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

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)

Genetic origins of social networks in rhesus macaques

This is the final version of the article. Available from the publisher via the DOI in this record.Sociality is believed to have evolved as a strategy for animals to cope with their environments. Yet the genetic basis of sociality remains unclear. Here we provide evidence that social network tendencies are heritable in a gregarious primate. The tendency for rhesus macaques, Macaca mulatta, to be tied affiliatively to others via connections mediated by their social partners - analogous to friends of friends in people - demonstrated additive genetic variance. Affiliative tendencies were predicted by genetic variation at two loci involved in serotonergic signalling, although this result did not withstand correction for multiple tests. Aggressive tendencies were also heritable and were related to reproductive output, a fitness proxy. Our findings suggest that, like humans, the skills and temperaments that shape the formation of multi-agent relationships have a genetic basis in nonhuman primates, and, as such, begin to fill the gaps in our understanding of the genetic basis of sociality.We thank Bonn Aure, Jacqueline Buhl, Monica Carlson, Matthew McConnell, Elizabeth Maldonado, David Paulsen, Cecilia Penedo & the Caribbean Primate Research Center (CPRC) for assistance, and Roger Mundry for the use of PSAM software. The authors were supported by NIMH grant R01-MH089484, an Incubator Award from the Duke Institute for Brain Sciences, and a Duke Center for Interdisciplinary Decision Sciences Fellowship to LJNB. The CPRC is supported by grant 8-P40 OD012217-25 from the National Center for Research Resources (NCRR) and the Office of Research Infrastructure Programs (ORIP) of the National Institutes of Health

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

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

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

Common permutation methods in animal social network analysis do not control for non-independence

This is the final version. Available on open access from Springer via the DOI in this recordData availability: The R code required to repeat the simulations has been deposited at: https://doi.org/10.5281/zenodo.4903396).The non-independence of social network data is a cause for concern among behavioural ecologists conducting social network analysis. This has led to the adoption of several permutation-based methods for testing common hypotheses. One of the most common types of analysis is nodal regression, where the relationships between node-level network metrics and nodal covariates are analysed using a permutation technique known as node-label permutations. We show that, contrary to accepted wisdom, node-label permutations do not automatically account for the non-independences assumed to exist in network data, because regression-based permutation tests still assume exchangeability of residuals. The same assumption also applies to the quadratic assignment procedure (QAP), a permutation-based method often used for conducting dyadic regression. We highlight that node-label permutations produce the same p-values as equivalent parametric regression models, but that in the presence of non-independence, parametric regression models can also produce accurate effect size estimates. We also note that QAP only controls for a specific type of non-independence between edges that are connected to the same nodes, and that appropriate parametric regression models are also able to account for this type of non-independence. Based on this, we suggest that standard parametric models could be used in the place of permutation-based methods. Moving away from permutation-based methods could have several benefits, including reducing over-reliance on p-values, generating more reliable effect size estimates, and facilitating the adoption of causal inference methods and alternative types of statistical analysis.Engineering and Physical Sciences Research Council (EPSRC)European Research Council (ERC)National Institutes of Health (NIH)Natural Environment Research Council (NERC