Krishna N. Balasubramaniam

Hierarchical steepness and phylogenetic models: phylogenetic signals in Macaca

Phylogenetic models of primate social behaviour posit that core social traits are inherent species characteristics that depend largely on phylogenetic histories of species rather than on adaptation to current socioecological conditions. These models predict that aspects of social structure will vary more between species than within species and that they will display strong phylogenetic signals. We tested these predictions in macaques focusing on dominance gradients, a relatively little studied, yet central, aspect of social structure. We used data from 14 social groups representing nine macaque species living in a variety of conditions. We examined proportions of counteraggression and two recently developed measures of dominance gradients (hierarchical steepness) for phylogenetic signals in nine phylogenetic trees constructed using (1) available genetic data sets and (2) Bayesian Markov Chain Monte Carlo (MCMC) and maximum likelihood algorithms. Hierarchical steepness and counteraggression showed significant variation between species but inconsistent variation within species. Both steepness and counteraggression showed evidence of phylogenetic signals, with results being particularly strong for one steepness measure and for counteraggression. Our results suggest that between-species variation in some core aspects of social structure are shaped by species’ evolutionary relationships, despite differences in living conditions. As such, they provide broad support for the phylogenetic model.

Hierarchical Steepness, Counter-Aggression, and Macaque Social Style Scale

Nonhuman primates show remarkable variation in several aspects of social structure. One way to characterize this variation in the genus Macaca is through the concept of social style, which is based on the observation that several social traits appear to covary with one another in a linear or at least continuous manner. In practice, macaques are more simply characterized as fitting a four‐grade scale in which species range from extremely despotic (grade 1) to extremely tolerant (grade 4). Here, we examine the fit of three core measures of social style—two measures of dominance gradients (hierarchical steepness) and another closely related measure (counter‐aggression)—to this scale, controlling for phylogenetic relationships. Although raw scores for both steepness and counter‐aggression correlated with social scale in predicted directions, the distributions appeared to vary by measure. Counter‐aggression appeared to vary dichotomously with scale, with grade 4 species being distinct from all other grades. Steepness measures appeared more continuous. Species in grades 1 and 4 were distinct from one another on all measures, but those in the intermediate grades varied inconsistently. This confirms previous indications that covariation is more readily observable when comparing species at the extreme ends of the scale than those in intermediate positions. When behavioral measures were mapped onto phylogenetic trees, independent contrasts showed no significant consistent directional changes at nodes below which there were evolutionary changes in scale. Further, contrasts were no greater at these nodes than at neutral nodes. This suggests that correlations with the scale can be attributed largely to species’ phylogenetic relationships. This could be due in turn to a structural linkage of social traits based on adaptation to similar ecological conditions in the distant past, or simply to unlinked phylogenetic closeness. Am. J. Primatol. 74:915‐925, 2012.

Using Biological Markets Principles to Examine Patterns of Grooming Exchange in Macaca thibetana

Biological markets principles offer testable hypotheses to explain variation in grooming exchange patterns among nonhuman primates. They predict that when within‐group contest competition (WGC) is high and dominance hierarchies steep, grooming interchange with other “commodity” behaviors (such as agonistic support) should prevail. In contrast, when WGC is low and gradients shallow, market theory predicts that grooming reciprocity should prevail. We tested these predictions in a wild, provisioned Tibetan macaque (Macaca thibetana) group across six time periods during which the group had been subjected to varying degrees of range restriction. Data on female–female aggression, grooming, and support were collected using all‐occurrences and focal animal sampling techniques, and analyzed using ANCOVA methods and correlation analyses. We found that hierarchical steepness varied significantly across periods, but did not correlate with two indirect indicators of WGC (group size and range restriction) in predicted directions. Contrary to expectations, we found a negative correlation between steepness and group size, perhaps because the responses of group members to external risks (i.e. prolonged and unavoidable exposure to humans) may have overshadowed the effects of WGC. As predicted, grooming reciprocity was significant in each period and negatively correlated with steepness, even after we controlled group size, kinship, rank differences, and proximity. In contrast, there was no evidence for grooming interchange with agonistic support or for a positive relationship between interchange and steepness. We hypothesize that stressful conditions and/or the presence of stable hierarchies during each period may have led to a greater market demand for grooming than support. We suggest that future studies testing these predictions consider more direct measures of WGC and commodities in addition to support, such as feeding tolerance and access to infants. Am. J. Primatol. 73:1269–1279, 2011.

Hierarchical steepness, counter-aggression, and Macaque social style scale

Nonhuman primates show remarkable variation in several aspects of social structure. One way to characterize this variation in the genus Macaca is through the concept of social style, which is based on the observation that several social traits appear to covary with one another in a linear or at least continuous manner. In practice, macaques are more simply characterized as fitting a four‐grade scale in which species range from extremely despotic (grade 1) to extremely tolerant (grade 4). Here, we examine the fit of three core measures of social style—two measures of dominance gradients (hierarchical steepness) and another closely related measure (counter‐aggression)—to this scale, controlling for phylogenetic relationships. Although raw scores for both steepness and counter‐aggression correlated with social scale in predicted directions, the distributions appeared to vary by measure. Counter‐aggression appeared to vary dichotomously with scale, with grade 4 species being distinct from all other grades. Steepness measures appeared more continuous. Species in grades 1 and 4 were distinct from one another on all measures, but those in the intermediate grades varied inconsistently. This confirms previous indications that covariation is more readily observable when comparing species at the extreme ends of the scale than those in intermediate positions. When behavioral measures were mapped onto phylogenetic trees, independent contrasts showed no significant consistent directional changes at nodes below which there were evolutionary changes in scale. Further, contrasts were no greater at these nodes than at neutral nodes. This suggests that correlations with the scale can be attributed largely to species’ phylogenetic relationships. This could be due in turn to a structural linkage of social traits based on adaptation to similar ecological conditions in the distant past, or simply to unlinked phylogenetic closeness. Am. J. Primatol. 74:915‐925, 2012.

Social buffering and contact transmission: network connections have beneficial and detrimental effects on Shigella infection risk among captive rhesus macaques

In social animals, group living may impact the risk of infectious disease acquisition in two ways. On the one hand, social connectedness puts individuals at greater risk or susceptibility for acquiring enteric pathogens via contact-mediated transmission. Yet conversely, in strongly bonded societies like humans and some nonhuman primates, having close connections and strong social ties of support can also socially buffer individuals against susceptibility or transmissibility of infectious agents. Using social network analyses, we assessed the potentially competing roles of contact-mediated transmission and social buffering on the risk of infection from an enteric bacterial pathogen (Shigella flexneri) among captive groups of rhesus macaques (Macaca mulatta). Our results indicate that, within two macaque groups, individuals possessing more direct and especially indirect connections in their grooming and huddling social networks were less susceptible to infection. These results are in sharp contrast to several previous studies that indicate that increased (direct) contact-mediated transmission facilitates infectious disease transmission, including our own findings in a third macaque group in which individuals central in their huddling network and/or which initiated more fights were more likely to be infected. In summary, our findings reveal that an individual’s social connections may increase or decrease its chances of acquiring infectious agents. They extend the applicability of the social buffering hypothesis, beyond just stress and immune-function-related health benefits, to the additional health outcome of infectious disease resistance. Finally, we speculate that the circumstances under which social buffering versus contact-mediated transmission may occur could depend on multiple factors, such as living condition, pathogen-specific transmission routes, and/or an overall social context such as a group’s social stability.

Human–wildlife conflict: Proximate predictors of aggression between humans and rhesus macaques in India

Macaques live in close contact with humans across South and Southeast Asia, and direct interaction is frequent. Aggressive contact is a concern in many locations, particularly among populations of rhesus and longtail macaques that co-inhabit urbanized cities and towns with humans. We investigated the proximate factors influencing the occurrence of macaque aggression toward humans as well as human aggression toward macaques to determine the extent to which human behavior elicits macaque aggression and vice versa. We conducted a 3-month study of four free-ranging populations of rhesus macaques in Dehradun, India from October-December 2012, using event sampling to record all instances of human-macaque interaction (N = 3120). Our results show that while human aggression was predicted by the potential for economic losses or damage, macaque aggression was influenced by aggressive or intimidating behavior by humans as well as recent rates of conspecific aggression. Further, adult female macaques participated in aggression more frequently than expected, whereas adult and subadult males participated as frequently as expected. Our analyses demonstrate that neither human nor macaque aggression is unprovoked. Rather, both humans and macaques are responding to one anothers behavior. Mitigation of human-primate conflict, and indeed other types of human-wildlife conflict in such coupled systems, will require a holistic investigation of the ways in which each participant is responding to, and consequently altering, the behavior of the other.

The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure

Among nonhuman primates, the evolutionary underpinnings of variation in social structure remain debated, with both ancestral relationships and adaptation to current conditions hypothesized to play determining roles. Here we assess whether interspecific variation in higher‐order aspects of female macaque (genus: Macaca) dominance and grooming social structure show phylogenetic signals, that is, greater similarity among more closely‐related species. We use a social network approach to describe higher‐order characteristics of social structure, based on both direct interactions and secondary pathways that connect group members. We also ask whether network traits covary with each other, with species‐typical social style grades, and/or with sociodemographic characteristics, specifically group size, sex‐ratio, and current living condition (captive vs. free‐living). We assembled 34–38 datasets of female‐female dyadic aggression and allogrooming among captive and free‐living macaques representing 10 species. We calculated dominance (transitivity, certainty), and grooming (centrality coefficient, Newmans modularity, clustering coefficient) network traits as aspects of social structure. Computations of K statistics and randomization tests on multiple phylogenies revealed moderate‐strong phylogenetic signals in dominance traits, but moderate‐weak signals in grooming traits. GLMMs showed that grooming traits did not covary with dominance traits and/or social style grade. Rather, modularity and clustering coefficient, but not centrality coefficient, were strongly predicted by group size and current living condition. Specifically, larger groups showed more modular networks with sparsely‐connected clusters than smaller groups. Further, this effect was independent of variation in living condition, and/or sampling effort. In summary, our results reveal that female dominance networks were more phylogenetically conserved across macaque species than grooming networks, which were more labile to sociodemographic factors. Such findings narrow down the processes that influence interspecific variation in two core aspects of macaque social structure. Future directions should include using phylogeographic approaches, and addressing challenges in examining the effects of socioecological factors on primate social structure.

Social network community structure and the contact-mediated sharing of commensal E. coli among captive rhesus macaques (Macaca mulatta)

In group-living animals, heterogeneity in individuals’ social connections may mediate the sharing of microbial infectious agents. In this regard, the genetic relatedness of individuals’ commensal gut bacterium Escherichia coli may be ideal to assess the potential for pathogen transmission through animal social networks. Here we use microbial phylogenetics and population genetics approaches, as well as host social network reconstruction, to assess evidence for the contact-mediated sharing of E. coli among three groups of captively housed rhesus macaques (Macaca mulatta), at multiple organizational scales. For each group, behavioral data on grooming, huddling, and aggressive interactions collected for a six-week period were used to reconstruct social network communities via the Data Cloud Geometry (DCG) clustering algorithm. Further, an E. coli isolate was biochemically confirmed and genotypically fingerprinted from fecal swabs collected from each macaque. Population genetics approaches revealed that Group Membership, in comparison to intrinsic attributes like age, sex, and/or matriline membership of individuals, accounted for the highest proportion of variance in E. coli genotypic similarity. Social network approaches revealed that such sharing was evident at the community-level rather than the dyadic level. Specifically, although we found no links between dyadic E. coli similarity and social contact frequencies, similarity was significantly greater among macaques within the same social network communities compared to those across different communities. Moreover, tests for one of our study-groups confirmed that E. coli isolated from macaque rectal swabs were more genotypically similar to each other than they were to isolates from environmentally deposited feces. In summary, our results suggest that among frequently interacting, spatially constrained macaques with complex social relationships, microbial sharing via fecal-oral, social contact-mediated routes may depend on both individuals’ direct connections and on secondary network pathways that define community structure. They lend support to the hypothesis that social network communities may act as bottlenecks to contain the spread of infectious agents, thereby encouraging disease control strategies to focus on multiple organizational scales. Future directions includeincreasing microbial sampling effort per individual to better-detect dyadic transmission events, and assessments of the co-evolutionary links between sociality, infectious agent risk, and host immune function.

Rates of human-macaque interactions affect grooming behavior among urban-dwelling rhesus macaques (Macaca mulatta)

OBJECTIVES The impact of anthropogenic environmental changes may impose strong pressures on the behavioral flexibility of free-ranging animals. Here, we examine whether rates of interactions with humans had both a direct and indirect influence on the duration and distribution of social grooming in commensal rhesus macaques (Macaca mulatta). MATERIALS AND METHODS Data were collected in two locations in the city of Shimla in northern India: an urban setting and a temple area. We divided these two locations in a series of similar-sized physical blocks (N = 48) with varying rates of human-macaque interactions. We conducted focal observations on three free-ranging rhesus macaque groups, one in the urban area and two in the temple area. RESULTS Our analysis shows that macaques engaged in shorter grooming bouts and were more vigilant while grooming in focal sessions during which they interacted with people more frequently, suggesting that humans directly affected grooming effort and vigilance behavior. Furthermore, we found that in blocks characterized by higher rates of human-macaque interactions grooming bouts were shorter, more frequently interrupted by vigilance behavior, and were less frequently reciprocated. DISCUSSION Our work shows that the rates of human-macaque interaction had both a direct and indirect impact on grooming behavior and that macaques flexibly modified their grooming interactions in relation to the rates of human-macaque interaction to which they were exposed. Because grooming has important social and hygienic functions in nonhuman primates, our work suggests that human presence can have important implications for animal health, social relationships and, ultimately, fitness. Our results point to the need of areas away from people even for highly adaptable species where they can engage in social interactions without human disruption.

Noel Rowe and Marc Myers (Eds.): All the World’s Primates

The last decade has seen an exponential increase in the discovery and taxonomic classification of new species. The reasons include (but are not restricted to) global expansions of human populations shrinking uncharted areas (Dickman 2012), reevaluations of species concepts (Groves 2012), and developments in whole genome sequencing technologies (Raupach et al. 2016). Primates have been no exception. Within just this order, there have been more than 250 newly discovered or reclassified species between 1996 and 2016. Sadly, the elation of such discovery remains marred by the reality of how many species continue to be listed as Critically Endangered or Vulnerable to Extinction. This is primarily because nonhuman primates, aside from common evolutionary histories (Hasegawa et al. 1985), have also shared and competed for ecological space and resources with humans for centuries (Dickman 2012). These reasons make reviews of primate taxonomic diversity especially significant. In 1996, Noel Rowe’s Pictorial Guide to Living Primates provided one of the most comprehensive overviews of primate taxonomic diversity written to date, covering 237 species (Rowe 1996). Since then, it has remained a primary, central resource for researchers interested in inferring simple, descriptive information and illustrations on primates. All the World’s Primates is a significant and timely upgrade to this effort. The book is a follow-up to the establishment of an online database, first launched in 2011 and being continuously updated since (www.alltheworldsprimates.org). The website is run by Primate Conservation Inc. (PCI), a nonprofit organization that provides financial support to scientists in habitat countries early in their careers. Other than its Int J Primatol DOI 10.1007/s10764-017-9966-9