's biology, and their social and spatial environments are indelibly linked through mutual causes and shared consequences. We define the 'spatial-social interface' as intersection of social and spatial aspects of individuals' phenotypes and environments. Behavioural variation at the spatial-social interface has implications for ecological and evolutionary processes including pathogen transmission, population dynamics, and the evolution of social systems. We link spatial and social processes through a foundation of shared theory, vocabulary, and methods. We provide examples and future directions for the integration of spatial and social behaviour and environments. We introduce key concepts and approaches that either implicitly or explicitly integrate social and spatial processes, for example, graph theory, density-dependent habitat selection, and niche specialization. Finally, we discuss how movement ecology helps link the spatial-social interface. Our review integrates social and spatial behavioural ecology and identifies testable hypotheses at the spatial-social interface.

Glycosylation and the global virome.

The sugars that coat the outsides of viruses and host cells are key to successful disease transmission, but they remain understudied compared to other molecular features. Understanding the comparative zoology of glycosylation - and harnessing it for predictive science - could help close the molecular gap in zoonotic risk assessment.

Pathogen transmission modes determine contact network structure, altering other pathogen characteristics.

Pathogen traits can vary greatly and heavily impact the ability of a pathogen to persist in a population. Although this variation is fundamental to disease ecology, little is known about the evolutionary pressures that drive these differences, particularly where they interact with host behaviour. We hypothesized that host behaviours relevant to different transmission routes give rise to differences in contact network structure, constraining the space over which pathogen traits can evolve to maximize fitness. Our analysis of 232 contact networks across mammals, birds, reptiles, amphibians, arthropods, fish and molluscs found that contact network topology varies by contact type, most notably in networks that are representative of fluid-exchange transmission. Using infectious disease model simulations, we showed that these differences in network structure suggest pathogens transmitted through fluid-exchange contact types will need traits associated with high transmissibility to successfully proliferate, compared to pathogens that transmit through other types of contact. These findings were supported through a review of known traits of pathogens that transmit in humans. Our work demonstrates that contact network structure may drive the evolution of compensatory pathogen traits according to transmission strategy, providing essential context for understanding pathogen evolution and ecology.

Helminth parasites are associated with reduced survival probability in young red deer.

Helminths are common parasites of wild ungulates that can have substantial costs for growth, mortality and reproduction. Whilst these costs are relatively well documented for mature animals, knowledge of helminths' impacts on juveniles is more limited. Identifying these effects is important because young individuals are often heavily infected, and juvenile mortality is a key process regulating wild populations. Here, we investigated associations between helminth infection and overwinter survival in juvenile wild red deer (Cervus elaphus) on the Isle of Rum, Scotland. We collected fecal samples non-invasively from known individuals and used them to count propagules of 3 helminth taxa (strongyle nematodes, Fasciola hepatica and Elaphostrongylus cervi). Using generalized linear models, we investigated associations between parasite counts and overwinter survival for calves and yearlings. Strongyles were associated with reduced survival in both age classes, and F. hepatica was associated with reduced survival in yearlings, whilst E. cervi infection showed no association with survival in either age class. This study provides observational evidence for fitness costs of helminth infection in juveniles of a wild mammal, and suggests that these parasites could play a role in regulating population dynamics.

Ageing red deer alter their spatial behaviour and become less social.

Social relationships are important to many aspects of animals' lives, and an individual's connections may change over the course of their lifespan. Currently, it is unclear whether social connectedness declines within individuals as they age, and what the underlying mechanisms might be, so the role of age in structuring animal social systems remains unresolved, particularly in non-primates. Here we describe senescent declines in social connectedness using 46 years of data in a wild, individually monitored population of a long-lived mammal (European red deer, Cervus elaphus). Applying a series of spatial and social network analyses, we demonstrate that these declines occur because of within-individual changes in social behaviour, with correlated changes in spatial behaviour (smaller home ranges and movements to lower-density, lower-quality areas). These findings demonstrate that within-individual socio-spatial behavioural changes can lead older animals in fission-fusion societies to become less socially connected, shedding light on the ecological and evolutionary processes structuring wild animal populations.

Mistletoes could moderate drought impacts on birds, but are themselves susceptible to drought-induced dieback.

Mistletoes are hemiparasitic plants and keystone species in many ecosystems globally. Given predicted increases in drought frequency and intensity, mistletoes may be crucial for moderating drought impacts on community structure. Dependent on host vascular flows, mistletoes can succumb to stress when water availability falls, making them susceptible to mortality during drought. We counted mistletoe across greater than 350 000 km2 of southeastern Australia and conducted standardized bird surveys between 2016 and 2021, spanning a major drought event in 2018-2019. We aimed to identify predictors of mistletoe abundance and mortality and determine whether mistletoes might moderate drought impacts on woodland birds. Live mistletoe abundance varied with tree species composition, land use and presence of mistletoebirds. Mistletoe mortality was widespread, consistent with high 2018/2019 summer temperatures, low 2019/2020 summer rainfall and the interaction between summer temperatures and rainfall in 2019/2020. The positive association between surviving mistletoes and woodland birds was greatest in the peak drought breeding seasons of 2018/2019 and 2019/2020, particularly for small residents and insectivores. Paradoxically, mistletoes could moderate drought impacts on birds, but are themselves vulnerable to drought-induced mortality. An improved understanding of the drivers and dynamics of mistletoe mortality is needed to address potential cascading trophic impacts associated with mistletoe die-off.

Urban-adapted mammal species have more known pathogens.

The world is rapidly urbanizing, inviting mounting concern that urban environments will experience increased zoonotic disease risk. Urban animals could have more frequent contact with humans, therefore transmitting more zoonotic parasites; however, this relationship is complicated by sampling bias and phenotypic confounders. Here we test whether urban mammal species host more zoonotic parasites, investigating the underlying drivers alongside a suite of phenotypic, taxonomic and geographic predictors. We found that urban-adapted mammals have more documented parasites and more zoonotic parasites: despite comprising only 6% of investigated species, urban mammals provided 39% of known host-parasite combinations. However, contrary to predictions, much of the observed effect was attributable to parasite discovery and research effort rather than to urban adaptation status, and urban-adapted species in fact hosted fewer zoonotic parasites than expected on the basis of their total parasite richness. We conclude that extended historical contact with humans has had a limited impact on zoonotic parasite richness in urban-adapted mammals; instead, their greater observed zoonotic richness probably reflects sampling bias arising from proximity to humans, supporting a near-universal conflation between zoonotic risk, research effort and synanthropy. These findings underscore the need to resolve the mechanisms linking anthropogenic change, sampling bias and observed wildlife disease dynamics.

Climate change increases cross-species viral transmission risk.

At least 10,000 virus species have the ability to infect humans but, at present, the vast majority are circulating silently in wild mammals1,2. However, changes in climate and land use will lead to opportunities for viral sharing among previously geographically isolated species of wildlife3,4. In some cases, this will facilitate zoonotic spillover-a mechanistic link between global environmental change and disease emergence. Here we simulate potential hotspots of future viral sharing, using a phylogeographical model of the mammal-virus network, and projections of geographical range shifts for 3,139 mammal species under climate-change and land-use scenarios for the year 2070. We predict that species will aggregate in new combinations at high elevations, in biodiversity hotspots, and in areas of high human population density in Asia and Africa, causing the cross-species transmission of their associated viruses an estimated 4,000 times. Owing to their unique dispersal ability, bats account for the majority of novel viral sharing and are likely to share viruses along evolutionary pathways that will facilitate future emergence in humans. Notably, we find that this ecological transition may already be underway, and holding warming under 2 °C within the twenty-first century will not reduce future viral sharing. Our findings highlight an urgent need to pair viral surveillance and discovery efforts with biodiversity surveys tracking the range shifts of species, especially in tropical regions that contain the most zoonoses and are experiencing rapid warming.

Assessing the risk of human-to-wildlife pathogen transmission for conservation and public health.

The SARS-CoV-2 pandemic has led to increased concern over transmission of pathogens from humans to animals, and its potential to threaten conservation and public health. To assess this threat, we reviewed published evidence of human-to-wildlife transmission events, with a focus on how such events could threaten animal and human health. We identified 97 verified examples, involving a wide range of pathogens; however, reported hosts were mostly non-human primates or large, long-lived captive animals. Relatively few documented examples resulted in morbidity and mortality, and very few led to maintenance of a human pathogen in a new reservoir or subsequent "secondary spillover" back into humans. We discuss limitations in the literature surrounding these phenomena, including strong evidence of sampling bias towards non-human primates and human-proximate mammals and the possibility of systematic bias against reporting human parasites in wildlife, both of which limit our ability to assess the risk of human-to-wildlife pathogen transmission. We outline how researchers can collect experimental and observational evidence that will expand our capacity for risk assessment for human-to-wildlife pathogen transmission.

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.

Mammal virus diversity estimates are unstable due to accelerating discovery effort.

Host-virus association data underpin research into the distribution and eco-evolutionary correlates of viral diversity and zoonotic risk across host species. However, current knowledge of the wildlife virome is inherently constrained by historical discovery effort, and there are concerns that the reliability of ecological inference from host-virus data may be undermined by taxonomic and geographical sampling biases. Here, we evaluate whether current estimates of host-level viral diversity in wild mammals are stable enough to be considered biologically meaningful, by analysing a comprehensive dataset of discovery dates of 6571 unique mammal host-virus associations between 1930 and 2018. We show that virus discovery rates in mammal hosts are either constant or accelerating, with little evidence of declines towards viral richness asymptotes, even in highly sampled hosts. Consequently, inference of relative viral richness across host species has been unstable over time, particularly in bats, where intensified surveillance since the early 2000s caused a rapid rearrangement of species' ranked viral richness. Our results illustrate that comparative inference of host-level virus diversity across mammals is highly sensitive to even short-term changes in sampling effort. We advise caution to avoid overinterpreting patterns in current data, since it is feasible that an analysis conducted today could draw quite different conclusions than one conducted only a decade ago.