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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Multiple spatial behaviours govern social network positions in a wild ungulate.

The structure of wild animal social systems depends on a complex combination of intrinsic and extrinsic drivers. Population structuring and spatial behaviour are key determinants of individuals' observed social behaviour, but quantifying these spatial components alongside multiple other drivers remains difficult due to data scarcity and analytical complexity. We used a 43-year dataset detailing a wild red deer population to investigate how individuals' spatial behaviours drive social network positioning, while simultaneously assessing other potential contributing factors. Using Integrated Nested Laplace Approximation (INLA) multi-matrix animal models, we demonstrate that social network positions are shaped by two-dimensional landscape locations, pairwise space sharing, individual range size, and spatial and temporal variation in population density, alongside smaller but detectable impacts of a selection of individual-level phenotypic traits. These results indicate strong, multifaceted spatiotemporal structuring in this society, emphasising the importance of considering multiple spatial components when investigating the causes and consequences of sociality.

Fitness Costs of Parasites Explain Multiple Life-History Trade-Offs in a Wild Mammal.

AbstractReproduction in wild animals can divert limited resources away from immune defense, resulting in increased parasite burdens. A long-standing prediction of life-history theory states that these parasites can harm the reproductive individual, reducing its subsequent survival and fecundity, producing reproduction-fitness trade-offs. Here, we examined associations among reproductive allocation, immunity, parasitism, and subsequent survival and fecundity in a wild population of individually identified red deer (Cervus elaphus). Using path analysis, we investigated whether costs of lactation in terms of downstream survival and fecundity were mediated by changes in strongyle nematode count and mucosal antibody levels. Lactating females exhibited increased parasite counts, which were in turn associated with substantially decreased fitness in the following year in terms of overwinter survival, fecundity, subsequent calf weight, and parturition date. This study offers observational evidence for parasite regulation of multiple life-history trade-offs, supporting the role of parasites as an important mediating factor in wild mammal populations.

Unifying spatial and social network analysis in disease ecology.

Social network analysis has achieved remarkable popularity in disease ecology, and is sometimes carried out without investigating spatial heterogeneity. Many investigations into sociality and disease may nevertheless be subject to cryptic spatial variation, so ignoring spatial processes can limit inference regarding disease dynamics. Disease analyses can gain breadth, power and reliability from incorporating both spatial and social behavioural data. However, the tools for collecting and analysing these data simultaneously can be complex and unintuitive, and it is often unclear when spatial variation must be accounted for. These difficulties contribute to the scarcity of simultaneous spatial-social network analyses in disease ecology thus far. Here, we detail scenarios in disease ecology that benefit from spatial-social analysis. We describe procedures for simultaneous collection of both spatial and social data, and we outline statistical approaches that can control for and estimate spatial-social covariance in disease ecology analyses. We hope disease researchers will expand social network analyses to more often include spatial components and questions. These measures will increase the scope of such analyses, allowing more accurate model estimates, better inference of transmission modes, susceptibility effects and contact scaling patterns, and ultimately more effective disease interventions.

Synzootics.

Ecologists increasingly recognise coinfection as an important component of emergent epidemiological patterns, connecting aspects of ecoimmunology, behaviour, ecosystem function and even extinction risk. Building on syndemic theory in medical anthropology, we propose the term 'synzootics' to describe co-occurring enzootic or epizootic processes that produce worse health outcomes in wild animals. Using framing from syndemic theory, we describe how the synzootic concept offers new insights into the ecology and evolution of infectious diseases. We then recommend a set of empirical criteria and lines of evidence that can be used to identify synzootics in nature. We conclude by exploring how synzootics could indirectly drive the emergence of novel pathogens in human populations.

Negative density-dependent parasitism in a group-living carnivore.

Animals living at high population densities commonly experience greater exposure to disease, leading to increased parasite burdens. However, social animals can benefit immunologically and hygienically from cooperation, and individuals may alter their socio-spatial behaviour in response to infection, both of which could counteract density-related increases in exposure. Consequently, the costs and benefits of sociality for disease are often uncertain. Here, we use a long-term study of a wild European badger population (Meles meles) to investigate how within-population variation in host density determines infection with multiple parasites. Four out of five parasite taxa exhibited consistent spatial hotspots of infection, which peaked among badgers living in areas of low local population density. Combined movement, survival, spatial and social network analyses revealed that parasite avoidance was the likely cause of this negative density dependence, with possible roles for localized mortality, encounter-dilution effects, and micronutrient-enhanced immunity. These findings demonstrate that animals can organize their societies in space to minimize parasite infection, with important implications for badger behavioural ecology and for the control of badger-associated diseases.

Expanding host specificity and pathogen sharing beyond viruses.

Most emerging pathogens of humans can infect multiple host species (Woolhouse & Gowtage-Sequeria, 2005). This simple fact has motivated multiple large-scale, comparative analyses of the drivers of pathogen sharing and zoonotic pathogen richness among hosts as well as the factors determining the zoonotic potential of pathogens themselves. However, most of this work focuses on viruses, limiting a broader understanding of how host range varies within and between pathogen groups. In this issue of Molecular Ecology, Shaw et al. (2020) compile a comprehensive data set of host-pathogen associations across viruses and bacteria and test whether previous patterns observed in the former occur in the latter. They find most viruses and bacteria are specialists, and viruses are more likely to be generalists; however, generalist bacteria encompass multiple host orders, whereas viral sharing occurs more within host orders. Lastly, the authors demonstrate that many factors previously identified as predictors of zoonotic richness for viruses occur for bacteria and that host phylogenetic similarity is a primary determinant of cross-species transmission. However, pathogen sharing with humans was more common and more weakly related to phylogenetic distance to Homo sapiens for bacteria compared to viruses, suggesting the former could pose greater spillover risks across host orders. This work represents a key advance in our understanding of host specificity and pathogen sharing beyond viruses.

Testing possible causes of gametocyte reduction in temporally out-of-synch malaria infections.

BACKGROUND: The intraerythrocytic development cycle (IDC) of the rodent malaria Plasmodium chabaudi is coordinated with host circadian rhythms. When this coordination is disrupted, parasites suffer a 50% reduction in both asexual stages and sexual stage gametocytes over the acute phase of infection. Reduced gametocyte density may not simply follow from a loss of asexuals because investment into gametocytes ("conversion rate") is a plastic trait; furthermore, the densities of both asexuals and gametocytes are highly dynamic during infection. Hence, the reasons for the reduction of gametocytes in infections that are out-of-synch with host circadian rhythms remain unclear. Here, two explanations are tested: first, whether out-of-synch parasites reduce their conversion rate to prioritize asexual replication via reproductive restraint; second, whether out-of-synch gametocytes experience elevated clearance by the host's circadian immune responses. METHODS: First, conversion rate data were analysed from a previous experiment comparing infections of P. chabaudi that were in-synch or 12 h out-of-synch with host circadian rhythms. Second, three new experiments examined whether the inflammatory cytokine TNF varies in its gametocytocidal efficacy according to host time-of-day and gametocyte age. RESULTS: There was no evidence that parasites reduce conversion or that their gametocytes become more vulnerable to TNF when out-of-synch with host circadian rhythms. CONCLUSIONS: The factors causing the reduction of gametocytes in out-of-synch infections remain mysterious. Candidates for future investigation include alternative rhythmic factors involved in innate immune responses and the rhythmicity in essential resources required for gametocyte development. Explaining why it matters for gametocytes to be synchronized to host circadian rhythms might suggest novel approaches to blocking transmission.

Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence.

The prevalence and intensity of parasites in wild hosts varies across space and is a key determinant of infection risk in humans, domestic animals and threatened wildlife. Because the immune system serves as the primary barrier to infection, replication and transmission following exposure, we here consider the environmental drivers of immunity. Spatial variation in parasite pressure, abiotic and biotic conditions, and anthropogenic factors can all shape immunity across spatial scales. Identifying the most important spatial drivers of immunity could help pre-empt infectious disease risks, especially in the context of how large-scale factors such as urbanization affect defence by changing environmental conditions. We provide a synthesis of how to apply macroecological approaches to the study of ecoimmunology (i.e. macroimmunology). We first review spatial factors that could generate spatial variation in defence, highlighting the need for large-scale studies that can differentiate competing environmental predictors of immunity and detailing contexts where this approach might be favoured over small-scale experimental studies. We next conduct a systematic review of the literature to assess the frequency of spatial studies and to classify them according to taxa, immune measures, spatial replication and extent, and statistical methods. We review 210 ecoimmunology studies sampling multiple host populations. We show that whereas spatial approaches are relatively common, spatial replication is generally low and unlikely to provide sufficient environmental variation or power to differentiate competing spatial hypotheses. We also highlight statistical biases in macroimmunology, in that few studies characterize and account for spatial dependence statistically, potentially affecting inferences for the relationships between environmental conditions and immune defence. We use these findings to describe tools from geostatistics and spatial modelling that can improve inference about the associations between environmental and immunological variation. In particular, we emphasize exploratory tools that can guide spatial sampling and highlight the need for greater use of mixed-effects models that account for spatial variability while also allowing researchers to account for both individual- and habitat-level covariates. We finally discuss future research priorities for macroimmunology, including focusing on latitudinal gradients, range expansions and urbanization as being especially amenable to large-scale spatial approaches. Methodologically, we highlight critical opportunities posed by assessing spatial variation in host tolerance, using metagenomics to quantify spatial variation in parasite pressure, coupling large-scale field studies with small-scale field experiments and longitudinal approaches, and applying statistical tools from macroecology and meta-analysis to identify generalizable spatial patterns. Such work will facilitate scaling ecoimmunology from individual- to habitat-level insights about the drivers of immune defence and help predict where environmental change may most alter infectious disease risk.

Seasonality of helminth infection in wild red deer varies between individuals and between parasite taxa.

Parasitism in wild mammals can vary according to myriad intrinsic and extrinsic factors, many of which vary seasonally. However, seasonal variation in parasitism is rarely studied using repeated samples from known individuals. Here we used a wild population of individually recognized red deer (Cervus elaphus) on the Isle of Rum to quantify seasonality and intrinsic factors affecting gastrointestinal helminth parasitism over the course of a year. We collected 1020 non-invasive faecal samples from 328 known individuals which we then analysed for propagules of three helminth taxa: strongyle nematodes, the common liver fluke Fasciola hepatica and the tissue nematode Elaphostrongylus cervi. Zero-inflated Poisson models were used to investigate how season, age and sex were associated with parasite prevalence and count intensity, while Poisson models were used to quantify individual repeatability within and between sampling seasons. Parasite intensity and prevalence varied according to all investigated factors, with opposing seasonality, age profiles and sex biases between parasite taxa. Repeatability was moderate, decreased between seasons and varied between parasites; both F. hepatica and E. cervi showed significant between-season repeatability, while strongyle nematode counts were only repeatable within-season and showed no repeatability within individuals across the year.

Ants show a leftward turning bias when exploring unknown nest sites.

Behavioural lateralization in invertebrates is an important field of study because it may provide insights into the early origins of lateralization seen in a diversity of organisms. Here, we present evidence for a leftward turning bias in Temnothorax albipennis ants exploring nest cavities and in branching mazes, where the bias is initially obscured by thigmotaxis (wall-following) behaviour. Forward travel with a consistent turning bias in either direction is an effective nest exploration method, and a simple decision-making heuristic to employ when faced with multiple directional choices. Replication of the same bias at the colony level would also reduce individual predation risk through aggregation effects, and may lead to a faster attainment of a quorum threshold for nest migration. We suggest the turning bias may be the result of an evolutionary interplay between vision, exploration and migration factors, promoted by the ants' eusociality.