Social inheritance of avoidances shapes the structure of animal social networks.

Social structure can have significant effects on selection, affecting both individual fitness traits and population-level processes. As such, research into its dynamics and evolution has spiked in the last decade, where theoretical and computational advances in social network analysis have increased our understanding of its ecological and inheritance underpinnings. Yet, the processes that shape the formation of structure within social networks are poorly understood and the role of social avoidances unknown. Social avoidances are an alternate of social affiliation in animal societies, which, although invisible, likely play a role in shaping animal social networks. Assuming social avoidances evolve under similar constraints as affiliative behavior, we extended a previous model of social inheritance of affiliations to investigate the impact of social inheritance of avoidances on social network structure. We modeled avoidances as relationships that individuals can copy from their mothers or from their mother's social environment and varied the degrees to which individuals inherit social affiliates and avoidances to test their combined influence on social network structure. We found that inheriting avoidances via maternal social environments made social networks less dense and more modular, thereby demonstrating how social avoidance can shape the evolution of animal social networks.

The interaction between cortisol and testosterone predicts leadership within rock hyrax social groups.

Group movement leadership is associated with higher risks for those in the front. Leaders are the first to explore new areas and may be exposed to predation. Individual differences in risk-taking behavior may be related to hormonal differences. In challenging circumstances, such as risk-taking leadership that may pose a cost to the leader, cortisol is secreted both to increase the likelihood of survival by restoring homeostasis, and to mediate cooperative behavior. Testosterone too has a well-established role in risk-taking behavior, and the dual-hormone hypothesis posits that the interaction of testosterone and cortisol can predict social behavior. Based on the dual-hormone hypothesis, we investigated here whether the interaction between testosterone and cortisol can predict risk-taking leadership behavior in wild rock hyraxes (Procavia capensis). We used proximity loggers, observations, and playback trials to characterize hyrax leaders in three different leadership contexts that varied in their risk levels. In support of the dual-hormone hypothesis, we found that cortisol and testosterone interactions predict leadership that involves risk. Across different circumstances that involved low or high levels of risk, testosterone was positively related to leadership, but only in individuals (both males and females) with low levels of cortisol. We also found an interaction between these hormone levels and age at the low-risk scenarios. We suggest that the close social interactions and affiliative behavior among hyrax females within small egalitarian groups may make female leadership less risky, and therefore less stressful, and allow female leaders to influence group activities.

Male rock hyraxes that maintain an isochronous song rhythm achieve higher reproductive success.

Rhythmic stability (nonrandom temporal structure) is required for many neural and physiological functions, whereas rhythmic irregularities can indicate genetic or developmental deficiencies. Therefore, rhythmic courtship or contest signals are widespread in nature as honest advertisement displays. Examination of bird songs revealed the pervasiveness of categorical rhythmic patterns that can be described as small integer ratios between sequential inter-call intervals. As similar rhythmic profiles are prevalent in human music, it was suggested that a shared functionality could drive both animal songs and human musical rhythms, facilitating synchrony between signallers and enabling easy identification of performance errors. Here we examined whether the rhythmic structure and the rhythmic stability of vocal displays are related to reproductive success in male rock hyraxes (Procavia capensis), which presents an unusual case of a terrestrial singing mammal. We combined long-term parentage analysis of 13 male hyraxes (22 male/years) with an analysis of an audio library of 105 hyrax songs. Male annual reproductive success was determined by the number of offspring that survived to the age of 1 year. The frequency of singing events was used to determine the seasonal singing effort for each male. Songs were analysed for rhythmic structure, focusing on the presence of categorical rhythms and the contribution of rhythmic stability to annual reproductive success. We found that male hyraxes that sing more frequently tend to have more surviving offspring and that the rhythmic profile of hyrax songs is predominantly isochronous with sequential vocal element pairs nearly equally spaced. The ratio of isochronous vocal element transitions (on-integer) to element transitions that deviate from an isochronous pattern (off-integer) in hyrax songs is positively correlated with male reproductive success. Our findings support the notion that isochronous rhythmic stability can serve as an indication of quality in sexually selected signals and is not necessarily driven by the need for multiple caller synchronization. The relative scarcity of nonisochronous rhythmic categories in individually performed hyrax songs raises the question of whether such rhythmic categories could be a product of collective, coordinated signalling, while being selected against in individual performance.

High-resolution tracking of hyrax social interactions highlights nighttime drivers of animal sociality.

Network structure is a key driver of animal fitness, pathogen transmission, information spread, and population demographics in the wild. Although a considerable body of research applied network analysis to animal societies, only little effort has been devoted to separate daytime and nighttime sociality and explicitly test working hypotheses on social structures emerging at night. Here, we investigated the nighttime sociality of a wild population of rock hyraxes (Procavia capensis) and its relation to daytime social structure. We recorded nearly 15,000 encounters over 27 consecutive days and nights using proximity loggers. Overall, we show that hyraxes are more selective of their social affiliates at night compared to daytime. We also show that hyraxes maintain their overall network topology while reallocating the weights of social relationships at the daily and monthly scales, which could help hyraxes maintain their social structure over long periods while adapting to local constraints and generate complex social dynamics. These results suggest that complex network dynamics can be a by-product of simple daily social tactics and do not require high cognitive abilities. Our work sheds light on the function of nighttime social interactions in diurnal social species.

Protocol to record multiple interaction types in small social groups of birds.

Here, we present a protocol for collecting data on multiple interaction types in small, stable groups of Arabian babblers (Argya squamiceps). We describe the procedure of habituation, the recording of social interactions, and how to classify the interaction types. Additionally, we provide code for testing, comparing, and visualizing data. The high-resolution data collection is time demanding and requires several data tests before forming the final protocol. The collected data can then be used for multiplex social network analysis. For complete details on the use and execution of this protocol, please refer to Dragic et al. (2021).

Maladaptive evolution or how a beneficial mutation may get lost due to nepotism.

Spotted hyenas are an exception in the animal kingdom not only due to female dominance over males, but also because of the strict female linear hierarchy which determines priority of access to resources and produces considerable female reproductive skew. This special social system raises a question: what would become of a beneficial mutation if it occurred in a low-ranking female? We used several simulation models in order to address this question. Our modeling results indicate that such a social system may inhibit the establishment of a beneficial mutation. However, this negative effect may be counteracted by random choice of mates by females.

Sex-associated and context-dependent leadership in the rock hyrax.

In many mammalian species, both sexes may take leadership role, but different traits may play a role in determining variation within species. Here we examine the effect of sex on leadership. We present three complementary datasets derived from a well-studied population of wild rock hyrax (Procavia capensis). The findings demonstrated that male and female rock hyraxes take on different leadership positions, depending on the context. When risk is moderate, more likely to lead are younger resident males, which experience high cortisol and lower testosterone levels. However, during acute predation scenarios, more likely to lead are males with lower centrality status. We suggest that hyrax males exhibit risky behaviors that may reflect their need for self-advertisement. In contrast, leadership among group females is more equally distributed. Females have little to gain from risky actions due to the lack of competition among them, but nonetheless take leadership positions.

Multilayer social networks reveal the social complexity of a cooperatively breeding bird.

The social environment of individuals affects various evolutionary and ecological processes. Their social environment is affected by individual and environmental traits. We assessed the effects of these traits on nodes and dyads in six layers of networks of Arabian babblers, representing different interaction types. Additionally, we tested how traits affect social niches in the multilayer networks using the t-distributed stochastic neighbor embedding (tSNE) dimensionality reduction algorithm. The effect of group size and season was similar across network layers, but individual traits had different effects on different layers. Additionally, we documented assortativity with respect to individual traits in the dominance display and allopreening networks. The joint analysis of all six layers revealed that most traits did not affect individuals' social niches. However, older individuals occupied fewer social niches than younger ones. Our results suggest that multilayer social networks are an important tool for understanding the complex social systems of cooperative breeders and intragroup interactions.

Rank-dependent social inheritance determines social network structure in spotted hyenas.

The structure of animal social networks influences survival and reproductive success, as well as pathogen and information transmission. However, the general mechanisms determining social structure remain unclear. Using data from 73,767 social interactions among wild spotted hyenas collected over 27 years, we show that the process of social inheritance determines how offspring relationships are formed and maintained. Relationships between offspring and other hyenas bear resemblance to those of their mothers for as long as 6 years, and the degree of similarity increases with maternal social rank. Mother-offspring relationship strength affects social inheritance and is positively correlated with offspring longevity. These results support the hypothesis that social inheritance of relationships can structure animal social networks and be subject to adaptive tradeoffs.

Early Life Experience Shapes Male Behavior and Social Networks in Drosophila.

Living in a group creates a complex and dynamic environment in which behavior of individuals is influenced by and affects the behavior of others. Although social interaction and group living are fundamental adaptations exhibited by many organisms, little is known about how prior social experience, internal states, and group composition shape behavior in groups. Here, we present an analytical framework for studying the interplay between social experience and group interaction in Drosophila melanogaster. We simplified the complexity of interactions in a group using a series of experiments in which we controlled the social experience and motivational states of individuals to compare behavioral patterns and social networks of groups under different conditions. We show that social enrichment promotes the formation of distinct group structure that is characterized by high network modularity, high inter-individual and inter-group variance, high inter-individual coordination, and stable social clusters. Using environmental and genetic manipulations, we show that visual cues and cVA-sensing neurons are necessary for the expression of social interaction and network structure in groups. Finally, we explored the formation of group behavior and structure in heterogenous groups composed of flies with distinct internal states and documented emergent structures that are beyond the sum of the individuals that constitute it. Our results demonstrate that fruit flies exhibit complex and dynamic social structures that are modulated by the experience and composition of different individuals within the group. This paves the path for using simple model organisms to dissect the neurobiology of behavior in complex social environments.

The "Law of Brevity" in animal communication: Sex-specific signaling optimization is determined by call amplitude rather than duration.

The efficiency of informational transfer is one of the key aspects of any communication system. The informational coding economy of human languages is often demonstrated by their almost universal fit to Zipf's "Law of Brevity," expressing negative relationship between word length and its usage frequency. Animal vocal systems, however, provided mixed results in their adherence to this relationship, potentially due to conflicting evolutionary pressures related to differences in signaling range and communicational needs. To examine this potential parallel between human and animal vocal communication, and also to explore how divergent, sex-specific, communicational settings affect signaling efficiency within a species, we examined the complete vocal repertoire of rock hyraxes (Procavia capensis). As male and female hyraxes differ in their sociality levels and male hyraxes vocal repertoire is dominated by sexual advertisement songs, we hypothesized that sex-specific vocal repertoires could be subjected to different signaling optimization pressures. Our results show that the sexes differ in repertoire size, call usage, and adherence to coding efficiency principles. Interestingly, the classic call length/call usage relationship is not consistently found in rock hyraxes. Rather, a negative relationship between call amplitude and call usage is found, suggesting that the efficiency of the vocal repertoire is driven by call amplitude rather than duration. We hypothesize that, in contrast to human speech that is mainly intended for short distance, the need for frequent long-range signaling shapes an animal's vocal repertoire efficiency according to the cost of call amplitude rather than call length. However, call duration may be a secondary factor affecting signaling efficiency, in cases where amplitude is under specific selection pressures, such as sexual selection.

Social context mediates testosterone's effect on snort acoustics in male hyrax songs.

Testosterone affects physical and motivational states, both of which may strongly influence vocalization structure and acoustics. The loud complex calls (i.e., songs) of male rock hyraxes (Procavia capensis) are used as honest signals for advertising physical and social states. The snort, a low frequency, noisy element of the song, encodes information on the singer's age and social rank via harshness, as measured by jitter (i.e., acoustic frequency stability) and duration; suggesting that the snort concomitantly advertises both vocal stability and aggression. Our past findings revealed that testosterone levels are related to both vocal elements and social status of male hyraxes, suggesting that hormonal mechanisms mediate the motivation for aggressive and courtship behaviors. Here we examined whether long-term androgen levels are related to snort acoustics and song structure by comparing levels of testosterone in hair with acoustic and structural parameters. We found that songs performed by individuals with higher testosterone levels include more singing bouts and longer, smoother snorts, but only in those songs induced by external triggers. It is possible that hyraxes with higher levels of testosterone possess the ability to perform higher-quality singing, but only invest in situations of high social arousal and potential benefit. Surprisingly, in spontaneous songs, hyraxes with high testosterone were found to snort more harshly than low-testosterone males. The context dependent effects of high testosterone on snort acoustics suggest that the aggressive emotional arousal associated with testosterone is naturally reflected in the jittery hyrax snort, but that it can be masked by high-quality performance.

The progression pattern of male hyrax songs and the role of climactic ending.

The study of animal vocal signals can either focus on the properties of distinct vocal elements or address the signal as a whole. Although some attention has been given to the continuous progression patterns of bird songs, such patterns in mammalian vocalisations have been largely overlooked. We examined temporal changes in structural and acoustic parameters in male rock hyrax songs. We found a gradual increase in call frequency and amplitude towards the song ending, as well as an abrupt increase in bout syntactic complexity, peaking in the last quintile of a song. In musical terms, such a pattern can be described as a crescendo (amplitude increase) with a terminal climax. In Western music, crescendos are used to maintain attention and direct the listeners towards a memorable highpoint of the musical piece. This structure may have an analogous function in animal communication, recruiting audience attention towards the climactic and potentially most informative part of the signal. Our playback experiments revealed that hyrax males tend to reply more to songs with a climactic ending, indicating that this progression pattern is important for hyrax communication. We suggest that animal vocal communication research can benefit from adding musical concepts to the analysis toolbox.

Analysing animal social network dynamics: the potential of stochastic actor-oriented models.

Animals are embedded in dynamically changing networks of relationships with conspecifics. These dynamic networks are fundamental aspects of their environment, creating selection on behaviours and other traits. However, most social network-based approaches in ecology are constrained to considering networks as static, despite several calls for such analyses to become more dynamic. There are a number of statistical analyses developed in the social sciences that are increasingly being applied to animal networks, of which stochastic actor-oriented models (SAOMs) are a principal example. SAOMs are a class of individual-based models designed to model transitions in networks between discrete time points, as influenced by network structure and covariates. It is not clear, however, how useful such techniques are to ecologists, and whether they are suited to animal social networks. We review the recent applications of SAOMs to animal networks, outlining findings and assessing the strengths and weaknesses of SAOMs when applied to animal rather than human networks. We go on to highlight the types of ecological and evolutionary processes that SAOMs can be used to study. SAOMs can include effects and covariates for individuals, dyads and populations, which can be constant or variable. This allows for the examination of a wide range of questions of interest to ecologists. However, high-resolution data are required, meaning SAOMs will not be useable in all study systems. It remains unclear how robust SAOMs are to missing data and uncertainty around social relationships. Ultimately, we encourage the careful application of SAOMs in appropriate systems, with dynamic network analyses likely to prove highly informative. Researchers can then extend the basic method to tackle a range of existing questions in ecology and explore novel lines of questioning.

Personality and Social Networks: A Generative Model Approach.

Social network analysis has produced important insights regarding the causes and consequences of animal social structure. Social structure has been shown to impact longevity, reproductive success, transmission of pathogens and information, and also play important role in the evolution of cooperation. Studies of the determinants of social structure have identified environmental, genetic, and structural factors in a variety of species. At the same time, most studies in the field have been descriptive in approach, statistically identifying patterns in social networks constructed from observed interactions. We argue that there is a need for predictive theory to complement descriptive studies, moving the field from pattern to process. As an example, we provide a simple model of the effect of personality on social network structure and social role differentiation. Our model suggests that variation in behavioral types can result in variation in individual social network traits, and that some patterns found in animal networks in the wild, such as assortativity with respect to personality, may be outcomes of social inheritance and individual variation in it. Our approach and results exemplify the potential of generative models to connect individual-level processes to emergent patterns and advance our understanding of social complexity in nature.

Social inheritance can explain the structure of animal social networks.

The social network structure of animal populations has major implications for survival, reproductive success, sexual selection and pathogen transmission of individuals. But as of yet, no general theory of social network structure exists that can explain the diversity of social networks observed in nature, and serve as a null model for detecting species and population-specific factors. Here we propose a simple and generally applicable model of social network structure. We consider the emergence of network structure as a result of social inheritance, in which newborns are likely to bond with maternal contacts, and via forming bonds randomly. We compare model output with data from several species, showing that it can generate networks with properties such as those observed in real social systems. Our model demonstrates that important observed properties of social networks, including heritability of network position or assortative associations, can be understood as consequences of social inheritance.

Acoustic sequences in non-human animals: a tutorial review and prospectus.

Animal acoustic communication often takes the form of complex sequences, made up of multiple distinct acoustic units. Apart from the well-known example of birdsong, other animals such as insects, amphibians, and mammals (including bats, rodents, primates, and cetaceans) also generate complex acoustic sequences. Occasionally, such as with birdsong, the adaptive role of these sequences seems clear (e.g. mate attraction and territorial defence). More often however, researchers have only begun to characterise - let alone understand - the significance and meaning of acoustic sequences. Hypotheses abound, but there is little agreement as to how sequences should be defined and analysed. Our review aims to outline suitable methods for testing these hypotheses, and to describe the major limitations to our current and near-future knowledge on questions of acoustic sequences. This review and prospectus is the result of a collaborative effort between 43 scientists from the fields of animal behaviour, ecology and evolution, signal processing, machine learning, quantitative linguistics, and information theory, who gathered for a 2013 workshop entitled, 'Analysing vocal sequences in animals'. Our goal is to present not just a review of the state of the art, but to propose a methodological framework that summarises what we suggest are the best practices for research in this field, across taxa and across disciplines. We also provide a tutorial-style introduction to some of the most promising algorithmic approaches for analysing sequences. We divide our review into three sections: identifying the distinct units of an acoustic sequence, describing the different ways that information can be contained within a sequence, and analysing the structure of that sequence. Each of these sections is further subdivided to address the key questions and approaches in that area. We propose a uniform, systematic, and comprehensive approach to studying sequences, with the goal of clarifying research terms used in different fields, and facilitating collaboration and comparative studies. Allowing greater interdisciplinary collaboration will facilitate the investigation of many important questions in the evolution of communication and sociality.

Spatial-Temporal Dynamics of High-Resolution Animal Networks: What Can We Learn from Domestic Animals?

Animal social network is the key to understand many ecological and epidemiological processes. We used real-time location system (RTLS) to accurately track cattle position, analyze their proximity networks, and tested the hypothesis of temporal stationarity and spatial homogeneity in these networks during different daily time periods and in different areas of the pen. The network structure was analyzed using global network characteristics (network density), subgroup clustering (modularity), triadic property (transitivity), and dyadic interactions (correlation coefficient from a quadratic assignment procedure) at hourly level. We demonstrated substantial spatial-temporal heterogeneity in these networks and potential link between indirect animal-environment contact and direct animal-animal contact. But such heterogeneity diminished if data were collected at lower spatial (aggregated at entire pen level) or temporal (aggregated at daily level) resolution. The network structure (described by the characteristics such as density, modularity, transitivity, etc.) also changed substantially at different time and locations. There were certain time (feeding) and location (hay) that the proximity network structures were more consistent based on the dyadic interaction analysis. These results reveal new insights for animal network structure and spatial-temporal dynamics, provide more accurate descriptions of animal social networks, and allow more accurate modeling of multiple (both direct and indirect) disease transmission pathways.

Topological effects of network structure on long-term social network dynamics in a wild mammal.

Social structure influences ecological processes such as dispersal and invasion, and affects survival and reproductive success. Recent studies have used static snapshots of social networks, thus neglecting their temporal dynamics, and focused primarily on a limited number of variables that might be affecting social structure. Here, instead we modelled effects of multiple predictors of social network dynamics in the spotted hyena, using observational data collected during 20 years of continuous field research in Kenya. We tested the hypothesis that the current state of the social network affects its long-term dynamics. We employed stochastic agent-based models that allowed us to estimate the contribution of multiple factors to network changes. After controlling for environmental and individual effects, we found that network density and individual centrality affected network dynamics, but that social bond transitivity consistently had the strongest effects. Our results emphasise the significance of structural properties of networks in shaping social dynamics.