Not your private tête-à-tête: leveraging the power of higher-order networks to study animal communication.

Animal communication is frequently studied with conventional network representations that link pairs of individuals who interact, for example, through vocalization. However, acoustic signals often have multiple simultaneous receivers, or receivers integrate information from multiple signallers, meaning these interactions are not dyadic. Additionally, non-dyadic social structures often shape an individual's behavioural response to vocal communication. Recently, major advances have been made in the study of these non-dyadic, higher-order networks (e.g. hypergraphs and simplicial complexes). Here, we show how these approaches can provide new insights into vocal communication through three case studies that illustrate how higher-order network models can: (i) alter predictions made about the outcome of vocally coordinated group departures; (ii) generate different patterns of song synchronization from models that only include dyadic interactions; and (iii) inform models of cultural evolution of vocal communication. Together, our examples highlight the potential power of higher-order networks to study animal vocal communication. We then build on our case studies to identify key challenges in applying higher-order network approaches in this context and outline important research questions that these techniques could help answer. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Social ageing can protect against infectious disease in a group-living primate.

The benefits of social living are well established, but sociality also comes with costs, including infectious disease risk. This cost-benefit ratio of sociality is expected to change across individuals' lifespans, which may drive changes in social behaviour with age. To explore this idea, we combine data from a group-living primate for which social ageing has been described with epidemiological models to show that having lower social connectedness when older can protect against the costs of a hypothetical, directly transmitted endemic pathogen. Assuming no age differences in epidemiological characteristics (susceptibility to, severity, and duration of infection), older individuals suffered lower infection costs, which was explained largely because they were less connected in their social networks than younger individuals. This benefit of 'social ageing' depended on epidemiological characteristics and was greatest when infection severity increased with age. When infection duration increased with age, social ageing was beneficial only when pathogen transmissibility was low. Older individuals benefited most from having a lower frequency of interactions (strength) and network embeddedness (closeness) and benefited less from having fewer social partners (degree). Our study provides a first examination of the epidemiology of social ageing, demonstrating the potential for pathogens to influence evolutionary dynamics of social ageing in natural populations.

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.

The interplay of social constraints and individual variation in risk tolerance in the emergence of superspreaders.

Individual host behaviours can drastically impact the spread of infection through a population. Differences in the value individuals place on both socializing with others and avoiding infection have been shown to yield emergent homophily in social networks and thereby shape epidemic outcomes. We build on this understanding to explore how individuals who do not conform to their social surroundings contribute to the propagation of infection during outbreaks. We show how non-conforming individuals, even if they do not directly expose a disproportionate number of other individuals themselves, can become functional superspreaders through an emergent social structure that positions them as the functional links by which infection jumps between otherwise separate communities. Our results can help estimate the potential success of real-world interventions that may be compromised by a small number of non-conformists if their impact is not anticipated, and plan for how best to mitigate their effects on intervention success.

Generation and applications of simulated datasets to integrate social network and demographic analyses.

Social networks are tied to population dynamics; interactions are driven by population density and demographic structure, while social relationships can be key determinants of survival and reproductive success. However, difficulties integrating models used in demography and network analysis have limited research at this interface. We introduce the R package genNetDem for simulating integrated network-demographic datasets. It can be used to create longitudinal social network and/or capture-recapture datasets with known properties. It incorporates the ability to generate populations and their social networks, generate grouping events using these networks, simulate social network effects on individual survival, and flexibly sample these longitudinal datasets of social associations. By generating co-capture data with known statistical relationships, it provides functionality for methodological research. We demonstrate its use with case studies testing how imputation and sampling design influence the success of adding network traits to conventional Cormack-Jolly-Seber (CJS) models. We show that incorporating social network effects into CJS models generates qualitatively accurate results, but with downward-biased parameter estimates when network position influences survival. Biases are greater when fewer interactions are sampled or fewer individuals observed in each interaction. While our results indicate the potential of incorporating social effects within demographic models, they show that imputing missing network measures alone is insufficient to accurately estimate social effects on survival, pointing to the importance of incorporating network imputation approaches. genNetDem provides a flexible tool to aid these methodological advancements and help researchers testing other sampling considerations in social network studies.

Influence of Lived Experiences on Public Responses to Future Diseases via (De)Sensitization of Concern.

OBJECTIVES: Public responses to a future novel disease might be influenced by a subset of individuals who are either sensitized or desensitized to concern-generating processes through their lived experiences during the coronavirus disease 2019 (COVID-19) pandemic. Such influences may be critical for shaping public health messaging during the next emerging threat. METHODS: This study explored the potential outcomes of the influence of lived experiences by using a dynamic multiplex network model to simulate a COVID-19 outbreak in a population of 2000 individuals, connected by means of disease and communication layers. Then a new disease was introduced, and a subset of individuals (50% or 100% of hospitalized during the COVID-19 outbreak) was assumed to be either sensitized or desensitized to concern-generating processes relative to the general population, which alters their adoption of non-pharmaceutical interventions (social distancing). RESULTS: Altered perceptions and behaviors from lived experiences with COVID-19 did not necessarily result in a strong mitigating effect for the novel outbreak. When public disease response is already strong or sensitization is assumed to be a robust effect, then a sensitized subset may enhance public mitigation of an outbreak through social distancing. CONCLUSIONS: In preparing for future outbreaks, assuming an experienced and disease-aware public may compromise effective design of effective public health messaging and mitigative action.

How reported outbreak data can shape individual behavior in a social world.

Agencies reporting on disease outbreaks face many choices about what to report and the scale of its dissemination. Reporting impacts an epidemic by influencing individual decisions directly, and the social network in which they are made. We simulated a dynamic multiplex network model-with coupled infection and communication layers-to examine behavioral impacts from the nature and scale of epidemiological information reporting. We explored how adherence to protective behaviors (social distancing) can be facilitated through epidemiological reporting, social construction of perceived risk, and local monitoring of direct connections, but eroded via social reassurance. We varied reported information (total active cases, daily new cases, hospitalizations, hospital capacity exceeded, or deaths) at one of two scales (population level or community level). Total active and new case reporting at the population level were the most effective approaches, relative to the other reporting approaches. Case reporting, which synergizes with test-trace-and-isolate and vaccination policies, should remain a priority throughout an epidemic.

Capturing complex interactions in disease ecology with simplicial sets.

Network approaches have revolutionized the study of ecological interactions. Social, movement and ecological networks have all been integral to studying infectious disease ecology. However, conventional (dyadic) network approaches are limited in their ability to capture higher-order interactions. We present simplicial sets as a tool that addresses this limitation. First, we explain what simplicial sets are. Second, we explain why their use would be beneficial in different subject areas. Third, we detail where these areas are: social, transmission, movement/spatial and ecological networks and when using them would help most in each context. To demonstrate their application, we develop a novel approach to identify how pathogens persist within a host population. Fourth, we provide an overview of how to use simplicial sets, highlighting specific metrics, generative models and software. Finally, we synthesize key research questions simplicial sets will help us answer and draw attention to methodological developments that will facilitate this.

High prevalence does not necessarily equal maintenance species: Avoiding biased claims of disease reservoirs when using surveillance data.

Many pathogens of public health and conservation concern persist in host communities. Identifying candidate maintenance and reservoir species is therefore a central component of disease management. The term maintenance species implies that if all species but the putative maintenance species were removed, then the pathogen would still persist. In the absence of field manipulations, this statement inherently requires a causal or mechanistic model to assess. However, we lack a systematic understanding of (i) how often conclusions are made about maintenance and reservoir species without reference to mechanistic models (ii) what types of biases may be associated with these conclusions and (iii) how explicitly invoking causal or mechanistic modelling can help ameliorate these biases. Filling these knowledge gaps is critical for robust inference about pathogen persistence and spillover in multihost-parasite systems, with clear implications for human and wildlife health. To address these gaps, we performed a literature review on the evidence previous studies have used to make claims regarding maintenance or reservoir species. We then developed multihost-parasite models to explore and demonstrate common biases that could arise when inferring maintenance potential from observational prevalence data. Finally, we developed new theory to show how model-driven inference of maintenance species can minimize and eliminate emergent biases. In our review, we found that 83% of studies used some form of observational prevalence data to draw conclusions on maintenance potential and only 6% of these studies combined observational data with mechanistic modelling. Using our model, we demonstrate how the community, spatial and temporal context of observational data can lead to substantial biases in inferences of maintenance potential. Importantly, our theory identifies that model-driven inference of maintenance species elucidates other streams of observational data that can be leveraged to correct these biases. Model-driven inference is an essential, yet underused, component of multidisciplinary studies that make inference about host reservoir and maintenance species. Better integration of wildlife disease surveillance and mechanistic models is necessary to improve the robustness and reproducibility of our conclusions regarding maintenance and reservoir species.

Diversity in valuing social contact and risk tolerance leading to the emergence of homophily in populations facing infectious threats.

How self-organization leads to the emergence of structure in social populations remains a fascinating and open question in the study of complex systems. One frequently observed structure that emerges again and again across systems is that of self-similar community, i.e., homophily. We use a game theoretic perspective to explore a case in which individuals choose affiliation partnerships based on only two factors: the value they place on having social contacts, and their risk tolerance for exposure to threat derived from social contact (e.g., infectious disease, threatening ideas, etc.). We show how diversity along just these two influences is sufficient to cause the emergence of self-organizing homophily in the population. We further consider a case in which extrinsic social factors influence the desire to maintain particular social ties, and show the robustness of emergent homophilic patterns to these additional influences. These results demonstrate how observable population-level homophily may arise out of individual behaviors that balance the value of social contacts against the potential risks associated with those contacts. We present and discuss these results in the context of outbreaks of infectious disease in human populations. Complementing the standard narrative about how social division alters epidemiological risk, we here show how epidemiological risk may deepen social divisions in human populations.

Balancing timeliness of reporting with increasing testing probability for epidemic data.

Reporting of epidemiological data requires coordinated action by numerous agencies, across a multitude of logistical steps. Using collated and reported information to inform direct interventions can be challenging due to associated delays. Mitigation can, however, occur indirectly through the public generation of concern, which facilitates adherence to protective behaviors. We utilized a coupled-dynamic multiplex network model with a communication- and disease-layer to examine how variation in reporting delay and testing probability are likely to impact adherence to protective behaviors, such as reducing physical contact. Individual concern mediated adherence and was informed by new- or active-case reporting, at the population- or community-level. Individuals received information from the communication layer: direct connections that were sick or adherent to protective behaviors increased their concern, but absence of illness eroded concern. Models revealed that the relative benefit of timely reporting and a high probability of testing was contingent on how much information was already obtained. With low rates of testing, increasing testing probability was of greater mitigating value. With high rates of testing, maximizing timeliness was of greater value. Population-level reporting provided advanced warning of disease risk from nearby communities; but we explore the relative costs and benefits of delays due to scale against the assumption that people may prioritize community-level information. Our findings emphasize the interaction of testing accuracy and reporting timeliness for the indirect mitigation of disease in a complex social system.

Associations between abundances of free-roaming gamebirds and common buzzards Buteo buteo are not driven by consumption of gamebirds in the buzzard breeding season.

Releasing gamebirds in large numbers for sport shooting may directly or indirectly influence the abundance, distribution and population dynamics of native wildlife. The abundances of generalist predators have been positively associated with the abundance of gamebirds. These relationships have implications for prey populations, with the potential for indirect impacts of gamebird releases on wider biodiversity. To understand the basis of these associations, we investigated variation in territory size, prey provisioning to chicks, and breeding success of common buzzards Buteo buteo, and associations with variation in the abundances of free-roaming gamebirds, primarily pheasants Phasianus colchicus, and of rabbits Oryctolagus cuniculus and field voles Microtus agrestis, as important prey for buzzards. The relative abundance of gamebirds, but not those of rabbits or voles, was weakly but positively correlated with our index of buzzard territory size. Gamebirds were rarely brought to the nest. Rabbits and voles, and not gamebirds, were provisioned to chicks in proportion to their relative abundance. The number of buzzard chicks increased with provisioning rates of rabbits, in terms of both provisioning frequency and biomass, but not with provisioning rates for gamebirds or voles. Associations between the abundances of buzzards and gamebirds may not be a consequence of the greater availability of gamebirds as prey during the buzzard breeding season. Instead, the association may arise either from habitat or predator management leading to higher densities of alternative prey (in this instance, rabbits), or from greater availability of gamebirds as prey or carrion during the autumn and winter shooting season. The interactions between gamebird releases and associated practices of predator control and shooting itself require better understanding to more effectively intervene in any one aspect of this complex social-ecological system.

Observations and conversations: how communities learn about infection risk can impact the success of non-pharmaceutical interventions against epidemics.

BACKGROUND: Individual behavioural decisions are responses to a person's perceived social norms that could be shaped by both their physical and social environment. In the context of the COVID-19 pandemic, these environments correspond to epidemiological risk from contacts and the social construction of risk by communication within networks of friends. Understanding the circumstances under which the influence of these different social networks can promote the acceptance of non-pharmaceutical interventions and consequently the adoption of protective behaviours is critical for guiding useful, practical public health messaging. METHODS: We explore how information from both physical contact and social communication layers of a multiplex network can contribute to flattening the epidemic curve in a community. Connections in the physical contact layer represent opportunities for transmission, while connections in the communication layer represent social interactions through which individuals may gain information, e.g. messaging friends. RESULTS: We show that maintaining focus on awareness of risk among each individual's physical contacts promotes the greatest reduction in disease spread, but only when an individual is aware of the symptoms of a non-trivial proportion of their physical contacts (~ ≥ 20%). Information from the social communication layer without was less useful when these connections matched less well with physical contacts and contributed little in combination with accurate information from physical contacts. CONCLUSIONS: We conclude that maintaining social focus on local outbreak status will allow individuals to structure their perceived social norms appropriately and respond more rapidly when risk increases. Finding ways to relay accurate local information from trusted community leaders could improve mitigation even where more intrusive/costly strategies, such as contact-tracing, are not possible.

Group size and modularity interact to shape the spread of infection and information through animal societies.

Social interactions between animals can provide many benefits, including the ability to gain useful environmental information through social learning. However, these social contacts can also facilitate the transmission of infectious diseases through a population. Animals engaging in social interactions therefore face a trade-off between the potential informational benefits and the risk of acquiring disease. Theoretical models have suggested that modular social networks, associated with the formation of groups or sub-groups, can slow spread of infection by trapping it within particular groups. However, these social structures will not necessarily impact the spread of information in the same way if its transmission follows a "complex contagion", e.g. through individuals disproportionally copying the majority (conformist learning). Here we use simulation models to demonstrate that modular networks can promote the spread of information relative to the spread of infection, but only when the network is fragmented and group sizes are small. We show that the difference in transmission between information and disease is maximised for more well-connected social networks when the likelihood of transmission is intermediate. Our results have important implications for understanding the selective pressures operating on the social structure of animal societies, revealing that highly fragmented networks such as those formed in fission-fusion social groups and multilevel societies can be effective in modulating the infection-information trade-off for individuals within them. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00265-021-03102-4.

The role of social structure and dynamics in the maintenance of endemic disease.

Social interactions are required for the direct transmission of infectious diseases. Consequently, the social network structure of populations plays a key role in shaping infectious disease dynamics. A huge research effort has examined how specific social network structures make populations more (or less) vulnerable to damaging epidemics. However, it can be just as important to understand how social networks can contribute to endemic disease dynamics, in which pathogens are maintained at stable levels for prolonged periods of time. Hosts that can maintain endemic disease may serve as keystone hosts for multi-host pathogens within an ecological community, and also have greater potential to act as key wildlife reservoirs of agricultural and zoonotic diseases. Here, we examine combinations of social and demographic processes that can foster endemic disease in hosts. We synthesise theoretical and empirical work to demonstrate the importance of both social structure and social dynamics in maintaining endemic disease. We also highlight the importance of distinguishing between the local and global persistence of infection and reveal how different social processes drive variation in the scale at which infectious diseases appear endemic. Our synthesis provides a framework by which to understand how sociality contributes to the long-term maintenance of infectious disease in wildlife hosts and provides a set of tools to unpick the social and demographic mechanisms involved in any given host-pathogen system. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00265-021-03055-8.

Spatial and temporal variation in proximity networks of commercial dairy cattle in Great Britain.

The nature of contacts between hosts can be important in facilitating or impeding the spread of pathogens within a population. Networks constructed from contacts between hosts allow examination of how individual variation might influence the spread of infections. Studying the contact networks of livestock species managed under different conditions can additionally provide insight into their influence on these contact structures. We collected high-resolution proximity and GPS location data from nine groups of domestic cattle (mean group size = 85) in seven dairy herds employing a range of grazing and housing regimes. Networks were constructed from cattle contacts (defined by proximity) aggregated by different temporal windows (2 h, 24 h, and approximately 1 week) and by location within the farm. Networks of contacts aggregated over the whole study were highly saturated but dividing contacts by space and time revealed substantial variation in cattle interactions. Cows showed statistically significant variation in the frequency of their contacts and in the number of cows with which they were in contact. When cows were in buildings, compared to being on pasture, contact durations were longer and cows contacted more other cows. A small number of cows showed evidence of consistent relationships but the majority of cattle did not. In one group where management allowed free access to all farm areas, cows showed asynchronous space use and, while at pasture, contacted fewer other cows and showed substantially greater between-individual variation in contacts than other groups. We highlight the degree to which variations in management (e.g. grazing access, milking routine) substantially alter cattle contact patterns, with potentially major implications for infection transmission and social interactions. In particular, where individual cows have free choice of their environment, the resulting contact networks may have a less-risky structure that could reduce the likelihood of direct transmission of infections.

Fungal microbiomes are determined by host phylogeny and exhibit widespread associations with the bacterial microbiome.

Interactions between hosts and their resident microbial communities are a fundamental component of fitness for both agents. Though recent research has highlighted the importance of interactions between animals and their bacterial communities, comparative evidence for fungi is lacking, especially in natural populations. Using data from 49 species, we present novel evidence of strong covariation between fungal and bacterial communities across the host phylogeny, indicative of recruitment by hosts for specific suites of microbes. Using co-occurrence networks, we demonstrate marked variation across host taxonomy in patterns of covariation between bacterial and fungal abundances. Host phylogeny drives differences in the overall richness of bacterial and fungal communities, but the effect of diet on richness was only evident in the mammalian gut microbiome. Sample type, tissue storage and DNA extraction method also affected bacterial and fungal community composition, and future studies would benefit from standardized approaches to sample processing. Collectively these data indicate fungal microbiomes may play a key role in host fitness and suggest an urgent need to study multiple agents of the animal microbiome to accurately determine the strength and ecological significance of host-microbe interactions.

A guide to choosing and implementing reference models for social network analysis.

Analysing social networks is challenging. Key features of relational data require the use of non-standard statistical methods such as developing system-specific null, or reference, models that randomize one or more components of the observed data. Here we review a variety of randomization procedures that generate reference models for social network analysis. Reference models provide an expectation for hypothesis testing when analysing network data. We outline the key stages in producing an effective reference model and detail four approaches for generating reference distributions: permutation, resampling, sampling from a distribution, and generative models. We highlight when each type of approach would be appropriate and note potential pitfalls for researchers to avoid. Throughout, we illustrate our points with examples from a simulated social system. Our aim is to provide social network researchers with a deeper understanding of analytical approaches to enhance their confidence when tailoring reference models to specific research questions.

Differentiated Social Relationships and the Pace-of-Life-History.

When selection is imposed by both social and ecological environments, the costs and benefits of social relationships can depend on life-history strategy. We argue that the formation and maintenance of differentiated social relationships will prevail in species and individuals with slow life histories. Social behaviours that benefit survival can promote slower life histories. Meanwhile, longer lifespan promotes the development of strong and stable social bonds by allowing fitness payoffs to be postponed. Differentiated social behaviours should be favoured for fast life histories only when they promote the rate of reproduction. Finally, associations between life-history strategies and other traits (e.g., personality) provide a mechanism to drive inter-individual variation in social relationships, making life-history important for sociality across taxonomic scales.

Common datastream permutations of animal social network data are not appropriate for hypothesis testing using regression models.

1. Social network methods have become a key tool for describing, modelling, and testing hypotheses about the social structures of animals. However, due to the non-independence of network data and the presence of confounds, specialized statistical techniques are often needed to test hypotheses in these networks. Datastream permutations, originally developed to test the null hypothesis of random social structure, have become a popular tool for testing a wide array of null hypotheses in animal social networks. In particular, they have been used to test whether exogenous factors are related to network structure by interfacing these permutations with regression models. 2. Here, we show that these datastream permutations typically do not represent the null hypothesis of interest to researchers interfacing animal social network analysis with regression modelling, and use simulations to demonstrate the potential pitfalls of using this methodology. 3. Our simulations show that, if used to indicate whether a relationship exists between network structure and a covariate, datastream permutations can result in extremely high type I error rates, in some cases approaching 50%. In the same set of simulations, traditional node-label permutations produced appropriate type I error rates (~ 5%). 4. Our analysis shows that datastream permutations do not represent the appropriate null hypothesis for these analyses. We suggest that potential alternatives to this procedure may be found in regarding the problems of non-independence of network data and unreliability of observations separately. If biases introduced during data collection can be corrected, either prior to model fitting or within the model itself, node-label permutations then serve as a useful test for interfacing animal social network analysis with regression modelling.