Noah Snyder-Mackler

Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups

By living in social groups with potential competitors, animals forgo monopolizing access to resources. Consequently, debate continues over how selection might favour sociality among competitors. For example, several models exist to account for the evolution of shared reproduction in groups. The ‘concession model’ hypothesizes that dominant reproducers benefit from the presence of subordinates, and hence tolerate some reproduction by subordinates. This mutual benefit to both dominants and subordinates may provide a foundation for the formation of social groups in which multiple members reproduce—a necessary step in the evolution of cooperation. To date, however, the concession model has received virtually no support in vertebrates. Instead, the vast majority of vertebrate data support ‘limited control models’, which posit that dominant reproducers are simply unable to prevent subordinates from reproducing. Here we present the most comprehensive evidence to date in support of the concession model in a vertebrate. We examined natural variation in the number of adult males in gelada (Theropithecus gelada) reproductive units to assess the extent of reproductive skew in multi-male units. Dominant (‘leader’) males in units that also had subordinate (‘follower’) males had a 30 per cent longer tenure than leaders in units that did not have followers, mainly because followers actively defended the group against potential immigrants. Follower males also obtained a small amount of reproduction in the unit, which may have functioned as a concession in return for defending the unit. These results suggest that dominants and subordinates may engage in mutually beneficial reproductive transactions, thus favouring male–male tolerance and cooperation.

Social status alters immune regulation and response to infection in macaques

Status alters immune function in macaques Rhesus macaques experience variable levels of stress on the basis of their position in the social hierarchy. To examine how stress affects immune function, Snyder-Mackler et al. manipulated the social status of individual macaques (see the Perspective by Sapolsky). Social status influenced the immune system at multiple levels, from immune cell numbers to gene expression, and altered signaling pathways in a model of response to infection. Macaques possess a plastic and adaptive immune response wherein social subordination promotes antibacterial responses, whereas high social status promotes antiviral responses. Science, this issue p. 1041; see also p. 967 Manipulation of social status in macaques affects cell-specific immune gene regulation. Social status is one of the strongest predictors of human disease risk and mortality, and it also influences Darwinian fitness in social mammals more generally. To understand the biological basis of these effects, we combined genomics with a social status manipulation in female rhesus macaques to investigate how status alters immune function. We demonstrate causal but largely plastic social status effects on immune cell proportions, cell type–specific gene expression levels, and the gene expression response to immune challenge. Further, we identify specific transcription factor signaling pathways that explain these differences, including low-status–associated polarization of the Toll-like receptor 4 signaling pathway toward a proinflammatory response. Our findings provide insight into the direct biological effects of social inequality on immune function, thus improving our understanding of social gradients in health.

The ontogeny of social skills: experimental increases in social complexity enhance reproductive success in adult cowbirds

The social environment can act as an important selective force on both morphological and behavioural traits by conferring a reproductive advantage on individuals that successfully navigate social interactions. The ontogeny of these social traits is poorly understood. We examined whether increasing exposure to more complex social environments could hone competitive skills and ultimately increase reproductive success in adult brown-headed cowbirds, Molothrus ater. We created two types of flocks (‘Dynamic’ and ‘Stable’) that differed in social complexity. In Dynamic flocks, birds were regularly exchanged across groups, whereas in ‘Stable’ flocks, the composition of birds remained static throughout a year. Social networking analyses revealed that males in the Dynamic flocks had larger and more variable singing networks during the manipulations than did the males in the Stable flocks. When we put males from the two conditions together into new environments with unfamiliar females, the Dynamic-condition males had greater mating success. Our results establish a link between social competence and reproductive success and suggest that social skills are extremely flexible characteristics, even in adulthood.

Efficient Genome-Wide Sequencing and Low-Coverage Pedigree Analysis from Noninvasively Collected Samples

Research on the genetics of natural populations was revolutionized in the 1990s by methods for genotyping noninvasively collected samples. However, these methods have remained largely unchanged for the past 20 years and lag far behind the genomics era. To close this gap, here we report an optimized laboratory protocol for genome-wide capture of endogenous DNA from noninvasively collected samples, coupled with a novel computational approach to reconstruct pedigree links from the resulting low-coverage data. We validated both methods using fecal samples from 62 wild baboons, including 48 from an independently constructed extended pedigree. We enriched fecal-derived DNA samples up to 40-fold for endogenous baboon DNA and reconstructed near-perfect pedigree relationships even with extremely low-coverage sequencing. We anticipate that these methods will be broadly applicable to the many research systems for which only noninvasive samples are available. The lab protocol and software (“WHODAD”) are freely available at www.tung-lab.org/protocols-and-software.html and www.xzlab.org/software.html, respectively.

Kinship and Dominance Rank Influence the Strength of Social Bonds in Female Geladas (Theropithecus gelada)

In many primates, close social relationships are associated with lower stress, better health, and increased life span. However, individuals do not form bonds indiscriminately; rather, they focus on a few primary partners. This suggests that the identity of the partner may be as important as the bond itself. Although dominance and kinship have repeatedly emerged as salient predictors of female relationships, most of this research comes from species with multimale, multifemale groups and strict dominance hierarchies. Further, kinship was typically determined based on either behavior or on known mother–daughter relationships alone. To understand the generality of previous findings, we use behavioral and genetic sampling to examine whether dominance rank and/or genetic relatedness mediate female social bonds in geladas (Theropithecus gelada) living in the Simien Mountains National Park, Ethiopia. First, we found that, even though females in the same unit are closely related, female geladas still preferentially bond with the closest of these relatives. Second, females that were close kin formed the strongest bonds with females of similar rank to themselves. Finally, rank disparity predicted grooming rates but did not predict whether females were nearest neighbors. This suggests that, in contrast with data from other cercopithecines, spatial proximity among females may be less indicative of strong social bonds for geladas, a species that routinely exhibits a high degree of spatial overlap with extra-unit individuals. Together, these results highlight the importance of combining genetic data with detailed behavioral observations to help us understand how individuals choose and interact with social partners.

Social networks and the development of social skills in cowbirds

The complex interrelationships among individuals within social environments can exert selection pressures on social skills: those behaviours and cognitive processes that allow animals to manipulate and out-reproduce others. Social complexity can also have a developmental effect on social skills by providing individuals with opportunities to hone their skills by dealing with the challenges posed in within-group interactions. We examined how social skills develop in captive, adult male brown-headed cowbirds (Molothrus ater) that were exposed to differing levels of ‘social complexity’ across a 2-year experiment. After each year, subjects housed in groups with dynamic social structure (where many individuals entered and exited the groups during the year) outcompeted birds who had been housed in static groups. Exposure to dynamic structure subsequently led to substantial changes to the social networks of the home conditions during the breeding season. Static groups were characterized by a predictable relationship between singing and reproductive success that was stable across years. In dynamic conditions, however, males showed significant variability in their dominance status, their courting and even in their mating success. Reproductive success of males varied dramatically across years and was responsive to social learning in adulthood, and socially dynamic environments ‘trained’ individuals to be better competitors, even at an age when the development of many traits important for breeding (like song quality) had ended.

Social 'predators' within a multilevel primate society

Group living confers a variety of benefits to individuals, particularly in predator detection and defence. Hamiltons selfish herd hypothesis ( Hamilton 1971 , Journal of Theoretical Biology, 31, 295–311) posits that individuals come together to reduce their own risk of predation, and numerous studies have shown that predators affect both the grouping and spacing patterns of their prey. We suggest that this hypothesis is also useful for understanding group responses to a very different threat: that posed by nonbreeding, potentially infanticidal males. In such cases, males may act as a predator-like force on the grouping patterns of breeding individuals. We hypothesized that nonbreeding males, like predators, can affect the spacing patterns of conspecifics. Specifically, we examined the effect of bachelor males on both the grouping and spacing patterns of gelada, Theropithecus gelada , reproductive units. First, we demonstrated that the number of bachelors was positively correlated with the number of animals in a group. Second, and more importantly, we found that bachelors exerted an acute pressure on the spacing of individuals; as bachelors approached, breeding individuals moved closer to their nearest neighbours. By approaching other breeding individuals, reproductive males and females may dilute the costs of associating with bachelor males.

Genomewide ancestry and divergence patterns from low-coverage sequencing data reveal a complex history of admixture in wild baboons

Naturally occurring admixture has now been documented in every major primate lineage, suggesting its key role in primate evolutionary history. Active primate hybrid zones can provide valuable insight into this process. Here, we investigate the history of admixture in one of the best‐studied natural primate hybrid zones, between yellow baboons (Papio cynocephalus) and anubis baboons (Papio anubis) in the Amboseli ecosystem of Kenya. We generated a new genome assembly for yellow baboon and low‐coverage genomewide resequencing data from yellow baboons, anubis baboons and known hybrids (n = 44). Using a novel composite likelihood method for estimating local ancestry from low‐coverage data, we found high levels of genetic diversity and genetic differentiation between the parent taxa, and excellent agreement between genome‐scale ancestry estimates and a priori pedigree, life history and morphology‐based estimates (r2 = 0.899). However, even putatively unadmixed Amboseli yellow individuals carried a substantial proportion of anubis ancestry, presumably due to historical admixture. Further, the distribution of shared vs. fixed differences between a putatively unadmixed Amboseli yellow baboon and an unadmixed anubis baboon, both sequenced at high coverage, is inconsistent with simple isolation–migration or equilibrium migration models. Our findings suggest a complex process of intermittent contact that has occurred multiple times in baboon evolutionary history, despite no obvious fitness costs to hybrids or major geographic or behavioural barriers. In combination with the extensive phenotypic data available for baboon hybrids, our results provide valuable context for understanding the history of admixture in primates, including in our own lineage.

Social status drives social relationships in groups of unrelated female rhesus macaques

Strong social relationships confer health and fitness benefits in a number of species, motivating the need to understand the processes through which they arise. In female cercopithecine primates, both kinship and dominance rank are thought to influence rates of affiliative behaviour and social partner preference. Teasing apart the relative importance of these factors has been challenging, however, as female kin often occupy similar positions in the dominance hierarchy. Here, we isolated the specific effects of rank on social relationships in female rhesus macaques by analysing grooming patterns in 18 social groups that did not contain close relatives, and in which dominance ranks were experimentally randomized. We found that grooming was asymmetrically directed towards higher-ranking females and that grooming bouts temporarily decreased the likelihood of aggression between grooming partners, supporting the idea that grooming is associated with social tolerance. Even in the absence of kin, females formed the strongest grooming relationships with females adjacent to them in rank, a pattern that was strongest for the highest-ranking females. Using simulations, we show that three rules for allocating grooming based on dominance rank recapitulated most of the relationships we observed. Finally, we evaluated whether a females tendency to engage in grooming behaviour was stable across time and social setting. We found that one measure, the rate of grooming females provided to others (but not the rate of grooming females received), exhibited modest stability after accounting for the primary effect of dominance rank. Together, our findings indicate that dominance rank has strong effects on social relationships in the absence of kin, suggesting the importance of considering social status and social connectedness jointly when investigating their health and fitness consequences.

The socio-genetics of a complex society: female gelada relatedness patterns mirror association patterns in a multilevel society

Multilevel societies with fission–fusion dynamics—arguably the most complex animal societies—are defined by two or more nested levels of organization. The core of these societies are modular social units that regularly fission and fuse with one another. Despite convergent evolution in disparate taxa, we know strikingly little about how such societies form and how fitness benefits operate. Understanding the kinship structure of complex societies could inform us about the origins of the social structure as well as about the potential for individuals in these societies to accrue indirect fitness benefits. Here, we combined genetic and behavioural data on geladas (Theropithecus gelada), an Old World Monkey, to complete the most comprehensive socio‐genetic analysis of a multilevel society to date. In geladas, individuals in the core social ‘units’, associate at different frequencies to form ‘teams’, ‘bands’ and, the largest aggregations, ‘communities’. Units were composed of closely related females, and females remained with their close kin during permanent fissions of units. Interestingly, female–female relatedness also significantly predicted between‐unit, between‐team and between‐band association patterns, while male–male relatedness did not. Thus, it is likely that the socio‐genetic structure of gelada society results from females maintaining associations with their female relatives during successive unit fissions—possibly in an attempt to balance the direct and indirect fitness benefits of group living. Overall, the persistence of associations among related females across generations appears to drive the formation of higher levels of gelada society, suggesting that females seek kin for inclusive fitness benefits at multiple levels of gelada society.