Friends of friends: Are indirect connections in social networks important to animal behaviour?

types: ArticleCopyright © 2015 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.Please cite this article in press as: Brent, L. J. N., Friends of friends: are indirect connections in social networks important to animal behaviour?, Animal Behaviour (2015), http://dx.doi.org/10.1016/j.anbehav.2015.01.020Friend of a friend relationships, or the indirect connections between people, influence our health, well-being, financial success and reproductive output. As with humans, social behaviours in other animals often occur within a broad interconnected network of social ties. Yet studies of animal social behaviour tend to focus on associations between pairs of individuals. With the increase in popularity of social network analysis, researchers have started to look beyond the dyad to examine the role of indirect connections in animal societies. Here, I provide an overview of the new knowledge that has been uncovered by these studies. I focus on research that has addressed both the causes of social behaviours, i.e. the cognitive and genetic basis of indirect connections, as well as their consequences, i.e. the impact of indirect connections on social cohesion, information transfer, cultural practices and fitness. From these studies, it is apparent that indirect connections play an important role in animal behaviour, although future research is needed to clarify their contribution.NERCNational Institutes of Mental Healt

Indirectly connected: simple social differences can explain the causes and apparent consequences of complex social network positions

This is the author accepted manuscript. The final version is available from Royal Society via the DOI in this record.Animal societies are often structurally complex. How individuals are positioned within the wider social network (i.e. their indirect social connections) has been shown to be repeatable, heritable and related to key life-history variables. Yet, there remains a general lack of understanding surrounding how complex network positions arise, whether they indicate active multifaceted social decisions by individuals, and how natural selection could act on this variation. We use simulations to assess how variation in simple social association rules between individuals can determine their positions within emerging social networks. Our results show that metrics of individuals' indirect connections can be more strongly related to underlying simple social differences than metrics of their dyadic connections. External influences causing network noise (typical of animal social networks) generally inflated these differences. The findings demonstrate that relationships between complex network positions and other behaviours or fitness components do not provide sufficient evidence for the presence, or importance, of complex social behaviours, even if direct network metrics provide less explanatory power than indirect ones. Interestingly however, a plausible and straightforward heritable basis for complex network positions can arise from simple social differences, which in turn creates potential for selection to act on indirect connections.The work was funded by a Research Fellowship from the EGI and a Junior Research Fellowship from Merton College, Oxford University to J.A.F., a BBSRC grant (BB/L006081/1) to B.C.S., and a Leverhulme Trust Early Career Fellowship to L.J.N.B

Persistent social isolation reflects identity and social context but not maternal effects or early environment

This is the final version of the article. Available from Springer Nature via the DOI in this record.Individuals who are well integrated into society have greater access to resources and tend to live longer. Why some individuals are socially isolated and others are not is therefore puzzling from an evolutionary perspective. Answering this question requires establishing the mix of intrinsic and contextual factors that contribute to social isolation. Using social network data spanning up to half of the median adult lifespan in a gregarious primate, we found that some measures of social isolation were modestly repeatable within individuals, consistent with a trait. By contrast, social isolation was not explained by the identity of an animal’s mother or the group into which it was born. Nevertheless, age, sex and social status each played a role, as did kin dynamics and familiarity. Females with fewer close relatives were more isolated, and the more time males spent in a new group the less isolated they became, independent of their social status. These results show that social isolation results from a combination of intrinsic and environmental factors. From an evolutionary perspective, these findings suggest that social isolation could be adaptive in some contexts and partly maintained by selection.This work was supported by National Institute of Mental Health grants R01-MH089484 and R01-MH096875, and an Incubator Award from the Duke Institute for Brain Sciences. L.J.N.B. was supported by an Early Career Fellowship from the Leverhulme Trust. Data provided by the University of Puerto Rico, and its facilities, are funded by grant number 2 P40 OD012217 from the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health (NIH)

Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate

This is the final version. Available on open access from Nature Research via the DOI in this recordData availability: The datasets generated during and/or analyzed during the current study are available at https://doi.org/10.6084/m9.figshare.11343971Sexual selection favours traits that increase reproductive success via increased competitive ability, attractiveness, or both. Male rhesus macaque (Macaca mulatta) morphological traits are likely to reflect the effects of multiple sexual selection pressures. Here, we use a quantitative genetic approach to investigate the production and maintenance of variation in male rhesus macaque morphometric traits which may be subject to sexual selection. We collected measurements of body size, canine length, and fat, from 125 male and 21 female free-ranging rhesus macaques on Cayo Santiago. We also collected testis volumes from males. We used a genetic pedigree to calculate trait heritability, to investigate potential trait trade-offs, and to estimate selection gradients. We found that variation in most male morphometric traits was heritable, but found no evidence of trait trade-offs nor that traits predicted reproductive success. Our results suggest that male rhesus macaque morphometric traits are either not under selection, or are under mechanisms of sexual selection that we could not test (e.g. balancing selection). In species subject to complex interacting mechanisms of selection, measures of body size, weaponry, and testis volume may not increase reproductive success via easily-testable mechanisms such as linear directional selection.New York University (NYU)National Institute of Mental HealthLeakey Foundatio

Social dominance and cooperation in female vampire bats

This is the final version. Available on open access from the Royal Society via the DOI in this recordData accessibility: All data and R code can be found on Figshare: https://doi.org/10.6084/m9.figshare.14043794.v1When group-living animals develop individualized social relationships, they often regulate cooperation and conflict through a dominance hierarchy. Female common vampire bats have been an experimental system for studying cooperative relationships, yet surprisingly little is known about female conflict. Here, we recorded the outcomes of 1023 competitive interactions over food provided ad libitum in a captive colony of 33 vampire bats (24 adult females and their young). We found a weakly linear dominance hierarchy using three common metrics (Landau's h’ measure of linearity, triangle transitivity and directional consistency). However, patterns of female dominance were less structured than in many other group-living mammals. Female social rank was not clearly predicted by body size, age, nor reproductive status, and competitive interactions were not correlated with kinship, grooming nor food sharing. We therefore found no evidence that females groomed or shared food up a hierarchy or that differences in rank explained asymmetries in grooming or food sharing. A possible explanation for such apparently egalitarian relationships among female vampire bats is the scale of competition. Female vampire bats that are frequent roostmates might not often directly compete for food in the wild.Smithsonian Tropical Research Institute (STRI)National Science Foundation (NSF

Reduced older male presence linked to increased rates of aggression to non-conspecific targets in male elephants

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this recordMales in many large mammal species spend a considerable portion of their lives in all-male groups segregated from females. In long-lived species, these all-male groups may contain individuals of vastly different ages, providing the possibility that behaviours such as aggression vary with the age demographic of the social environment, as well as an individual’s own age. Here, we explore social factors affecting aggression and fear behaviours in non-musth male African elephants (Loxodonta africana) aggregating in an all-male area. Adolescent males had greater probabilities of directing aggressive and fearful behaviours to non-elephant targets when alone compared to when with other males. All males, regardless of age, were less aggressive toward non-elephant targets, e.g., vehicles and non-elephant animals, when larger numbers of males from the oldest age cohort were present. Presence of older males did not influence the probability that other males were aggressive to conspecifics or expressed fearful behaviours toward non-elephant targets. Older bulls may police aggression directed toward non-elephant targets, or may lower elephants’ perception of their current threat level. Our results suggest male elephants may pose an enhanced threat to humans and livestock when adolescents are socially isolated, and when fewer older bulls are nearby.Leverhulme TrustExplorers ClubWilderness Wildlife TrustElephants for AfricaIDEAWIL

Social network dynamics precede a mass eviction in group-living rhesus macaques

This is the author accepted manuscript. The final version is available from Elsevier Masson via the DOI in this record.Network dynamics can reveal information about the adaptive function of social behaviour and the extent to which social relationships can flexibly respond to extrinsic pressures. Changes in social networks occur following changes to the social and physical environment. By contrast, we have limited understanding of whether changes in social networks precede major group events. Permanent evictions can be important determinants of gene flow and population structure and are a clear example of an event that might be preceded by social network dynamics. Here we examined the social networks of a group of rhesus macaques, Macaca mulatta, in the 2 years leading up to the eviction of 22% of adult females, which are the philopatric sex. We found that females engaged in the same amount of aggression and grooming in the 2 years leading up to the eviction but that there were clear changes in their choice of social partners. Females that would eventually be evicted received more aggression from lower-ranking females as the eviction approached. Evicted females also became more discriminating in their grooming relationships in the year nearer the split, showing a greater preference for one another and becoming more cliquish. Put simply, the females that would later be evicted continued to travel with the rest of the group as the eviction approached but were less likely to interact with other group members in an affiliative manner. These results have potential implications for understanding group cohesion and the balance between cooperation and competition that mediates social groups.We were supported by National Institute of Mental Health grants R01-MH089484 and R01-MH096875, and an Incubator Award from the Duke Institute for Brain Sciences. L.J.N.B. was supported by a Duke Center for Interdisciplinary Decision Sciences Fellowship and by an Early Career Fellowship from the Leverhulme Trust. The CPRC is funded by grant number 2 P40 OD012217 from the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health (NIH)

Using Machine Learning to Discover Latent Social Phenotypes in Free-Ranging Macaques

This is the final version of the article. Available from MDPI via the DOI in this record.Investigating the biological bases of social phenotypes is challenging because social behavior is both high-dimensional and richly structured, and biological factors are more likely to influence complex patterns of behavior rather than any single behavior in isolation. The space of all possible patterns of interactions among behaviors is too large to investigate using conventional statistical methods. In order to quantitatively define social phenotypes from natural behavior, we developed a machine learning model to identify and measure patterns of behavior in naturalistic observational data, as well as their relationships to biological, environmental, and demographic sources of variation. We applied this model to extensive observations of natural behavior in free-ranging rhesus macaques, and identified behavioral states that appeared to capture periods of social isolation, competition over food, conflicts among groups, and affiliative coexistence. Phenotypes, represented as the rate of being in each state for a particular animal, were strongly and broadly influenced by dominance rank, sex, and social group membership. We also identified two states for which variation in rates had a substantial genetic component. We discuss how this model can be extended to identify the contributions to social phenotypes of particular genetic pathways.The authors would like to thank John Pearson, Sam Larson, Ashley Walker, Joel Glick, Josue Negron, and the CPRC staff for their feedback and research support. This research supported by NIH grant 5R01-MH096875-02. The CPRC is supported by grant 8-P40 OD012217-25 from the National Center for Research Resources and the Office of Research Infrastructure Programs of the National Institutes of Health

Kinship composition in mammals

This is the final version. Available from the Royal Society via the DOI in this record. Data accessibility: The data, metadata and code are provided in the main text and the electronic supplementary materialUnderstanding the evolution of group-living and cooperation requires information on who animals live and cooperate with. Animals can live with kin, non-kin or both, and kinship structure can influence the benefits and costs of group-living and the evolution of within-group cooperation. One aspect of kinship structure is kinship composition, i.e. a group-level attribute of the presence of kin and/or non-kin dyads in groups. Despite its putative importance, the kinship composition of mammalian groups has yet to be characterized. Here, we use the published literature to build an initial kinship composition dataset in mammals, laying the groundwork for future work in the field. In roughly half of the 18 species in our sample, individuals lived solely with same-sex kin, and, in the other half, individuals lived with related and unrelated individuals of the same sex. These initial results suggest that it is not rare for social mammals to live with unrelated individuals of the same sex, highlighting the importance of considering indirect and direct fitness benefits as co-drivers of the evolution of sociality. We hope that our initial dataset and insights will spur the study of kinship structure and sociality towards new exciting avenues.European CommissionRepública Portuguesa/ Ministério Ciência, Tecnologia e Ensino Superio

Social ageing: exploring the drivers of late-life changes in social behaviour in mammals

This is the final version. Available from The Royal Society via the DOI in this record. No datasets were generated or analysed during the current study.Social interactions help group-living organisms cope with socio-environmental challenges and are central to survival and reproductive success. Recent research has shown that social behaviour and relationships can change across the lifespan, a phenomenon referred to as 'social ageing'. Given the importance of social integration for health and well-being, age-dependent changes in social behaviour can modulate how fitness changes with age and may be an important source of unexplained variation in individual patterns of senescence. However, integrating social behaviour into ageing research requires a deeper understanding of the causes and consequences of age-based changes in social behaviour. Here, we provide an overview of the drivers of late-life changes in sociality. We suggest that explanations for social ageing can be categorized into three groups: changes in sociality that (a) occur as a result of senescence; (b) result from adaptations to ameliorate the negative effects of senescence; and/or (c) result from positive effects of age and demographic changes. Quantifying the relative contribution of these processes to late-life changes in sociality will allow us to move towards a more holistic understanding of how and why these patterns emerge and will provide important insights into the potential for social ageing to delay or accelerate other patterns of senescence.National Institute of HealthNational Institute of Healt