Publications by category
Journal articles
Hart JDA, Franks DW, Brent LJN, Weiss MN (In Press). Accuracy and Power Analysis of Social Networks Built from Count Data.
Abstract:
Accuracy and Power Analysis of Social Networks Built from Count Data
AbstractPower analysis is used to estimate the probability of correctly rejecting a null hypothesis for a given statistical model and dataset. Conventional power analyses assume complete information, but the stochastic nature of behavioural sampling can mean that true and estimated networks are poorly correlated. Power analyses do not currently take the effect of sampling into account. This could lead to inaccurate estimates of statistical power, potentially yielding misleading results.Here we develop a method for computing network correlation: the correlation between an estimated social network and its true network, using a Gamma-Poisson model of social event rates for networks constructed from count data. We use simulations to assess how the level of network correlation affects the power of nodal regression analyses. We also develop a generic method of power analysis applicable to any statistical test, based on the concept of diminishing returns.We demonstrate that our network correlation estimator is both accurate and moderately robust to its assumptions being broken. We show that social differentiation, mean social event rate, and the harmonic mean of sampling times positively impacts the strength of network correlation. We also show that the required level of network correlation to achieve a given power level depends on many factors, but that 0.80 network correlation usually corresponds to around 0.80 power for nodal regression in ideal circumstances.We provide guidelines for using our network correlation estimator to verify the accuracy of networks built from count data, and to conduct power analysis. This can be used prior to data collection, in post hoc analyses, or even for subsetting networks in dynamic network analysis. The network correlation estimator and custom power analysis methods have been made available as an R package.
Abstract.
Fernandes AG, Alexopoulos P, Burgos-Rodriguez A, Martinez MI, Ghassibi M, Leskov I, Brent LJN, Snyder-Mackler N, Danias J, Wollstein G, et al (2023). Age-Related Differences in Ocular Features of a Naturalistic Free-Ranging Population of Rhesus Macaques. Investigative Opthalmology & Visual Science, 64(7), 3-3.
Siracusa ER, Pereira AS, Brask JB, Negron-Del Valle JE, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (2023). Ageing in a collective: the impact of ageing individuals on social network structure.
Philosophical Transactions of the Royal Society B: Biological Sciences,
378(1874).
Abstract:
Ageing in a collective: the impact of ageing individuals on social network structure
Ageing affects many phenotypic traits, but its consequences for social behaviour have only recently become apparent. Social networks emerge from associations between individuals. The changes in sociality that occur as individuals get older are thus likely to impact network structure, yet this remains unstudied. Here we use empirical data from free-ranging rhesus macaques and an agent-based model to test how age-based changes in social behaviour feed up to influence: (i) an individual's level of indirect connectedness in their network and (ii) overall patterns of network structure. Our empirical analyses revealed that female macaques became less indirectly connected as they aged for some, but not for all network measures examined. This suggests that indirect connectivity is affected by ageing, and that ageing animals can remain well integrated in some social contexts. Surprisingly, we did not find evidence for a relationship between age distribution and the structure of female macaque networks. We used an agent-based model to gain further understanding of the link between age-based differences in sociality and global network structure, and under which circumstances global effects may be detectable. Overall, our results suggest a potentially important and underappreciated role of age in the structure and function of animal collectives, which warrants further investigation.
. This article is part of a discussion meeting issue ‘Collective behaviour through time’.
Abstract.
Hart J, Weiss MN, Franks D, Brent L (2023). BISoN: a Bayesian framework for inference of social networks.
Methods in Ecology and Evolution,
14(9), 2411-2420.
Abstract:
BISoN: a Bayesian framework for inference of social networks
Abstract
Animal social networks are often constructed from point estimates of edge weights. In many contexts, edge weights are inferred from observational data, and the uncertainty around estimates can be affected by various factors. Though this has been acknowledged in previous work, methods that explicitly quantify uncertainty in edge weights have not yet been widely adopted and remain undeveloped for many common types of data. Furthermore, existing methods are unable to cope with some of the complexities often found in observational data, and do not propagate uncertainty in edge weights to subsequent statistical analyses.
We introduce a unified Bayesian framework for modelling social networks based on observational data. This framework, which we call BISoN, can accommodate many common types of observational social data, can capture confounds and model effects at the level of observations and is fully compatible with popular methods used in social network analysis.
We show how the framework can be applied to common types of data and how various types of downstream statistical analyses can be performed, including non‐random association tests and regressions on network properties.
Our framework opens up the opportunity to test new types of hypotheses, make full use of observational datasets, and increase the reliability of scientific inferences. We have made both an R package and example R scripts available to enable adoption of the framework.
Abstract.
Watowich MM, Chiou KL, Graves B, Montague MJ, Brent LJN, Higham JP, Horvath JE, Lu A, Martinez MI, Platt ML, et al (2023). Best practices for genotype imputation from low‐coverage sequencing data in natural populations.
Molecular Ecology ResourcesAbstract:
Best practices for genotype imputation from low‐coverage sequencing data in natural populations
AbstractMonitoring genetic diversity in wild populations is a central goal of ecological and evolutionary genetics and is critical for conservation biology. However, genetic studies of nonmodel organisms generally lack access to species‐specific genotyping methods (e.g. array‐based genotyping) and must instead use sequencing‐based approaches. Although costs are decreasing, high‐coverage whole‐genome sequencing (WGS), which produces the highest confidence genotypes, remains expensive. More economical reduced representation sequencing approaches fail to capture much of the genome, which can hinder downstream inference. Low‐coverage WGS combined with imputation using a high‐confidence reference panel is a cost‐effective alternative, but the accuracy of genotyping using low‐coverage WGS and imputation in nonmodel populations is still largely uncharacterized. Here, we empirically tested the accuracy of low‐coverage sequencing (0.1–10×) and imputation in two natural populations, one with a large (n = 741) reference panel, rhesus macaques (Macaca mulatta), and one with a smaller (n = 68) reference panel, gelada monkeys (Theropithecus gelada). Using samples sequenced to coverage as low as 0.5×, we could impute genotypes at >95% of the sites in the reference panel with high accuracy (median r2 ≥ 0.92). We show that low‐coverage imputed genotypes can reliably calculate genetic relatedness and population structure. Based on these data, we also provide best practices and recommendations for researchers who wish to deploy this approach in other populations, with all code available on GitHub (https://github.com/mwatowich/LoCSI‐for‐non‐model‐species). Our results endorse accurate and effective genotype imputation from low‐coverage sequencing, enabling the cost‐effective generation of population‐scale genetic datasets necessary for tackling many pressing challenges of wildlife conservation.
Abstract.
Pereira A, De Moor D, Casanova C, Brent LJN (2023). Kinship composition in mammals. Royal Society Open Science
Patterson SK, Petersen RM, Brent LJN, Snyder-Mackler N, Lea AJ, Higham JP (2023). Natural Animal Populations as Model Systems for Understanding Early Life Adversity Effects on Aging.
Integrative and Comparative Biology,
63(3), 681-692.
Abstract:
Natural Animal Populations as Model Systems for Understanding Early Life Adversity Effects on Aging
Synopsis
. Adverse experiences in early life are associated with aging-related disease risk and mortality across many species. In humans, confounding factors, as well as the difficulty of directly measuring experiences and outcomes from birth till death, make it challenging to identify how early life adversity impacts aging and health. These challenges can be mitigated, in part, through the study of non-human animals, which are exposed to parallel forms of adversity and can age similarly to humans. Furthermore, studying the links between early life adversity and aging in natural populations of non-human animals provides an excellent opportunity to better understand the social and ecological pressures that shaped the evolution of early life sensitivities. Here, we highlight ongoing and future research directions that we believe will most effectively contribute to our understanding of the evolution of early life sensitivities and their repercussions.
Abstract.
Grimes C, Brent LJN, Ellis S, Weiss MN, Franks DW, Ellifrit DK, Croft DP (2023). Postreproductive female killer whales reduce socially inflicted injuries in their male offspring. Current Biology, 33(15), 3250-3256.e4.
Newman LE, Testard C, DeCasien AR, Chiou KL, Watowich MM, Janiak MC, Pavez-Fox MA, Sanchez Rosado MR, Cooper EB, Costa CE, et al (2023). The biology of aging in a social world: insights from free-ranging rhesus macaques.
bioRxivAbstract:
The biology of aging in a social world: insights from free-ranging rhesus macaques.
Social adversity can increase the age-associated risk of disease and death, yet the biological mechanisms that link social adversities to aging remain poorly understood. Long-term naturalistic studies of nonhuman animals are crucial for integrating observations of social behavior throughout an individual's life with detailed anatomical, physiological, and molecular measurements. Here, we synthesize the body of research from one such naturalistic study system, Cayo Santiago Island, which is home to the world's longest continuously monitored free-ranging population of rhesus macaques. We review recent studies of age-related variation in morphology, gene regulation, microbiome composition, and immune function. We also discuss ecological and social modifiers of age-markers in this population. In particular, we summarize how a major natural disaster, Hurricane Maria, affected rhesus macaque physiology and social structure and highlight the context-dependent and domain-specific nature of aging modifiers. Finally, we conclude by providing directions for future study, on Cayo Santiago and elsewhere, that will further our understanding of aging across different domains and how social adversity modifies aging processes.
Abstract.
Author URL.
Kimock CM, Dubuc C, Brent L, Higham JP (2022). Body size and canine size do not confer a competitive advantage in male rhesus macaques. Animal Behaviour
Hart JDA, Weiss MN, Brent LJN, Franks DW (2022). Common permutation methods in animal social network analysis do not control for non-independence.
Behavioral Ecology and Sociobiology,
76(11).
Abstract:
Common permutation methods in animal social network analysis do not control for non-independence
AbstractThe 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.
Abstract.
Cooper EB, Watowich MM, Beeby N, Whalen C, Montague MJ, Brent LJN, Snyder-Mackler N, Higham JP (2022). Concentrations of urinary neopterin, but not suPAR, positively correlate with age in rhesus macaques.
Frontiers in Ecology and Evolution,
10Abstract:
Concentrations of urinary neopterin, but not suPAR, positively correlate with age in rhesus macaques
Identifying biomarkers of age-related changes in immune system functioning that can be measured non-invasively is a significant step in progressing research on immunosenescence and inflammaging in free-ranging and wild animal populations. In the present study, we aimed to investigate the suitability of two urinary compounds, neopterin and suPAR, as biomarkers of age-related changes in immune activation and inflammation in a free-ranging rhesus macaque (Macaca mulatta) population. We also investigated age-associated variation in gene transcription from blood samples to understand the underlying proximate mechanisms that drive age-related changes in urinary neopterin or suPAR. Neopterin was significantly positively correlated with age, and had a moderate within-individual repeatability, indicating it is applicable as a biomarker of age-related changes. The age-related changes in urinary neopterin are not apparently driven by an age-related increase in the primary signaler of neopterin, IFN-y, but may be driven instead by an age-related increase in both CD14+ and CD14− monocytes. suPAR was not correlated with age, and had low repeatability within-individuals, indicating that it is likely better suited to measure acute inflammation rather than chronic age-related increases in inflammation (i.e. “inflammaging”). Neopterin and suPAR had a correlation of 25%, indicating that they likely often signal different processes, which if disentangled could provide a nuanced picture of immune-system function and inflammation when measured in tandem.
Abstract.
Bonnet T, Morrissey MB, de Villemereuil P, Alberts SC, Arcese P, Bailey LD, Boutin S, Brekke P, Brent LJN, Camenisch G, et al (2022). Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.
Science,
376(6596), 1012-1016.
Abstract:
Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals
The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.
Abstract.
Kuthyar S, Watson K, Huang S, Brent LJN, Platt M, Horvath J, Gonzalez-Martinez J, Martínez M, Godoy-Vitorino F, Knight R, et al (2022). Limited microbiome differences in captive and semi-wild primate populations consuming similar diets.
FEMS Microbiology Ecology,
98(10).
Abstract:
Limited microbiome differences in captive and semi-wild primate populations consuming similar diets
Abstract
. Gut microbial communities are shaped by a myriad of extrinsic factors, including diet and the environment. Although distinct human populations consistently exhibit different gut microbiome compositions, variation in diet and environmental factors are almost always coupled, making it difficult to disentangle their relative contributions to shaping the gut microbiota. Data from discrete animal populations with similar diets can help reduce confounds. Here, we assessed the gut microbiota of free-ranging and captive rhesus macaques with at least 80% diet similarity to test the hypothesis that hosts in difference environments will have different gut microbiomes despite a shared diet. Although we found that location was a significant predictor of gut microbial composition, the magnitude of observed differences was relatively small. These patterns suggest that a shared diet may limit the typical influence of environmental microbial exposure on the gut microbiota.
Abstract.
Chiou KL, DeCasien AR, Rees KP, Testard C, Spurrell CH, Gogate AA, Pliner HA, Tremblay S, Mercer A, Whalen CJ, et al (2022). Multiregion transcriptomic profiling of the primate brain reveals signatures of aging and the social environment.
Nat Neurosci,
25(12), 1714-1723.
Abstract:
Multiregion transcriptomic profiling of the primate brain reveals signatures of aging and the social environment.
Aging is accompanied by a host of social and biological changes that correlate with behavior, cognitive health and susceptibility to neurodegenerative disease. To understand trajectories of brain aging in a primate, we generated a multiregion bulk (N = 527 samples) and single-nucleus (N = 24 samples) brain transcriptional dataset encompassing 15 brain regions and both sexes in a unique population of free-ranging, behaviorally phenotyped rhesus macaques. We demonstrate that age-related changes in the level and variance of gene expression occur in genes associated with neural functions and neurological diseases, including Alzheimer's disease. Further, we show that higher social status in females is associated with younger relative transcriptional ages, providing a link between the social environment and aging in the brain. Our findings lend insight into biological mechanisms underlying brain aging in a nonhuman primate model of human behavior, cognition and health.
Abstract.
Author URL.
Watowich MM, Chiou KL, Montague MJ, Simons ND, Horvath JE, Ruiz-Lambides AV, Martínez MI, Higham JP, Brent LJN, Platt ML, et al (2022). Natural disaster and immunological aging in a nonhuman primate.
Proceedings of the National Academy of Sciences,
119(8).
Abstract:
Natural disaster and immunological aging in a nonhuman primate
Significance
. Survivors of extreme adverse events, including natural disasters, often exhibit chronic inflammation and early onset of age-related diseases. Adversity may therefore accelerate aging via the immune system, which is sensitive to lived experiences. We tested if experiencing a hurricane was associated with immune gene expression in a population of free-ranging macaques. Exposure to Hurricane Maria broadly recapitulated age-associated molecular changes, including disruptions of protein folding genes, greater inflammatory immune cell marker gene expression, and older biological aging by an average of 2 y—approximately 7 to 8 y of the human lifespan. Together, our findings suggest that experiencing an extreme hurricane is associated with alterations in immune cell gene regulation similar to aging, potentially accelerating aspects of the aging process.
Abstract.
O’Hearn WJ, Ruiz-Lambides A, Platt ML, Brent LJN (2022). No evidence that grooming is exchanged for coalitionary support in the short- or long-term via direct or generalized reciprocity in unrelated rhesus macaques.
Behavioral Ecology and Sociobiology,
76(4).
Abstract:
No evidence that grooming is exchanged for coalitionary support in the short- or long-term via direct or generalized reciprocity in unrelated rhesus macaques
. Abstract
. Reciprocity is a prominent explanation for cooperation between non-kin. Studies designed to demonstrate reciprocity often focus on direct reciprocity in the timescale of minutes to hours, whereas alternative mechanisms like generalized reciprocity and the possibility of reciprocation over longer timescales of months and years are less often explored. Using a playback experiment, we tested for evidence of direct and generalized reciprocity across short and longer timescales. We examined the exchange of grooming for coalitionary support between unrelated female rhesus macaques in a population with a complete genetic pedigree. Females that received grooming were not more responsive to calls for coalitionary support from unrelated female group mates compared to control females that received agonism or no interaction — even when the call belonged to a females’ most recent grooming partner. Similarly, females were not more responsive to calls for support from their most frequent unrelated grooming partner of the last two years, nor if they received large amounts of grooming from all other females in their group. We interpret these results as an absence of evidence for direct or generalized reciprocity on any timescale in the exchange of grooming for coalitionary support in rhesus macaques. If grooming is exchanged for support in this population, it is with an intensity below our ability to detect it or over a longer timescale than we examined. We propose by-product explanations may also be at play and highlight the importance of investigating multiple mechanisms when testing apparently cooperative behaviors.
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. Significance statement
. The receipt of help can make some animals more likely to provide help in return, whether it be a singular act, or many acts accumulated over months. Similarly, the receipt of help, be it one act of aid, or a group’s worth of help over time, can make some animals more likely to pay help forward to others. Studies on Old World monkeys suggest females may give grooming and in return receive aid in future physical conflicts. Using a playback experiment, we found female rhesus macaques were not more responsive to calls for intervention in a simulated conflict after being groomed by unrelated females, even if the calling combatant was her most recent, or a long-time grooming partner. Our results suggest females in our study population may be receiving benefits other than support in conflicts for the grooming they provide.
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Abstract.
Ellis S, Cant M, Weiss M, Brent L, Meniri M, Thompson F, Croft D (2022). Patterns and consequences of age-linked change in local relatedness in animal societies.
Nature Ecology and EvolutionAbstract:
Patterns and consequences of age-linked change in local relatedness in animal societies
The ultimate payoff of behaviours depends not only on their direct impact on an individual but also on the impact on their relatives. Local relatedness – the average relatedness of an individual to their social environment – therefore has profound impacts on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual’s lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their impacts on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly impact lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.
Abstract.
Pavez-Fox MA, Kimock CM, Rivera-Barreto N, Negron-Del Valle JE, Phillips D, Ruiz-Lambides A, Snyder-Mackler N, Higham JP, Siracusa ER, Brent LJN, et al (2022). Reduced injury risk links sociality to survival in a group-living primate. iScience, 25(11), 105454-105454.
Siracusa ER, Higham JP, Snyder-Mackler N, Brent LJN (2022). Social ageing: exploring the drivers of late-life changes in social behaviour in mammals.
Biology Letters,
18(3).
Abstract:
Social ageing: exploring the drivers of late-life changes in social behaviour in mammals
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.
Abstract.
Testard C, Brent L, Andersson J, Chiou KL, Negron Del-Valle JE, DeCasien AR, Acevedo-Ithier A, Stock MK, Anton SC, Gonzalez O, et al (2022). Social connections predict brain structure in a multidimensional free-ranging primate society. Science Advances
Cooper EB, Brent LJN, Snyder-Mackler N, Singh M, Sengupta A, Khatiwada S, Malaivijitnond S, Qi Hai Z, Higham JP (2022). The rhesus macaque as a success story of the Anthropocene.
Elife,
11Abstract:
The rhesus macaque as a success story of the Anthropocene.
Of all the non-human primate species studied by researchers, the rhesus macaque (Macaca mulatta) is likely the most widely used across biological disciplines. Rhesus macaques have thrived during the Anthropocene and now have the largest natural range of any non-human primate. They are highly social, exhibit marked genetic diversity, and display remarkable niche flexibility (which allows them to live in a range of habitats and survive on a variety of diets). These characteristics mean that rhesus macaques are well-suited for understanding the links between sociality, health and fitness, and also for investigating intra-specific variation, adaptation and other topics in evolutionary ecology.
Abstract.
Author URL.
Siracusa ER, Negron-Del Valle JE, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (2022). Within-individual changes reveal increasing social selectivity with age in rhesus macaques.
Proceedings of the National Academy of Sciences,
119(49).
Abstract:
Within-individual changes reveal increasing social selectivity with age in rhesus macaques
Accumulating evidence in humans and other mammals suggests older individuals tend to have smaller social networks. Uncovering the cause of these declines can inform how changes in social relationships with age affect health and fitness in later life. While age-based declines in social networks have been thought to be detrimental, physical and physiological limitations associated with age may lead older individuals to adjust their social behavior and be more selective in partner choice. Greater selectivity with age has been shown in humans, but the extent to which this phenomenon occurs across the animal kingdom remains an open question. Using longitudinal data from a population of rhesus macaques on Cayo Santiago, we provide compelling evidence in a nonhuman animal for within-individual increases in social selectivity with age. Our analyses revealed that adult female macaques actively reduced the size of their networks as they aged and focused on partners previously linked to fitness benefits, including kin and partners to whom they were strongly and consistently connected earlier in life. Females spent similar amounts of time socializing as they aged, suggesting that network shrinkage does not result from lack of motivation or ability to engage, nor was this narrowing driven by the deaths of social partners. Furthermore, females remained attractive companions and were not isolated by withdrawal of social partners. Taken together, our results provide rare empirical evidence for social selectivity in nonhumans, suggesting that patterns of increasing selectivity with age may be deeply rooted in primate evolution.
Abstract.
Hart JDA, Franks DW, Brent LJN, Weiss MN (2021). Accuracy and power analysis of social networks built from count data.
Methods in Ecology and Evolution,
13(1), 157-166.
Abstract:
Accuracy and power analysis of social networks built from count data
Abstract
Power analysis is used to estimate the probability of correctly rejecting a null hypothesis for a given statistical model and dataset. Conventional power analyses assume complete information, but the stochastic nature of behavioural sampling can mean that true and estimated networks are poorly correlated. Power analyses do not currently take the effect of sampling into account. This could lead to inaccurate estimates of statistical power, potentially yielding misleading results.
Here we develop a method for computing network correlation: the correlation between an estimated social network and its true network, using a Gamma–Poisson model of social event rates for networks constructed from count data. We use simulations to assess how the level of network correlation affects the power of nodal regression analyses. We also develop a generic method of power analysis applicable to any statistical test, based on the concept of diminishing returns.
We demonstrate that our network correlation estimator is both accurate and moderately robust to its assumptions being broken. We show that social differentiation, mean social event rate and the harmonic mean of sampling times positively impacts the strength of network correlation. We also show that the required level of network correlation to achieve a given power level depends on many factors, but that 0.80 network correlation usually corresponds to around 80% power for nodal regression in ideal circumstances.
We provide guidelines for using our network correlation estimator to verify the accuracy of networks built from count data, and to conduct power analysis. This can be used prior to data collection, in post hoc analyses or even for subsetting networks in dynamic network analysis. The network correlation estimator and custom power analysis methods have been made available as an r package.
Abstract.
Allen C, Brent L, Thatayaone M, Croft D (2021). Field evidence supporting monitoring of chemical information on pathways by male African elephants. Animal Behaviour
Allen C, Croft D, Testard C, Brent L (2021). Function of trunk-mediated “greeting” behaviours between male African elephants: insights from choice of partners. Animals
Allen C, Croft DP, Brent LJN (2021). Reduced older male presence linked to increased rates of aggression to non-conspecific targets in male elephants. Proceedings of the Royal Society B: Biological Sciences
Testard C, Larson SM, Watowich MM, Kaplinsky CH, Bernau A, Faulder M, Marshall HH, Lehmann J, Ruiz-Lambides A, Higham JP, et al (2021). Rhesus macaques build new social connections after a natural disaster. Current Biology, 31(11), 2299-2309.e7.
Crisp RJ, Brent LJN, Carter GG (2021). Social dominance and cooperation in female vampire bats.
Royal Society Open Science,
8(7), 210266-210266.
Abstract:
Social dominance and cooperation in female vampire bats
When 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'sh’ 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.
Abstract.
Pavez-Fox MA, Negron-Del Valle JE, Thompson IJ, Walker CS, Bauman SE, Gonzalez O, Compo N, Ruiz-Lambides A, Martinez MI, Platt ML, et al (2021). Sociality predicts individual variation in the immunity of free-ranging rhesus macaques. Physiology & Behavior, 241, 113560-113560.
Grimes C, Brent L, Weiss M, Franks DW, Balcomb KC, Ellifrit DK, Ellis S, Croft D (2021). The effect of age, sex, and resource abundance on patterns of rake markings in resident killer whales (Orcinus orca). Marine Mammal Science
Weiss M, Franks DW, Brent L, Ellis S, Silk M, Croft D (2020). Common datastream permutations of animal social network data are not appropriate for hypothesis testing using regression models. Methods in Ecology and Evolution
Morrison RE, Eckardt W, Stoinski TS, Brent LJN (2020). Comparing measures of social complexity: larger mountain gorilla groups do not have a greater diversity of relationships.
Proceedings of the Royal Society B: Biological Sciences,
287(1931).
Abstract:
Comparing measures of social complexity: larger mountain gorilla groups do not have a greater diversity of relationships
Social complexity reflects the intricate patterns of social interactions in societies. Understanding social complexity is fundamental for studying the evolution of diverse social systems and the cognitive innovations used to cope with the demands of social life. Social complexity has been predominantly quantified by social unit size, but newer measures of social complexity reflect the diversity of relationships. However, the association between these two sets of measures remains unclear. We used 12 years of data on 13 gorilla groups to investigate how measures of social complexity relate to each other. We found that group size was a poor proxy for relationship diversity and that the social complexity individuals experienced within the same group varied greatly. Our findings demonstrate two fundamental takeaways: first, that the number of relationships and the diversity of those relationships represent separate components of social complexity, both of which should be accounted for; and second, that social complexity measured at the group level may not represent the social complexity experienced by individuals in those groups. These findings suggest that comprehensive studies of social complexity, particularly those relating to the social demands faced by individuals, may require fine-scale social data to allow accurate comparisons across populations and species.
Abstract.
Allen C, Brent L, Motsentwa T, Weiss M, Croft D (2020). Importance of Old Bulls: Leaders and Followers in Collective Movements of All-Male Groups in African Savannah Elephants (Loxodonta africana). Scientific Reports
Chiou KL, Montague MJ, Goldman EA, Watowich MM, Sams SN, Song J, Horvath JE, Sterner KN, Ruiz-Lambides AV, Martinez MI, et al (2020). Rhesus macaques as a tractable physiological model of human ageing. Philosophical Transactions of the Royal Society B: Biological Sciences
Ellis S, Snyder-Mackler N, Ruiz-Lambides A, Platt ML, Brent LJN (2019). Deconstructing sociality: the types of social connections that predict longevity in a group-living primate.
Proceedings of the Royal Society B: Biological Sciences,
286(1917), 20191991-20191991.
Abstract:
Deconstructing sociality: the types of social connections that predict longevity in a group-living primate
. Many species use social interactions to cope with challenges in their environment and a growing number of studies show that individuals which are well-connected to their group have higher fitness than socially isolated individuals. However, there are many ways to be ‘well-connected’ and it is unclear which aspects of sociality drive fitness benefits. Being well-connected can be conceptualized in four main ways: individuals can be socially integrated by engaging in a high rate of social behaviour or having many partners; they can have strong and stable connections to favoured partners; they can indirectly connect to the broader group structure; or directly engage in a high rate of beneficial behaviours, such as grooming. In this study, we use survival models and long-term data in adult female rhesus macaques (
. Macaca mulatta
. ) to compare the fitness outcomes of multiple measures of social connectedness. Females that maintained strong connections to favoured partners had the highest relative survival probability, as did females well-integrated owing to forming many weak connections. We found no survival benefits to being structurally well-connected or engaging in high rates of grooming. Being well-connected to favoured partners could provide fitness benefits by, for example, increasing the efficacy of coordinated or mutualistic behaviours.
.
Abstract.
Kimock CM, Dubuc C, Brent LJN, Higham JP (2019). Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate.
Scientific Reports,
9(1).
Abstract:
Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate
AbstractSexual 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.
Abstract.
Madlon-Kay S, Montague MJ, Brent LJN, Eliis S, Zhong B, Snyder-Mackler N, Horvath JE, Skene JHP, Platt ML (2018). Weak effects of common genetic variation in oxytocin and vasopressin receptor genes on rhesus macaque social behavior. American Journal of Primatology
Lacy RC, Williams R, Ashe E, Balcomb KC, Brent LJN, Clark CW, Croft DP, Giles DA, MacDuffee M, Paquet PC, et al (2017). Evaluating anthropogenic threats to endangered killer whales to inform effective recovery plans. Scientific Reports
Lacy RC, Williams R, Ashe E, Balcomb KC, Brent LJN, Clark CW, Croft DP, Giles DA, MacDuffee M, Paquet P, et al (2017). Evaluating anthropogenic threats to endangered killer whales to inform effective recovery plans. Scientific Reports
Brent LJN, Ruiz-Lambides A, Platt ML (2017). Family network size and survival across the lifespan of female macaques.
Proceedings of the Royal Society B: Biological Sciences,
284(1854), 20170515-20170515.
Abstract:
Family network size and survival across the lifespan of female macaques
Two decades of research suggest social relationships have a common evolutionary basis in humans and other gregarious mammals. Critical to the support of this idea is growing evidence that mortality is influenced by social integration, but when these effects emerge and how long they last is mostly unknown. Here, we report in adult female macaques that the impact of number of close adult female relatives, a proxy for social integration, on survival is not experienced uniformly across the life course; prime-aged females with a greater number of relatives had better survival outcomes compared with prime-aged females with fewer relatives, whereas no such effect was found in older females. Group size and dominance rank did not influence this result. Older females were less frequent targets of aggression, suggesting enhanced experience navigating the social landscape may obviate the need for social relationships in old age. Only one study of humans has found age-based dependency in the association between social integration and survival. Using the largest dataset for any non-human animal to date, our study extends support for the idea that sociality promotes survival and suggests strategies employed across the life course change along with experience of the social world.
Abstract.
Firth JA, Brent LJN, Sheldon BC (2017). Indirectly connected: simple social differences can explain the causes and apparent consequences of complex social network positions. Proceedings of the Royal Society B: Biological Sciences
Brent LJN (2017). Mammal societies.
ANIMAL BEHAVIOUR,
131, 43-43.
Author URL.
Brent LJN, Ruiz-Lambides A, Platt ML (2017). Persistent social isolation reflects identity and social context but not maternal effects or early environment. Scientific Reports
Croft DP, Johnstone RA, Ellis S, Nattrass S, Franks DW, Brent LJN, Mazzi S, Balcomb C, Ford JKB, Cant MA, et al (2017). Reproductive Conflict and the Evolution of Menopause in Killer Whales. Current Biology
Larson SM, Ruiz-Lambides A, Platt ML, Brent LJN (2017). Social network dynamics precede a mass eviction in group-living rhesus macaques. Animal Behaviour
Madlon-Kay S, Brent LJN, Montague M, Heller K, Platt ML (2017). Using Machine Learning to Discover Latent Social Phenotypes in Free-Ranging Macaques. Brain Sciences
Franks DW, Nattrass S, Brent LJN, Whitehead H, Foote AD, Mazzi S, Ford JKB, Balcomb KC, Cant MA, Croft DP, et al (2016). The significance of postreproductive lifespans in killer whales: a comment on Robeck et al. Journal of Mammalogy, gyw021-gyw021.
Boyland N, Mlynski DT, James R, Brent LJN, Croft DP (2016). The social network structure of a dynamic group of dairy cows: from individual to group level patterns.
Applied Animal Behaviour ScienceAbstract:
The social network structure of a dynamic group of dairy cows: from individual to group level patterns
Social relationships have been shown to significantly impact individual and group success in wild animal populations, but are largely ignored in farm animal management. There are substantial gaps in our knowledge of how farm animals respond to their social environment, which varies greatly between farms but is commonly unstable due to regrouping. Fundamental to addressing these gaps is an understanding of the social network structure resulting from the patterning of relationships between individuals in a group. Here, we investigated the social structure of a group of 110 lactating dairy cows during four one-month periods. Spatial proximity loggers collected data on associations between cows, allowing us to construct social networks. First we demonstrate that proximity loggers can be used to measure relationships between cows; proximity data was significantly positively correlated to affiliative interactions but had no relationship with agonistic interactions. We measured group-level patterns by testing for community structure, centralisation and repeatability of network structure over time. We explored individual-level patterns by measuring social differentiation (heterogeneity of social associations) and assortment of cows in the network by lactation number, breed, gregariousness and milk production. There was no evidence that cows were subdivided into social communities; individuals belonged to a single cluster and networks showed significant centralisation. Repeatability of the social network was low, which may have consequences for animal welfare. Individuals formed differentiated social relationships and there was evidence of positive assortment by traits; cows associated more with conspecifics of similar lactation number in all study periods. There was also positive assortment by breed, gregariousness and milk production in some study periods. There is growing interest in the farming industry in the impact of social factors on production and welfare; this study takes an important step towards understanding social dynamics.
Abstract.
Brent LJN, Franks DW, Foster EA, Balcomb KC, Cant MA, Croft DP (2015). Ecological Knowledge, Leadership, and the Evolution of Menopause in Killer Whales EDITORIAL COMMENT.
OBSTETRICAL & GYNECOLOGICAL SURVEY,
70(11), 701-702.
Author URL.
Brent LJN, Franks DW, Foster EA, Balcomb KC, Cant MA, Croft DP (2015). Ecological knowledge, leadership, and the evolution of menopause in killer whales. Current Biology, 25(6), 746-750.
Brent LJN (2015). Friends of friends: Are indirect connections in social networks important to animal behaviour?. Animal Behaviour, 103, 211-222.
Watson KK, Li D, Brent LJN, Horvath JE, Gonzalez-Martinez J, Ruiz-Lambides AV, Robinson AG, Skene JHP, Platt MLP (2015). Genetic influences on social attention in free-ranging rhesus macaques. Animal Behaviour, 103, 267-275.
Croft DP, Brent LJN, Franks DW, Cant MA (2015). The evolution of prolonged life after reproduction.
Trends in Ecology and EvolutionAbstract:
The evolution of prolonged life after reproduction
Why females of some species cease ovulation before the
end of their natural lifespan is a longstanding evolutionary
puzzle. For many species in captivity, post-reproductive
life is simply an epiphenomenon of lengthened
lifespan. Yet in natural populations of humans as well
as some cetaceans and insects, reproductive senescence
occurs much faster than somatic aging and females
exhibit prolonged post-reproductive lifespans (PRLSs).
Determining the mechanisms and functions that underpin
PRLSs has proved a significant challenge. Here we
bring together both classic and modern hypotheses
proposed to explain PRLSs and discuss their application
to both human and nonhuman animals. By taking an
integrative and broad taxonomic approach we highlight
the need to consider multiple interacting explanations
for the evolution of PRLSs.
Abstract.
Croft DP, Brent LJN, Franks DW, Cant MA (2015). The evolution of prolonged life after reproduction.
Trends in Ecology and Evolution,
30(7), 407-416.
Abstract:
The evolution of prolonged life after reproduction
© 2015 the Authors. Why females of some species cease ovulation before the end of their natural lifespan is a longstanding evolutionary puzzle. For many species in captivity, post-reproductive life is simply an epiphenomenon of lengthened lifespan. Yet in natural populations of humans as well as some cetaceans and insects, reproductive senescence occurs much faster than somatic aging and females exhibit prolonged post-reproductive lifespans (PRLSs). Determining the mechanisms and functions that underpin PRLSs has proved a significant challenge. Here we bring together both classic and modern hypotheses proposed to explain PRLSs and discuss their application to both human and nonhuman animals. By taking an integrative and broad taxonomic approach we highlight the need to consider multiple interacting explanations for the evolution of PRLSs.
Abstract.
Brent L (2014). A rewarding relationship. New Scientist, 222(2970), 37-39.
Blomquist GE, Brent LJN (2014). Applying Quantitative Genetic Methods to Primate Social Behavior.
International Journal of Primatology,
35(1), 108-128.
Abstract:
Applying Quantitative Genetic Methods to Primate Social Behavior
Increasingly, behavioral ecologists have applied quantitative genetic methods to investigate the evolution of behaviors in wild animal populations. The promise of quantitative genetics in unmanaged populations opens the door for simultaneous analysis of inheritance, phenotypic plasticity, and patterns of selection on behavioral phenotypes all within the same study. In this article, we describe how quantitative genetic techniques provide studies of the evolution of behavior with information that is unique and valuable. We outline technical obstacles for applying quantitative genetic techniques that are of particular relevance to studies of behavior in primates, especially those living in noncaptive populations, e.g. the need for pedigree information, non-Gaussian phenotypes, and demonstrate how many of these barriers are now surmountable. We illustrate this by applying recent quantitative genetic methods to spatial proximity data, a simple and widely collected primate social behavior, from adult rhesus macaques on Cayo Santiago. Our analysis shows that proximity measures are consistent across repeated measurements on individuals (repeatable) and that kin have similar mean measurements (heritable). Quantitative genetics may hold lessons of considerable importance for studies of primate behavior, even those without a specific genetic focus. © 2013 Springer Science+Business Media New York.
Abstract.
Brent LJN, Semple S, MacLarnon A, Ruiz-Lambides A, Gonzalez-Martinez J, Platt ML (2014). Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output.
International Journal of Primatology,
35(1), 188-209.
Abstract:
Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output
There is growing evidence that behavioral tendencies, or "personalities," in animals are an important aspect of their biology, yet their evolutionary basis is poorly understood. Specifically, how individual variation in personality arises and is subsequently maintained by selection remains unclear. To address this gap, studies of personality require explicit incorporation of genetic information. Here, we explored the genetic basis of personality in rhesus macaques by determining the heritability of personality components and by examining the fitness consequences of those components. We collected observational data for 108 adult females living in three social groups in a free-ranging population via focal animal sampling. We applied principal component analysis to nine spontaneously occurring behaviors and identified six putative personality components, which we named Meek, Bold, Aggressive, Passive, Loner, and Nervous. All components were repeatable and heritable, with heritability estimates ranging from 0.14 to 0.35. We found no evidence of an association with reproductive output, measured either by infant survival or by interbirth interval, for any of the personality components. This finding suggests either that personality does not have fitness-related consequences in this population or that selection has acted to reduce fitness-associated variation in personality. © 2013 Springer Science+Business Media New York.
Abstract.
Dubuc C, Winters S, Allen WL, Brent LJN, Casio J, Maestripieri D, Ruiz-Lambides AV, Widdig A, Higham JP (2014). Sexually selected skin color is heritable and related to fitness in a non-human primate. Proceedings of the Royal Society of London: Biological Sciences, 281, 20141602-20141602.
Brent LJN, Melin AD (2014). The Genetic Basis of Primate Behavior: Genetics and Genomics in Field-Based Primatology. International Journal of Primatology, 35(1), 1-10.
MacLean EL, Hare B, Nun CL, Addess E, Amic F, Anderson RC, Aureli F, Baker JM, Bania AE, Barnard AM, et al (2014). The evolution of self-control.
Proceedings of the National Academy of Sciences of the United States of America,
111(20).
Abstract:
The evolution of self-control
Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.
Abstract.
Brent LJN, Chang SW, Gariepy JF, Platt ML (2014). The neuroethology of friendship. Annals of the New York Academy of Sciences, 1316, 1-17.
Gilby IC, Brent LJN, Wroblewski EE, Rudicell RS, Hahn BH, Goodall J, Pusey AE (2013). Fitness benefits of coalitionary aggression in male chimpanzees.
Behavioral Ecology and Sociobiology,
67(3), 373-381.
Abstract:
Fitness benefits of coalitionary aggression in male chimpanzees
Coalitionary aggression occurs when at least two individuals jointly direct aggression at one or more conspecific targets. Scientists have long argued that this common form of cooperation has positive fitness consequences. Nevertheless, despite evidence that social bond strength (which is thought to promote coalition formation) is correlated with fitness in primates, cetaceans, and ungulates, few studies have directly examined whether coalitionary aggression improves reproductive success. We tested the hypothesis that among free-ranging chimpanzees (Pan troglodytes schweinfurthii), participation in coalitionary aggression increases reproductive output. Using 14 years of genetic and behavioral data from Gombe National Park, Tanzania, we found that coalitionary aggression increased a male's chances of (A) siring offspring, compared to other males of similar dominance rank, and (B) ascending in rank, a correlate of future reproductive output. Because male chimpanzees form coalitions with many others within a complex network, we used social network analysis to identify the types of connections correlated with these fitness benefits. The beneficiaries of coalitionary aggression were males with the highest "betweenness"-that is, those who tended to have coalition partners who themselves did not form coalitions with each other. This suggests that beyond simply recognizing third-party relationships, chimpanzees may use this knowledge to choose coalition partners. If so, this is a significant step forward in our knowledge of the adaptive value of social intelligence. Regardless of mechanism, however, this is the first evidence of genetic benefits of coalitionary aggression in this species, and therefore has important implications for understanding the evolution of cooperation. © 2012 Springer-Verlag Berlin Heidelberg.
Abstract.
Brent LJN, Heilbronner SR, Horvath JE, Gonzalez-Martinez J, Ruiz-Lambides A, Robinson AG, Pate Skene JH, Platt ML (2013). Genetic origins of social networks in rhesus macaques.
Scientific Reports,
3Abstract:
Genetic origins of social networks in rhesus macaques
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.
Abstract.
Chang SW, Brent LJN, Adams GK, Pearson J, Klein J, Watson KK, Platt ML (2013). Neuroethology of primate social behavior. Proceedings of the National Academy of Sciences of USA, 110, 10387-10394.
Dobson SD, Brent LJN (2013). On the evolution of the serotonin transporter linked polymorphic region (5-HTTLPR) in primates.
Frontiers in Human Neuroscience(NOV).
Abstract:
On the evolution of the serotonin transporter linked polymorphic region (5-HTTLPR) in primates
Some allelic variants of the serotonin transporter linked polymorphic region (5-HTTLPR) result in lower levels of expression of the serotonin transporter gene (SLC6A4). These low-expressing (LE) alleles are associated with mental-health disorders in a minority of humans that carry them. Humans are not the only primates that exhibit this polymorphism; other species, including some monkeys, also have LE and high-expressing (HE) variants of 5-HTTLPR. We propose a behavioral genetic framework to explain the adaptive evolution of this polymorphism in primates, including humans. We hypothesize that both LE and HE alleles are maintained by balancing selection in species characterized by short-term fluctuations in social competition levels. More specifically, we propose that LE carriers benefit from their hypervigilant tendencies during periods of elevated competition, whereas HE homozygotes cope best when competition levels do not deviate from the norm. Thus, both alleles have long-term benefits when competition levels tend to vary substantially over relatively short timescales within a social group. We describe this hypothesis in detail and outline a series of predictions to test it. Some of these predictions are supported by findings in the current literature, while others remain areas of future research. © 2013 Dobson and Brent.
Abstract.
Brent LJN, Semple S, MacLarnon A, Ruiz-Lambides A, Gonzalez-Martinez J, Platt ML (2013). Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output. International Journal of Primatology, 1-22.
Brent LJN, MacLarnon A, Platt ML, Semple S (2013). Seasonal changes in the structure of rhesus macaque social networks.
Behavioral Ecology and Sociobiology,
67(3), 349-359.
Abstract:
Seasonal changes in the structure of rhesus macaque social networks
Social structure emerges from the patterning of interactions between individuals and plays a critical role in shaping some of the main characteristics of animal populations. The topological features of social structure, such as the extent to which individuals interact in clusters, can influence many biologically important factors, including the persistence of cooperation, and the rate of spread of disease. Yet, the extent to which social structure topology fluctuates over relatively short periods of time in relation to social, demographic, or environmental events remains unclear. Here, we use social network analysis to examine seasonal changes in the topology of social structures that emerge from socio-positive associations in adult female rhesus macaques (Macaca mulatta). Behavioral data for two different association types (grooming and spatial proximity) were collected for females in two free-ranging groups during two seasons: the mating and birth seasons. Stronger dyadic bonds resulted in social structures that were more tightly connected (i. e. of greater density) in the mating season compared to the birth season. Social structures were also more centralized around a subset of individuals and more clustered in the mating season than those in the birth season, although the latter differences were mostly driven by differences in density alone. Our results suggest a degree of temporal variation in the topological features of social structure in this population. Such variation may feed back on interactions, hence affecting the behaviors of individuals, and may therefore be important to take into account in studies of animal behavior. © 2012 Springer-Verlag Berlin Heidelberg.
Abstract.
Brent LJN, Melin AD (2013). The Genetic Basis of Primate Behavior: Genetics and Genomics in Field-Based Primatology. International Journal of Primatology, 1-10.
Buhl JS, Aure B, Ruiz-Lambides A, Gonzalez-Martinez J, Platt ML, Brent LJN (2012). Response of Rhesus Macaques (Macaca mulatta) to the Body of a Group Member That Died from a Fatal Attack.
International Journal of Primatology,
33(4), 860-871.
Abstract:
Response of Rhesus Macaques (Macaca mulatta) to the Body of a Group Member That Died from a Fatal Attack
Among animals that form social bonds, the death of a conspecific may be a significant social event, representing the loss of an ally and resulting in disruptions to the dominance hierarchy. Despite this potential biological importance, we have only limited knowledge of animals' reactions to the death of a group member. This is particularly true of responses to dead adults, as most reports describe the responses of mothers to dead infants. Here, we describe in detail and provide video evidence of the behavioral responses of a group of free-ranging rhesus macaques (Macaca mulatta) immediately after the death of a mid-ranking adult male as a result of a fatal attack. High-ranking male members of the group, suspected to have carried out the attack, dragged and bit the dead body, exhibiting a rate of aggression 20 times greater than baseline levels. Lower-ranking individuals approached and inspected the body by looking closely, smelling, and grooming the fur. There was inconclusive evidence that these rhesus macaques found the death of a conspecific stressful: Levels of grooming between group members after the fatal attack were significantly higher than baseline levels, and higher than levels of grooming after nonfatal attacks. However, when grooming levels were adjusted based on the assumption that individuals positioned close to the body, i. e. those visible to researchers, were more likely to be engaged in grooming than those positioned farther away, this difference from baseline was no longer significant. The rate of self-directed behaviors after the fatal attack was also not different from baseline. Many of the behaviors we observed directed toward the body (aggression, inspection) have been previously reported in chimpanzees and geladas, and are similar to reactions sometimes displayed by humans. As such, this report represents a potentially valuable contribution the nascent field of nonhuman primate thanatology. © 2012 Springer Science+Business Media, LLC.
Abstract.
Higham JP, Hughes KD, Brent LJN, Dubuc C, Engelhardt A, Heistermann M, Maestriperi D, Santos LR, Stevens M (2011). Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques.
Proceedings of the Royal Society B: Biological Sciences,
278(1723), 3452-3458.
Abstract:
Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques
Animals signal their reproductive status in a range of sensory modalities. Highly social animals, such as primates, have access not only to such signals, but also to prior experience of other group members. Whether this experience affects how animals interpret reproductive signals is unknown. Here, we explore whether familiarity with a specific female affects a male's ability to assess that female's reproductive signals. We used a preferential looking procedure to assess signal discrimination in free-ranging rhesus macaques, a species in which female facial luminance covaries with reproductive status. We collected images of female faces throughout the reproductive cycle, and using faecal hormone analysis to determine ovulation, categorized images as coming from a female's pre-fertile, ovulating, or post-fertile period. Weprinted colour-calibrated stimuli of these faces, reproducing stimuli perceptually the same in colour and luminance to the original appearance of females. These images were presented to males who were either unfamiliar or familiar with stimuli females. Overall, males distinguished ovulatory from pre-ovulatory faces. However, a significant proportion of males did so only among males familiar with stimuli females. These experiments demonstrate that familiarity may increase a receiver's ability to use a social partner's signals to discern their reproductive status. © 2011 the Royal Society.
Abstract.
Brent LJN, Semple S, Dubuc C, Heistermann M, MacLarnon A (2011). Social capital and physiological stress levels in free-ranging adult female rhesus macaques.
Physiology and Behavior,
102(1), 76-83.
Abstract:
Social capital and physiological stress levels in free-ranging adult female rhesus macaques
Social animals with greater access to social support, i.e. higher levels of social capital, may be able to cope better with the challenges they face in their day-to-day lives, and this may be reflected in lower physiological stress levels. Here, we examine the relationship between social capital and fecal glucocorticoid (GC) levels in pregnant free-ranging adult female rhesus macaques. In addition to social capital measures based on direct connections between social partners, which have been examined previously, we use social network analysis to generate measures of social capital based on indirect connections (i.e. connections between pairs of individuals which result from their mutual direct connection to a third party). We consider social capital based on three different types of affiliative association: grooming, the exchange of affiliative vocalizations and proximity. After controlling for variables known to affect GC output in primates (e.g. month of pregnancy), GC levels of females were significantly predicted by a social network measure of indirect connectedness in the proximity network, proximity reach, in interaction with dominance rank. High ranking females had significantly lower GC levels in months in which they had low levels of proximity reach (i.e. in months in which their proximity networks were smaller and therefore more focused). The results of our study add to a growing body of evidence which suggests that social capital may be an important means by which gregarious animals cope with day-to-day challenges. Our study also joins a small body of recent research which has demonstrated that indirect connections may be important factors in the lives of social animals. © 2010 Elsevier Inc.
Abstract.
Brent LJN, Lehmann J, Ramos-Fernandez G (2011). Social networks in the study of nonhuman primates: a historical perspective. American Journal of Primatology(73), 720-730.
Higham JP, Brent LJN, Dubuc C, Accamando AK, Engelhardt A, Gerald MS, Heistermann M, Stevens M (2010). Color signal information content and the eye of the beholder: a case study in the rhesus macaque.
Behavioral Ecology,
21(4), 739-746.
Abstract:
Color signal information content and the eye of the beholder: a case study in the rhesus macaque
Animal coloration has provided many classical examples of both natural and sexual selection. Methods to study color signals range from human assessment to models of receiver vision, with objective measurements commonly involving spectrometry or digital photography. However, signal assessment by a receiver is not objective but linked to receiver perception. Here, we use standardized digital photographs of female rhesus macaque (Macaca mulatta) face and hindquarter regions, combined with estimates of the timing of the female fertile phase, to assess how color varies with respect to this timing. We compare objective color measures (camera sensor responses) with models of rhesus vision (retinal receptor stimulation and visual discriminability). Due to differences in spectral separation between camera sensors and rhesus receptors, camera measures overestimated color variation and underestimated luminance variation compared with rhesus macaques. Consequently, objective digital camera measurements can produce statistically significant relationships that are probably undetectable to rhesus macaques, and hence biologically irrelevant, while missing variation in the measure that may be relevant. Discrimination modeling provided results that were most meaningful (as they were directly related to receiver perception) and were easiest to relate to underlying physiology. Further, this gave new insight into the function of such signals, revealing perceptually salient signal luminance changes outside of the fertile phase that could potentially enhance paternity confusion. Our study demonstrates how, even for species with similar visual systems to humans, models of vision may provide more accurate and meaningful information on the form and function of visual signals than objective color measures do. © the Author 2010.
Abstract.
Dubuc C, Brent LJN, Accamando AK, Gerald MS, MacLarnon A, Semple S, Heistermann M, Engelhardt A (2009). Sexual skin color contains information about the timing of the fertile phase in free-ranging macaca mulatta.
International Journal of Primatology,
30(6), 777-789.
Abstract:
Sexual skin color contains information about the timing of the fertile phase in free-ranging macaca mulatta
Females of several primate species undergo cyclical changes of their sexual skin, i.e. the development of a swelling or a change in color. The relationship between intracycle probability of fertility and the size of sexual swellings is well established, but in the only study to combine an objective measure of color with endocrinological data, researchers found no evidence that swelling color contains such information. To evaluate the role of female skin color in the context of sexual signaling further, we investigated whether changes in sexual skin color contain information about the timing of the fertile phase in rhesus macaques (Macaca mulatta), a species in which adult females do not develop sexual swellings, but do express visually detectable changes in the skin color of the face and hindquarters. Using an objective and quantitative measure of color, along with detailed data on fecal progestogen and estrogen metabolite levels collected from 8 females of the Cayo Santiago colony, we show that the ratio of red to green (R/G) for facial and hindquarter skin significantly varies throughout the ovarian cycle. In addition, facial skin R/G is significantly higher during the 5-d fertile phase versus the 5-d periods immediately before or after this time, but no such pattern occurs in hindquarter R/G. This suggests that skin color change in female rhesus macaques may potentially signal information about the intracycle probability of fertility to male receivers, but that only facial skin color may signal reliable information about its timing. © 2009 Springer Science+Business Media, LLC.
Abstract.
Brent LJN, Teichroeb JA, Sicotte P (2008). Preliminary assessment of natal attraction and infant handling in wild Colobus vellerosus. American Journal of Primatology, 70(1), 101-105.
Brent LJN, Drapeau P (2002). Targeted 'knockdown' of channel expression in vivo with an antisense morpholino oligonucleotide.
Neuroscience,
114(2), 275-278.
Abstract:
Targeted 'knockdown' of channel expression in vivo with an antisense morpholino oligonucleotide
We have examined whether antisense morpholino oligonucleotides (morpholinos) can be used as a tool to suppress or 'knockdown' the expression of ion channels during development of the zebrafish. Because the acetylcholine receptor channel is well characterized in zebrafish and is abundant as skeletal muscle is found throughout the body, we sought to knock down its expression as a general test of the feasibility of this approach. A 25-mer morpholino was designed to target the 5′ region of the cloned α-subunit and was injected into early stage blastulae in order to trap it in all developing cells. From the time of hatching (early on the third day of development) and for a few days after, a fraction of the injected embryos were immobile, i.e. were 'morphant'. Injection of blastulae without the morpholino or with a control morpholino containing four mispaired bases did not affect the embryos. Although the morphant embryos were generally normal in appearance, they lacked staining with α-bungarotoxin or an α-subunit-specific monoclonal antibody. In whole muscle cell recordings from morphant embryos, miniature end-plate potentials were undetectable in many of the cells and in most they had a slower, immature time course. These results are consistent with a greatly reduced, dysfunctional level of expression of acetylcholine receptors in morphant embryos. Because of their stability and specificity, morpholinos should prove useful for targeted deletion of transmitter receptors and channels in developing zebrafish and possibly in other preparations. © 2002 IBRO. Published by Elsevier Science Ltd. All rights reserved.
Abstract.
Chapters
Pavelka MSM, Brent LJN, Croft DP, Fedigan LM (2018). Post-fertile Lifespan in Female Primates and Cetaceans. In Kalbitzer U, Jack K (Eds.) Primate Life Histories, Sex Roles, and Adaptability. Developments in Primatology: Progress and Prospects, Springer, Cham.
Publications by year
In Press
Goldman EA, Chiou KL, Watowich MM, Mercer A, Sams SN, Horvath JE, Anderson JA, Tung J, Higham JP, Brent LJN, et al (In Press). A generalizable epigenetic clock captures aging in two nonhuman primates.
Abstract:
A generalizable epigenetic clock captures aging in two nonhuman primates
ABSTRACTEpigenetic clocks generated from DNA methylation array data provide important insights into biological aging, disease susceptibility, and mortality risk. However, these clocks cannot be applied to high-throughput, sequence-based datasets more commonly used to study nonhuman animals. Here, we built a generalizable epigenetic clock using genome-wide DNA methylation data from 493 free-ranging rhesus macaques. Using a sliding-window approach that maximizes generalizability across datasets and species, this model predicted age with high accuracy (± 1.42 years) in held-out test samples, as well as in two independent test sets: rhesus macaques from a captive population (n=43) and wild baboons in Kenya (n=271). Our model can also be used to generate insight into the factors hypothesized to alter epigenetic aging, including social status and exposure to traumatic events. Our results thus provide a flexible tool for predicting age in other populations and species and illustrate how connecting behavioral data with the epigenetic clock can uncover social influences on biological age.
Abstract.
Hart JDA, Franks DW, Brent LJN, Weiss MN (In Press). Accuracy and Power Analysis of Social Networks Built from Count Data.
Abstract:
Accuracy and Power Analysis of Social Networks Built from Count Data
AbstractPower analysis is used to estimate the probability of correctly rejecting a null hypothesis for a given statistical model and dataset. Conventional power analyses assume complete information, but the stochastic nature of behavioural sampling can mean that true and estimated networks are poorly correlated. Power analyses do not currently take the effect of sampling into account. This could lead to inaccurate estimates of statistical power, potentially yielding misleading results.Here we develop a method for computing network correlation: the correlation between an estimated social network and its true network, using a Gamma-Poisson model of social event rates for networks constructed from count data. We use simulations to assess how the level of network correlation affects the power of nodal regression analyses. We also develop a generic method of power analysis applicable to any statistical test, based on the concept of diminishing returns.We demonstrate that our network correlation estimator is both accurate and moderately robust to its assumptions being broken. We show that social differentiation, mean social event rate, and the harmonic mean of sampling times positively impacts the strength of network correlation. We also show that the required level of network correlation to achieve a given power level depends on many factors, but that 0.80 network correlation usually corresponds to around 0.80 power for nodal regression in ideal circumstances.We provide guidelines for using our network correlation estimator to verify the accuracy of networks built from count data, and to conduct power analysis. This can be used prior to data collection, in post hoc analyses, or even for subsetting networks in dynamic network analysis. The network correlation estimator and custom power analysis methods have been made available as an R package.
Abstract.
Fernandes AG, Alexopoulos P, Burgos-Rodriguez A, Martinez MI, Ghassibi M, Leskov I, Brent LJN, Snyder-Mackler N, Danias J, Wollstein G, et al (In Press). Age-related differences in ocular features of a naturalistic free-ranging population of rhesus macaques.
Abstract:
Age-related differences in ocular features of a naturalistic free-ranging population of rhesus macaques
ABSTRACTPurposeRhesus macaques (Macaca mulatta) are the premier nonhuman primate model for studying human health and disease. We aimed to investigate if age was associated with ocular features of clinical relevance in a large cohort of free-ranging rhesus macaques from Cayo Santiago, Puerto Rico.MethodsWe evaluated 120 rhesus macaques (73 males, 47 females) aged from 0 to 29 years old (mean±SD: 12.6±6.4) from September to December, 2021. The ophthalmic evaluation included IOP assessment, corneal pachymetry, anterior segment biomicroscopy, A-Scan biometry, automated refraction, and fundus photography after pupil dilation. The effects of age on the outcome variables were investigated through multilevel mixed-effects models adjusted for sex and weight.ResultsOn average, IOP, pachymetry, axial length, and automated refraction spherical equivalent were 15.47±2.47 mmHg, 474.43±32.21 μm, 19.49±1.24 mm, and 0.30±1.70 D, respectively. Age was significantly associated with pachymetry (Coef.= -1.20; 95%CI: -2.27 to -0.14; p=0.026), axial length (Coef.= 0.03; 95%CI: 0.01 to 0.05; p=0.002), and spherical equivalent (Coef.= -0.12; 95%CI: -0.22 to -0.02; p=0.015). No association was detected between age and IOP. The prevalence of cataracts in either eye was 10.83% (95% CI: 6.34 – 17.89%) and was significantly associated with age (OR= 1.20; 95%CI: 1.06 – 1.36; p=0.004). Retinal drusen in either eye was observed in 15.00% (95% CI: 9.60 – 22.68%) of the animals, which was also significantly associated with age (OR=1.14; 95%CI: 1.02 – 1.27; p=0.020).ConclusionsRhesus macaques exhibit age-related ocular associations similar to those observed in human aging, including decreased corneal thickness, increased axial length, myopic shift, and higher occurrence of cataract and retinal drusen.
Abstract.
Siracusa ER, Pereira AS, Brask JB, Negron-Del Valle JE, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (In Press). Ageing in a collective: the impact of ageing individuals on social network structure.
Abstract:
Ageing in a collective: the impact of ageing individuals on social network structure
AbstractAgeing affects many phenotypic traits, but its consequences for social behaviour have only recently become apparent. Social networks emerge from associations between individuals. The changes in sociality that occur as individuals get older are thus likely to impact network structure, yet this remains unstudied. Here we use empirical data from free-ranging rhesus macaques and an agent-based model to test how age-based changes in social behaviour feed up to influence: (1) an individual’s level of indirect connectedness in their network; and (2) overall patterns of network structure. Our empirical analyses revealed that female macaques became less indirectly connected as they aged for some, but not all network measures examined, suggesting that indirect connectivity is affected by ageing, and that ageing animals can remain well integrated in some social contexts. Surprisingly, we did not find evidence for a relationship between age distribution and the structure of female macaque networks. We used an agent-based model to gain further understanding of the link between age-based differences in sociality and global network structure, and under which circumstances global effects may be detectable. Overall, our results suggest a potentially important and underappreciated role of age in the structure and function of animal collectives, which warrants further investigation.
Abstract.
Hart JDA, Weiss MN, Franks DW, Brent LJN (In Press). BISoN: a Bayesian Framework for Inference of Social Networks.
Abstract:
BISoN: a Bayesian Framework for Inference of Social Networks
AbstractSocial networks are often constructed from point estimates of edge weights. In many contexts, edge weights are inferred from observational data, and the uncertainty around estimates can be affected by various factors. Though this has been acknowledged in previous work, methods that explicitly quantify uncertainty in edge weights have not yet been widely adopted, and remain undeveloped for many common types of data. Furthermore, existing methods are unable to cope with some of the complexities often found in observational data, and do not propagate uncertainty in edge weights to subsequent statistical analyses.We introduce a unified Bayesian framework for modelling social networks based on observational data. This framework, which we call BISoN, can accommodate many common types of observational social data, can capture confounds and model effects at the level of observations, and is fully compatible with popular methods used in social network analysis.We show how the framework can be applied to common types of data and how various types of downstream statistical analyses can be performed, including non-random association tests and regressions on network properties.Our framework opens up the opportunity to test new types of hypotheses, make full use of observational datasets, and increase the reliability of scientific inferences. We have made example R scripts available to enable adoption of the framework.
Abstract.
De Moor D, Skelton M, Schülke O, Ostner J, Neumann C, Duboscq J, Brent LJN (In Press). MacaqueNet: big-team research into the biological drivers of social relationships.
Abstract:
MacaqueNet: big-team research into the biological drivers of social relationships
AbstractFor many animals, social relationships are a key determinant of fitness. However, major gaps remain in our understanding of the adaptive function, ontogeny, evolution, and mechanistic underpinnings of social relationships. There is a vast and ever-accumulating amount of social behavioural data on individually recognised animals, an incredible resource to shed light onto the biological basis of social relationships. Yet, the full potential of such data lies in comparative research across taxa with distinct life histories and ecologies. Substantial challenges impede systematic comparisons, one of which is the lack of persistent, accessible, and standardised databases.Here, we advocate for the creation of big-team collaborations and comparative databases to unlock the wealth of behavioural data for research on social relationships by introducing MacaqueNet (https://macaquenet.github.io/).As a global collaboration of over 100 researchers, the MacaqueNet database encompasses data from 1981 to the present on 14 species and is the first publicly searchable and standardised database on affiliative and agonistic animal social networks. With substantial inter-specific variation in ecology and social structure and the first published record on macaque behaviour dating back to 1956, macaque research has already contributed to answering fundamental questions on the biological bases and evolution of social relationships. Building on these strong foundations, we believe that MacaqueNet can further promote collaborative and comparative research on social behaviour.We believe that big-team approaches to building standardised databases, bringing together data contributors and researchers, will aid much-needed large-scale comparative research in behavioural ecology and beyond. We describe the establishment of MacaqueNet, from starting a large-scale collective to the creation of a cross-species collaborative database and the implementation of data entry and retrieval protocols. As such, we hope to provide a functional example for future endeavours of large-scale collaborative research into the biology of social behaviour.
Abstract.
2023
Fernandes AG, Alexopoulos P, Burgos-Rodriguez A, Martinez MI, Ghassibi M, Leskov I, Brent LJN, Snyder-Mackler N, Danias J, Wollstein G, et al (2023). Age-Related Differences in Ocular Features of a Naturalistic Free-Ranging Population of Rhesus Macaques. Investigative Opthalmology & Visual Science, 64(7), 3-3.
Siracusa ER, Pereira AS, Brask JB, Negron-Del Valle JE, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (2023). Ageing in a collective: the impact of ageing individuals on social network structure.
Philosophical Transactions of the Royal Society B: Biological Sciences,
378(1874).
Abstract:
Ageing in a collective: the impact of ageing individuals on social network structure
Ageing affects many phenotypic traits, but its consequences for social behaviour have only recently become apparent. Social networks emerge from associations between individuals. The changes in sociality that occur as individuals get older are thus likely to impact network structure, yet this remains unstudied. Here we use empirical data from free-ranging rhesus macaques and an agent-based model to test how age-based changes in social behaviour feed up to influence: (i) an individual's level of indirect connectedness in their network and (ii) overall patterns of network structure. Our empirical analyses revealed that female macaques became less indirectly connected as they aged for some, but not for all network measures examined. This suggests that indirect connectivity is affected by ageing, and that ageing animals can remain well integrated in some social contexts. Surprisingly, we did not find evidence for a relationship between age distribution and the structure of female macaque networks. We used an agent-based model to gain further understanding of the link between age-based differences in sociality and global network structure, and under which circumstances global effects may be detectable. Overall, our results suggest a potentially important and underappreciated role of age in the structure and function of animal collectives, which warrants further investigation.
. This article is part of a discussion meeting issue ‘Collective behaviour through time’.
Abstract.
Hart J, Weiss MN, Franks D, Brent L (2023). BISoN: a Bayesian framework for inference of social networks.
Methods in Ecology and Evolution,
14(9), 2411-2420.
Abstract:
BISoN: a Bayesian framework for inference of social networks
Abstract
Animal social networks are often constructed from point estimates of edge weights. In many contexts, edge weights are inferred from observational data, and the uncertainty around estimates can be affected by various factors. Though this has been acknowledged in previous work, methods that explicitly quantify uncertainty in edge weights have not yet been widely adopted and remain undeveloped for many common types of data. Furthermore, existing methods are unable to cope with some of the complexities often found in observational data, and do not propagate uncertainty in edge weights to subsequent statistical analyses.
We introduce a unified Bayesian framework for modelling social networks based on observational data. This framework, which we call BISoN, can accommodate many common types of observational social data, can capture confounds and model effects at the level of observations and is fully compatible with popular methods used in social network analysis.
We show how the framework can be applied to common types of data and how various types of downstream statistical analyses can be performed, including non‐random association tests and regressions on network properties.
Our framework opens up the opportunity to test new types of hypotheses, make full use of observational datasets, and increase the reliability of scientific inferences. We have made both an R package and example R scripts available to enable adoption of the framework.
Abstract.
Hart J (2023). Bayesian Methods for Animal Social Network Analysis.
Abstract:
Bayesian Methods for Animal Social Network Analysis
Over the last two decades, animal social network analysis has become central in the study of animal social systems. This methodology has given researchers a powerful set of tools to ask deep questions about the social structures of animals, and how these are linked to many other important biological processes. Animal social networks are often constructed from noisy, uncertain data, which would be well-suited to a Bayesian statistical philosophy. However, despite recent advances in Bayesian methodologies, they remain underutilised in animal social network analysis. In part this is due to unique features of animal network data that have led to the development and use of non-standard statistical procedures in the field. In this thesis I study some of the issues around existing methods, and highlight how a Bayesian methodology could substantially improve animal social network analyses. I introduce, implement, and explore a Bayesian framework for animal social network analysis. The framework makes it possible to conduct new types of analyses while accounting for both uncertainty and sampling biases. In addition to this, I have developed an R software package to allow researchers to use the new Bayesian framework to conduct animal social network analyses. The development of this framework raises new questions and opens up new opportunities in animal social network analysis, which I briefly explore towards the end of this thesis. I hope the developments made in this thesis will help to guide the future of animal social network analyses to make the most of hard-won network data, and to generate more reliable and insightful scientific inferences.
Abstract.
Watowich MM, Chiou KL, Graves B, Montague MJ, Brent LJN, Higham JP, Horvath JE, Lu A, Martinez MI, Platt ML, et al (2023). Best practices for genotype imputation from low‐coverage sequencing data in natural populations.
Molecular Ecology ResourcesAbstract:
Best practices for genotype imputation from low‐coverage sequencing data in natural populations
AbstractMonitoring genetic diversity in wild populations is a central goal of ecological and evolutionary genetics and is critical for conservation biology. However, genetic studies of nonmodel organisms generally lack access to species‐specific genotyping methods (e.g. array‐based genotyping) and must instead use sequencing‐based approaches. Although costs are decreasing, high‐coverage whole‐genome sequencing (WGS), which produces the highest confidence genotypes, remains expensive. More economical reduced representation sequencing approaches fail to capture much of the genome, which can hinder downstream inference. Low‐coverage WGS combined with imputation using a high‐confidence reference panel is a cost‐effective alternative, but the accuracy of genotyping using low‐coverage WGS and imputation in nonmodel populations is still largely uncharacterized. Here, we empirically tested the accuracy of low‐coverage sequencing (0.1–10×) and imputation in two natural populations, one with a large (n = 741) reference panel, rhesus macaques (Macaca mulatta), and one with a smaller (n = 68) reference panel, gelada monkeys (Theropithecus gelada). Using samples sequenced to coverage as low as 0.5×, we could impute genotypes at >95% of the sites in the reference panel with high accuracy (median r2 ≥ 0.92). We show that low‐coverage imputed genotypes can reliably calculate genetic relatedness and population structure. Based on these data, we also provide best practices and recommendations for researchers who wish to deploy this approach in other populations, with all code available on GitHub (https://github.com/mwatowich/LoCSI‐for‐non‐model‐species). Our results endorse accurate and effective genotype imputation from low‐coverage sequencing, enabling the cost‐effective generation of population‐scale genetic datasets necessary for tackling many pressing challenges of wildlife conservation.
Abstract.
Pereira A, De Moor D, Casanova C, Brent LJN (2023). Kinship composition in mammals. Royal Society Open Science
Patterson SK, Petersen RM, Brent LJN, Snyder-Mackler N, Lea AJ, Higham JP (2023). Natural Animal Populations as Model Systems for Understanding Early Life Adversity Effects on Aging.
Integrative and Comparative Biology,
63(3), 681-692.
Abstract:
Natural Animal Populations as Model Systems for Understanding Early Life Adversity Effects on Aging
Synopsis
. Adverse experiences in early life are associated with aging-related disease risk and mortality across many species. In humans, confounding factors, as well as the difficulty of directly measuring experiences and outcomes from birth till death, make it challenging to identify how early life adversity impacts aging and health. These challenges can be mitigated, in part, through the study of non-human animals, which are exposed to parallel forms of adversity and can age similarly to humans. Furthermore, studying the links between early life adversity and aging in natural populations of non-human animals provides an excellent opportunity to better understand the social and ecological pressures that shaped the evolution of early life sensitivities. Here, we highlight ongoing and future research directions that we believe will most effectively contribute to our understanding of the evolution of early life sensitivities and their repercussions.
Abstract.
Grimes C, Brent LJN, Ellis S, Weiss MN, Franks DW, Ellifrit DK, Croft DP (2023). Postreproductive female killer whales reduce socially inflicted injuries in their male offspring. Current Biology, 33(15), 3250-3256.e4.
Newman LE, Testard C, DeCasien AR, Chiou KL, Watowich MM, Janiak MC, Pavez-Fox MA, Sanchez Rosado MR, Cooper EB, Costa CE, et al (2023). The biology of aging in a social world: insights from free-ranging rhesus macaques.
bioRxivAbstract:
The biology of aging in a social world: insights from free-ranging rhesus macaques.
Social adversity can increase the age-associated risk of disease and death, yet the biological mechanisms that link social adversities to aging remain poorly understood. Long-term naturalistic studies of nonhuman animals are crucial for integrating observations of social behavior throughout an individual's life with detailed anatomical, physiological, and molecular measurements. Here, we synthesize the body of research from one such naturalistic study system, Cayo Santiago Island, which is home to the world's longest continuously monitored free-ranging population of rhesus macaques. We review recent studies of age-related variation in morphology, gene regulation, microbiome composition, and immune function. We also discuss ecological and social modifiers of age-markers in this population. In particular, we summarize how a major natural disaster, Hurricane Maria, affected rhesus macaque physiology and social structure and highlight the context-dependent and domain-specific nature of aging modifiers. Finally, we conclude by providing directions for future study, on Cayo Santiago and elsewhere, that will further our understanding of aging across different domains and how social adversity modifies aging processes.
Abstract.
Author URL.
2022
Kimock CM, Dubuc C, Brent L, Higham JP (2022). Body size and canine size do not confer a competitive advantage in male rhesus macaques. Animal Behaviour
Hart JDA, Weiss MN, Brent LJN, Franks DW (2022). Common permutation methods in animal social network analysis do not control for non-independence.
Behavioral Ecology and Sociobiology,
76(11).
Abstract:
Common permutation methods in animal social network analysis do not control for non-independence
AbstractThe 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.
Abstract.
Cooper EB, Watowich MM, Beeby N, Whalen C, Montague MJ, Brent LJN, Snyder-Mackler N, Higham JP (2022). Concentrations of urinary neopterin, but not suPAR, positively correlate with age in rhesus macaques.
Frontiers in Ecology and Evolution,
10Abstract:
Concentrations of urinary neopterin, but not suPAR, positively correlate with age in rhesus macaques
Identifying biomarkers of age-related changes in immune system functioning that can be measured non-invasively is a significant step in progressing research on immunosenescence and inflammaging in free-ranging and wild animal populations. In the present study, we aimed to investigate the suitability of two urinary compounds, neopterin and suPAR, as biomarkers of age-related changes in immune activation and inflammation in a free-ranging rhesus macaque (Macaca mulatta) population. We also investigated age-associated variation in gene transcription from blood samples to understand the underlying proximate mechanisms that drive age-related changes in urinary neopterin or suPAR. Neopterin was significantly positively correlated with age, and had a moderate within-individual repeatability, indicating it is applicable as a biomarker of age-related changes. The age-related changes in urinary neopterin are not apparently driven by an age-related increase in the primary signaler of neopterin, IFN-y, but may be driven instead by an age-related increase in both CD14+ and CD14− monocytes. suPAR was not correlated with age, and had low repeatability within-individuals, indicating that it is likely better suited to measure acute inflammation rather than chronic age-related increases in inflammation (i.e. “inflammaging”). Neopterin and suPAR had a correlation of 25%, indicating that they likely often signal different processes, which if disentangled could provide a nuanced picture of immune-system function and inflammation when measured in tandem.
Abstract.
Bonnet T, Morrissey MB, de Villemereuil P, Alberts SC, Arcese P, Bailey LD, Boutin S, Brekke P, Brent LJN, Camenisch G, et al (2022). Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.
Science,
376(6596), 1012-1016.
Abstract:
Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals
The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.
Abstract.
Allen C (2022). Importance of older males: influence of age structure on social dynamics between males in an elephant bull area.
Abstract:
Importance of older males: influence of age structure on social dynamics between males in an elephant bull area.
This thesis explores male sociality in African savannah elephants (Loxodonta africana), focusing on the influence of age structure on social dynamics between males in a male dominated area. There is much to learn regarding the nature of relationships in non-reproductive all-male groupings and the benefits afforded to males in associating with each other. Moreover, in long-lived species, all-male groupings provide an opportunity for individuals of vastly different age and experience to interact, and there may be different benefits afforded to males of different age in associating with one another.
I conducted focal animal sampling of male elephants aggregating at hotspots of social activity, and a camera trap survey of elephant movements and behaviours on elephant pathways in Makgadikgadi Pans National Park, Botswana.
I found differences in grouping and performance of several behaviours with male age. Adolescents were more likely to travel in all-male groups, and mature bulls were more likely to travel alone, suggesting association with other males is more beneficial for younger males. Adolescents performed greeting behaviours at greater rates than adults, and such behaviours may facilitate further beneficial interactions between males. Adolescents also directed more aggressive and fear-related behaviours to non-elephant targets when alone, compared to when with other males. Adolescents may therefore perceive themselves to be at greater risk when socially isolated, and grouping with other males may reduce predation risks, and improve adolescents’ ability to safely navigate unknown, risky environments. Males’ olfactory responses to pathways and experimentally placed urine deposits, however, did not vary with age, suggesting remote monitoring of same-sex conspecifics is equally important across the life course. Urine from adult males was more likely to evoke heightened responses than urine of adolescent males, suggesting males may be able to discern the age of same-sex conspecifics from their remote deposits. Such remote assessment of potential affiliates, threats or competitors sharing the environment is likely beneficial for males living in highly fission-fusion societies.
I also found evidence for important social roles of older males in all-male groupings. Older males were more likely to lead their group movements, suggesting they may guide younger, less experienced males in locating critical resources. Male elephants were less likely to direct aggression to non-elephant targets when more males from the oldest age cohort were present. Older males may be particularly effective assessors of environmental risk, and elephants may perform less aggressive behaviours to non-elephant targets when more older males are present due to reductions in anxiety. Alternatively, older males may police other males’ aggression behaviours.
The African elephant is of conservation concern and a species involved in several unresolved human-wildlife conflicts. Throughout this thesis I therefore also relate findings to potential management and conservation implications.
Abstract.
Kuthyar S, Watson K, Huang S, Brent LJN, Platt M, Horvath J, Gonzalez-Martinez J, Martínez M, Godoy-Vitorino F, Knight R, et al (2022). Limited microbiome differences in captive and semi-wild primate populations consuming similar diets.
FEMS Microbiology Ecology,
98(10).
Abstract:
Limited microbiome differences in captive and semi-wild primate populations consuming similar diets
Abstract
. Gut microbial communities are shaped by a myriad of extrinsic factors, including diet and the environment. Although distinct human populations consistently exhibit different gut microbiome compositions, variation in diet and environmental factors are almost always coupled, making it difficult to disentangle their relative contributions to shaping the gut microbiota. Data from discrete animal populations with similar diets can help reduce confounds. Here, we assessed the gut microbiota of free-ranging and captive rhesus macaques with at least 80% diet similarity to test the hypothesis that hosts in difference environments will have different gut microbiomes despite a shared diet. Although we found that location was a significant predictor of gut microbial composition, the magnitude of observed differences was relatively small. These patterns suggest that a shared diet may limit the typical influence of environmental microbial exposure on the gut microbiota.
Abstract.
Chiou KL, DeCasien AR, Rees KP, Testard C, Spurrell CH, Gogate AA, Pliner HA, Tremblay S, Mercer A, Whalen CJ, et al (2022). Multiregion transcriptomic profiling of the primate brain reveals signatures of aging and the social environment.
Nat Neurosci,
25(12), 1714-1723.
Abstract:
Multiregion transcriptomic profiling of the primate brain reveals signatures of aging and the social environment.
Aging is accompanied by a host of social and biological changes that correlate with behavior, cognitive health and susceptibility to neurodegenerative disease. To understand trajectories of brain aging in a primate, we generated a multiregion bulk (N = 527 samples) and single-nucleus (N = 24 samples) brain transcriptional dataset encompassing 15 brain regions and both sexes in a unique population of free-ranging, behaviorally phenotyped rhesus macaques. We demonstrate that age-related changes in the level and variance of gene expression occur in genes associated with neural functions and neurological diseases, including Alzheimer's disease. Further, we show that higher social status in females is associated with younger relative transcriptional ages, providing a link between the social environment and aging in the brain. Our findings lend insight into biological mechanisms underlying brain aging in a nonhuman primate model of human behavior, cognition and health.
Abstract.
Author URL.
Watowich MM, Chiou KL, Montague MJ, Simons ND, Horvath JE, Ruiz-Lambides AV, Martínez MI, Higham JP, Brent LJN, Platt ML, et al (2022). Natural disaster and immunological aging in a nonhuman primate.
Proceedings of the National Academy of Sciences,
119(8).
Abstract:
Natural disaster and immunological aging in a nonhuman primate
Significance
. Survivors of extreme adverse events, including natural disasters, often exhibit chronic inflammation and early onset of age-related diseases. Adversity may therefore accelerate aging via the immune system, which is sensitive to lived experiences. We tested if experiencing a hurricane was associated with immune gene expression in a population of free-ranging macaques. Exposure to Hurricane Maria broadly recapitulated age-associated molecular changes, including disruptions of protein folding genes, greater inflammatory immune cell marker gene expression, and older biological aging by an average of 2 y—approximately 7 to 8 y of the human lifespan. Together, our findings suggest that experiencing an extreme hurricane is associated with alterations in immune cell gene regulation similar to aging, potentially accelerating aspects of the aging process.
Abstract.
O’Hearn WJ, Ruiz-Lambides A, Platt ML, Brent LJN (2022). No evidence that grooming is exchanged for coalitionary support in the short- or long-term via direct or generalized reciprocity in unrelated rhesus macaques.
Behavioral Ecology and Sociobiology,
76(4).
Abstract:
No evidence that grooming is exchanged for coalitionary support in the short- or long-term via direct or generalized reciprocity in unrelated rhesus macaques
. Abstract
. Reciprocity is a prominent explanation for cooperation between non-kin. Studies designed to demonstrate reciprocity often focus on direct reciprocity in the timescale of minutes to hours, whereas alternative mechanisms like generalized reciprocity and the possibility of reciprocation over longer timescales of months and years are less often explored. Using a playback experiment, we tested for evidence of direct and generalized reciprocity across short and longer timescales. We examined the exchange of grooming for coalitionary support between unrelated female rhesus macaques in a population with a complete genetic pedigree. Females that received grooming were not more responsive to calls for coalitionary support from unrelated female group mates compared to control females that received agonism or no interaction — even when the call belonged to a females’ most recent grooming partner. Similarly, females were not more responsive to calls for support from their most frequent unrelated grooming partner of the last two years, nor if they received large amounts of grooming from all other females in their group. We interpret these results as an absence of evidence for direct or generalized reciprocity on any timescale in the exchange of grooming for coalitionary support in rhesus macaques. If grooming is exchanged for support in this population, it is with an intensity below our ability to detect it or over a longer timescale than we examined. We propose by-product explanations may also be at play and highlight the importance of investigating multiple mechanisms when testing apparently cooperative behaviors.
.
. Significance statement
. The receipt of help can make some animals more likely to provide help in return, whether it be a singular act, or many acts accumulated over months. Similarly, the receipt of help, be it one act of aid, or a group’s worth of help over time, can make some animals more likely to pay help forward to others. Studies on Old World monkeys suggest females may give grooming and in return receive aid in future physical conflicts. Using a playback experiment, we found female rhesus macaques were not more responsive to calls for intervention in a simulated conflict after being groomed by unrelated females, even if the calling combatant was her most recent, or a long-time grooming partner. Our results suggest females in our study population may be receiving benefits other than support in conflicts for the grooming they provide.
.
Abstract.
Ellis S, Cant M, Weiss M, Brent L, Meniri M, Thompson F, Croft D (2022). Patterns and consequences of age-linked change in local relatedness in animal societies.
Nature Ecology and EvolutionAbstract:
Patterns and consequences of age-linked change in local relatedness in animal societies
The ultimate payoff of behaviours depends not only on their direct impact on an individual but also on the impact on their relatives. Local relatedness – the average relatedness of an individual to their social environment – therefore has profound impacts on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual’s lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their impacts on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly impact lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.
Abstract.
Pavez-Fox MA, Kimock CM, Rivera-Barreto N, Valle JEN-D, Phillips D, Ruiz-Lambides A, Snyder-Mackler N, Higham JP, Siracusa ER, Brent LJN, et al (2022). Reduced injury risk links sociality to survival in a group-living primate.
Pavez-Fox MA, Kimock CM, Rivera-Barreto N, Negron-Del Valle JE, Phillips D, Ruiz-Lambides A, Snyder-Mackler N, Higham JP, Siracusa ER, Brent LJN, et al (2022). Reduced injury risk links sociality to survival in a group-living primate. iScience, 25(11), 105454-105454.
Siracusa ER, Higham JP, Snyder-Mackler N, Brent LJN (2022). Social ageing: exploring the drivers of late-life changes in social behaviour in mammals.
Biology Letters,
18(3).
Abstract:
Social ageing: exploring the drivers of late-life changes in social behaviour in mammals
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.
Abstract.
Testard C, Brent L, Andersson J, Chiou KL, Negron Del-Valle JE, DeCasien AR, Acevedo-Ithier A, Stock MK, Anton SC, Gonzalez O, et al (2022). Social connections predict brain structure in a multidimensional free-ranging primate society. Science Advances
Cooper EB, Brent LJN, Snyder-Mackler N, Singh M, Sengupta A, Khatiwada S, Malaivijitnond S, Qi Hai Z, Higham JP (2022). The rhesus macaque as a success story of the Anthropocene.
Elife,
11Abstract:
The rhesus macaque as a success story of the Anthropocene.
Of all the non-human primate species studied by researchers, the rhesus macaque (Macaca mulatta) is likely the most widely used across biological disciplines. Rhesus macaques have thrived during the Anthropocene and now have the largest natural range of any non-human primate. They are highly social, exhibit marked genetic diversity, and display remarkable niche flexibility (which allows them to live in a range of habitats and survive on a variety of diets). These characteristics mean that rhesus macaques are well-suited for understanding the links between sociality, health and fitness, and also for investigating intra-specific variation, adaptation and other topics in evolutionary ecology.
Abstract.
Author URL.
Grimes C (2022). The social and ecological drivers of aggression in southern resident killer whales, Orcinus orca.
Abstract:
The social and ecological drivers of aggression in southern resident killer whales, Orcinus orca
The social behaviour of individuals within group living species is a topic of great interest. for. behavioural. ecologists. as. interactions. between. conspecifics. can fluctuate. between. affiliative. and. aggressive. in response. to. various. social. and ecologicalfactors.Aggressivebehaviourisprevalentacrosstheanimalkingdom, often. arising. as. a. result. ofcompetition. for. valuable. resources. and. can. have. a profoundimpactonsurvivalandreproduction.Examiningwhyconflictarisesand how it is mitigated is crucial for understanding how individuals gain the benefits associated with sociality. Intraspecific aggression is widely studied in terrestrial mammals;. however. for. cetacean. species. gaps. in. our. knowledge. about. the frequency and intensity of aggressive interactions remain,dueto the difficulty in directly. observing. social. interactions. in. many. marine. mammals. Southern resident killer whales (Orcinus orca) are one of the most studied populations of killer. whales. in. the. world. with. decades. of. individual-based. data. collected. on them. providing. a. unique. opportunity. to. study. drivers. of. aggressive. social interactions. In. this. thesis. using. a. longitudinal. dataset. spanning. 37. years. of photographic images and tooth rake marks as an indicator of social interactions, I. investigate. demographic. ecological. and. social. drivers. of socially. acquired marksinsouthernresidentkillerwhales.Specifically,Iexamine patterns of tooth rake density across age and sex classes and find rake density to be highest in young whales, decreasing across the lifespan. I also investigate the influence of their primary food source, Chinooksalmon (Oncorhynchus tshawytscha), on rake density, and observe an increase in tooth rake density across the population as the abundance of salmon increases. Finally, I explore how the composition of the social environment impacts rake density and present an important finding which suggests that postreproductivefemales mayreducethe intensity of social contact
3events between individuals within their social group. Although this effect is seen in. both. sexes. a. stronger. effect. is. observed. in. males. Furthermore. I. observe subadult. males. to. exhibit. a. higher. density. of. rakes. when. there. aremore. adult males present. in. their social. environment. suggesting. that. adult. males. may. be responsible. for. producing. these. marks. This. thesis. presents. the. first comprehensiveanalysisofsocialandecologicaldriversoftoothrakedensityina long-lived mammal, revealing the life-history stages at which individuals may face aggression. from. conspecifics. and. how. these. whales. might. be. organised. to moderateconflict.Whilstthesefindingsaddressimportantquestionsaroundkiller whale social behaviour, I suggest that further research, utilising unmanned aerial vehicles. would. be. pertinent. to. further. elucidate. the. complex. social. lives. of. this endangeredpopulation.
Abstract.
Siracusa ER, Valle JEN-D, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (2022). Within-individual changes reveal increasing social selectivity with age in rhesus macaques.
Siracusa ER, Negron-Del Valle JE, Phillips D, Platt ML, Higham JP, Snyder-Mackler N, Brent LJN (2022). Within-individual changes reveal increasing social selectivity with age in rhesus macaques.
Proceedings of the National Academy of Sciences,
119(49).
Abstract:
Within-individual changes reveal increasing social selectivity with age in rhesus macaques
Accumulating evidence in humans and other mammals suggests older individuals tend to have smaller social networks. Uncovering the cause of these declines can inform how changes in social relationships with age affect health and fitness in later life. While age-based declines in social networks have been thought to be detrimental, physical and physiological limitations associated with age may lead older individuals to adjust their social behavior and be more selective in partner choice. Greater selectivity with age has been shown in humans, but the extent to which this phenomenon occurs across the animal kingdom remains an open question. Using longitudinal data from a population of rhesus macaques on Cayo Santiago, we provide compelling evidence in a nonhuman animal for within-individual increases in social selectivity with age. Our analyses revealed that adult female macaques actively reduced the size of their networks as they aged and focused on partners previously linked to fitness benefits, including kin and partners to whom they were strongly and consistently connected earlier in life. Females spent similar amounts of time socializing as they aged, suggesting that network shrinkage does not result from lack of motivation or ability to engage, nor was this narrowing driven by the deaths of social partners. Furthermore, females remained attractive companions and were not isolated by withdrawal of social partners. Taken together, our results provide rare empirical evidence for social selectivity in nonhumans, suggesting that patterns of increasing selectivity with age may be deeply rooted in primate evolution.
Abstract.
2021
Hart JDA, Franks DW, Brent LJN, Weiss MN (2021). Accuracy and power analysis of social networks built from count data.
Methods in Ecology and Evolution,
13(1), 157-166.
Abstract:
Accuracy and power analysis of social networks built from count data
Abstract
Power analysis is used to estimate the probability of correctly rejecting a null hypothesis for a given statistical model and dataset. Conventional power analyses assume complete information, but the stochastic nature of behavioural sampling can mean that true and estimated networks are poorly correlated. Power analyses do not currently take the effect of sampling into account. This could lead to inaccurate estimates of statistical power, potentially yielding misleading results.
Here we develop a method for computing network correlation: the correlation between an estimated social network and its true network, using a Gamma–Poisson model of social event rates for networks constructed from count data. We use simulations to assess how the level of network correlation affects the power of nodal regression analyses. We also develop a generic method of power analysis applicable to any statistical test, based on the concept of diminishing returns.
We demonstrate that our network correlation estimator is both accurate and moderately robust to its assumptions being broken. We show that social differentiation, mean social event rate and the harmonic mean of sampling times positively impacts the strength of network correlation. We also show that the required level of network correlation to achieve a given power level depends on many factors, but that 0.80 network correlation usually corresponds to around 80% power for nodal regression in ideal circumstances.
We provide guidelines for using our network correlation estimator to verify the accuracy of networks built from count data, and to conduct power analysis. This can be used prior to data collection, in post hoc analyses or even for subsetting networks in dynamic network analysis. The network correlation estimator and custom power analysis methods have been made available as an r package.
Abstract.
Rosado MRS, Marzan-Rivera N, Watowich MM, Valle ADN-D, Pantoja P, Pavez-Fox MA, Siracusa ER, Cooper EB, Valle JEN-D, Phillips D, et al (2021). Age, sex, and social environmental effects on immune cell composition in a free-ranging non-human primate.
Allen C, Brent L, Thatayaone M, Croft D (2021). Field evidence supporting monitoring of chemical information on pathways by male African elephants. Animal Behaviour
Allen C, Croft D, Testard C, Brent L (2021). Function of trunk-mediated “greeting” behaviours between male African elephants: insights from choice of partners. Animals
Allen C, Croft DP, Brent LJN (2021). Reduced older male presence linked to increased rates of aggression to non-conspecific targets in male elephants. Proceedings of the Royal Society B: Biological Sciences
Testard C, Larson SM, Watowich MM, Kaplinsky CH, Bernau A, Faulder M, Marshall HH, Lehmann J, Ruiz-Lambides A, Higham JP, et al (2021). Rhesus macaques build new social connections after a natural disaster. Current Biology, 31(11), 2299-2309.e7.
Crisp RJ, Brent LJN, Carter GG (2021). Social dominance and cooperation in female vampire bats.
Royal Society Open Science,
8(7), 210266-210266.
Abstract:
Social dominance and cooperation in female vampire bats
When 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'sh’ 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.
Abstract.
Pavez-Fox MA, Negron-Del Valle JE, Thompson IJ, Walker CS, Bauman SE, Gonzalez O, Compo N, Ruiz-Lambides A, Martinez MI, Platt ML, et al (2021). Sociality predicts individual variation in the immunity of free-ranging rhesus macaques. Physiology & Behavior, 241, 113560-113560.
Grimes C, Brent L, Weiss M, Franks DW, Balcomb KC, Ellifrit DK, Ellis S, Croft D (2021). The effect of age, sex, and resource abundance on patterns of rake markings in resident killer whales (Orcinus orca). Marine Mammal Science
2020
Weiss M, Franks DW, Brent L, Ellis S, Silk M, Croft D (2020). Common datastream permutations of animal social network data are not appropriate for hypothesis testing using regression models. Methods in Ecology and Evolution
Weiss MN, Franks DW, Brent LJN, Ellis S, Silk MJ, Croft DP (2020). Common datastream permutations of animal social network data are not appropriate for hypothesis testing using regression models.
Morrison RE, Eckardt W, Stoinski TS, Brent LJN (2020). Comparing measures of social complexity: larger mountain gorilla groups do not have a greater diversity of relationships.
Proceedings of the Royal Society B: Biological Sciences,
287(1931).
Abstract:
Comparing measures of social complexity: larger mountain gorilla groups do not have a greater diversity of relationships
Social complexity reflects the intricate patterns of social interactions in societies. Understanding social complexity is fundamental for studying the evolution of diverse social systems and the cognitive innovations used to cope with the demands of social life. Social complexity has been predominantly quantified by social unit size, but newer measures of social complexity reflect the diversity of relationships. However, the association between these two sets of measures remains unclear. We used 12 years of data on 13 gorilla groups to investigate how measures of social complexity relate to each other. We found that group size was a poor proxy for relationship diversity and that the social complexity individuals experienced within the same group varied greatly. Our findings demonstrate two fundamental takeaways: first, that the number of relationships and the diversity of those relationships represent separate components of social complexity, both of which should be accounted for; and second, that social complexity measured at the group level may not represent the social complexity experienced by individuals in those groups. These findings suggest that comprehensive studies of social complexity, particularly those relating to the social demands faced by individuals, may require fine-scale social data to allow accurate comparisons across populations and species.
Abstract.
Allen C, Brent L, Motsentwa T, Weiss M, Croft D (2020). Importance of Old Bulls: Leaders and Followers in Collective Movements of All-Male Groups in African Savannah Elephants (Loxodonta africana). Scientific Reports
Chiou KL, Montague MJ, Goldman EA, Watowich MM, Sams SN, Song J, Horvath JE, Sterner KN, Ruiz-Lambides AV, Martinez MI, et al (2020). Rhesus macaques as a tractable physiological model of human ageing. Philosophical Transactions of the Royal Society B: Biological Sciences
2019
Ellis S, Snyder-Mackler N, Ruiz-Lambides A, Platt ML, Brent LJN (2019). Deconstructing sociality: the types of social connections that predict longevity in a group-living primate.
Proceedings of the Royal Society B: Biological Sciences,
286(1917), 20191991-20191991.
Abstract:
Deconstructing sociality: the types of social connections that predict longevity in a group-living primate
. Many species use social interactions to cope with challenges in their environment and a growing number of studies show that individuals which are well-connected to their group have higher fitness than socially isolated individuals. However, there are many ways to be ‘well-connected’ and it is unclear which aspects of sociality drive fitness benefits. Being well-connected can be conceptualized in four main ways: individuals can be socially integrated by engaging in a high rate of social behaviour or having many partners; they can have strong and stable connections to favoured partners; they can indirectly connect to the broader group structure; or directly engage in a high rate of beneficial behaviours, such as grooming. In this study, we use survival models and long-term data in adult female rhesus macaques (
. Macaca mulatta
. ) to compare the fitness outcomes of multiple measures of social connectedness. Females that maintained strong connections to favoured partners had the highest relative survival probability, as did females well-integrated owing to forming many weak connections. We found no survival benefits to being structurally well-connected or engaging in high rates of grooming. Being well-connected to favoured partners could provide fitness benefits by, for example, increasing the efficacy of coordinated or mutualistic behaviours.
.
Abstract.
O'Hearn W (2019). Direct and generalized reciprocity in the cooperative exchanges of free living Rhesus macaques on Cayo Santiago.
Abstract:
Direct and generalized reciprocity in the cooperative exchanges of free living Rhesus macaques on Cayo Santiago
Direct reciprocity is the most cited explanation for the evolution of cooperation between unrelated individuals. Yet, few studies have examined generalized reciprocity as an alternative mechanism, despite generalized reciprocity’s minimal cognitive demands and capacity to explain the same patterns of cooperation as direct reciprocity. Studies of direct reciprocity tend to explore reciprocal exchange across either individual interactions or long periods of time, rarely studying both at once. In addition, most studies of reciprocity only account for maternal relatedness between cooperative partners, failing to rule out the effect of kin selection through paternal relatedness. In this thesis we investigated the role of direct and generalized reciprocity in female rhesus macaque cooperative exchanges. We modified a classic playback experiment and explored the effect of both recent and repeated grooming interactions on females’ willingness to provide coalitionary support to other adult females. We conducted this study using the rhesus macaques at the Cayo Santiago field station, where maternal and paternal relatedness is known for all study subjects. We found no evidence of direct or generalized reciprocity in the exchange of grooming for coalitionary support. Our results contradict the findings of similar playback experiments but are consistent with correlational studies in species that are despotic like rhesus macaques. The despotic nature of our study system, combined with our finding that females’ willingness to provide support declined as the number of infants in their matriline increased, could suggest that grooming is not a sufficient price to pay to acquire coalitionary support from unrelated rhesus macaques. We propose by-product mutualism and kin-selection may play a larger role than has been previously appreciated in decisions regarding who to support in agnostic encounters, and we highlight the importance of investigating multiple cooperative mechanisms when studying of the evolution of cooperative behaviours.
Abstract.
Crisp R (2019). Dominance behaviour of female vampire bats.
Abstract:
Dominance behaviour of female vampire bats
Female vampire bats (Desmodus rotundus) are a model for the study of cooperation in behavioural ecology, but we know very little of their conflict. This gap in knowledge is surprising given that competition over resources, and thus conflict, is an expected consequence of group living (Clutton-Brock & Huchard, 2013). Further, it is important to understand how vampire bats compete and resolve conflict because there is evidence to suggest that patterns of conflict are associated with patterns of cooperation (e.g. Schino & Aureli, 2008). We aimed to address this gap by observing competitive interactions occurring over food within a captive colony of 33 vampire bats which included adult females and their young aged 5 months and younger. To understand whether there was a pattern to competitive interactions we looked for evidence of a dominance hierarchy. We found strong evidence for a weakly linear dominance hierarchy, tested using three standard metrics: directional consistency, Landua’s h’, and triangle transitivity. Randomised Elo-ratings showed that the hierarchy was not steep. We also found no evidence that rank was predicted by body size, sex, age, reproductive status, social group origin, or kinship. Taken together, these results strongly indicate that vampire bat social interactions are predominantly egalitarian. To put our results in a broader context, we compared dominance hierarchy metrics in female vampire bats to 172 published datasets from other taxa. Female vampire bat dominance was less linear and less steep than over 95% of other taxa. This indicates that female vampire bats are exceptional in their lack of a strict dominance hierarchy. Our results are consistent with the prediction that egalitarian or low-sloped hierarchies will occur in species characterised by symmetrical and reciprocal cooperative relationships which supports the biological market theory of cooperation.
Abstract.
Kimock CM, Dubuc C, Brent LJN, Higham JP (2019). Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate.
Scientific Reports,
9(1).
Abstract:
Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate
AbstractSexual 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.
Abstract.
2018
Pavelka MSM, Brent LJN, Croft DP, Fedigan LM (2018). Post-fertile Lifespan in Female Primates and Cetaceans. In Kalbitzer U, Jack K (Eds.) Primate Life Histories, Sex Roles, and Adaptability. Developments in Primatology: Progress and Prospects, Springer, Cham.
Madlon-Kay S, Montague MJ, Brent LJN, Eliis S, Zhong B, Snyder-Mackler N, Horvath JE, Skene JHP, Platt ML (2018). Weak effects of common genetic variation in oxytocin and vasopressin receptor genes on rhesus macaque social behavior. American Journal of Primatology
2017
Lacy RC, Williams R, Ashe E, Balcomb KC, Brent LJN, Clark CW, Croft DP, Giles DA, MacDuffee M, Paquet PC, et al (2017). Evaluating anthropogenic threats to endangered killer whales to inform effective recovery plans. Scientific Reports
Lacy RC, Williams R, Ashe E, Balcomb KC, Brent LJN, Clark CW, Croft DP, Giles DA, MacDuffee M, Paquet P, et al (2017). Evaluating anthropogenic threats to endangered killer whales to inform effective recovery plans. Scientific Reports
Brent LJN, Ruiz-Lambides A, Platt ML (2017). Family network size and survival across the lifespan of female macaques.
Proceedings of the Royal Society B: Biological Sciences,
284(1854), 20170515-20170515.
Abstract:
Family network size and survival across the lifespan of female macaques
Two decades of research suggest social relationships have a common evolutionary basis in humans and other gregarious mammals. Critical to the support of this idea is growing evidence that mortality is influenced by social integration, but when these effects emerge and how long they last is mostly unknown. Here, we report in adult female macaques that the impact of number of close adult female relatives, a proxy for social integration, on survival is not experienced uniformly across the life course; prime-aged females with a greater number of relatives had better survival outcomes compared with prime-aged females with fewer relatives, whereas no such effect was found in older females. Group size and dominance rank did not influence this result. Older females were less frequent targets of aggression, suggesting enhanced experience navigating the social landscape may obviate the need for social relationships in old age. Only one study of humans has found age-based dependency in the association between social integration and survival. Using the largest dataset for any non-human animal to date, our study extends support for the idea that sociality promotes survival and suggests strategies employed across the life course change along with experience of the social world.
Abstract.
Firth JA, Brent LJN, Sheldon BC (2017). Indirectly connected: simple social differences can explain the causes and apparent consequences of complex social network positions. Proceedings of the Royal Society B: Biological Sciences
Brent LJN (2017). Mammal societies.
ANIMAL BEHAVIOUR,
131, 43-43.
Author URL.
Brent LJN, Ruiz-Lambides A, Platt ML (2017). Persistent social isolation reflects identity and social context but not maternal effects or early environment. Scientific Reports
Croft DP, Johnstone RA, Ellis S, Nattrass S, Franks DW, Brent LJN, Mazzi S, Balcomb C, Ford JKB, Cant MA, et al (2017). Reproductive Conflict and the Evolution of Menopause in Killer Whales. Current Biology
Larson SM, Ruiz-Lambides A, Platt ML, Brent LJN (2017). Social network dynamics precede a mass eviction in group-living rhesus macaques. Animal Behaviour
Madlon-Kay S, Brent LJN, Montague M, Heller K, Platt ML (2017). Using Machine Learning to Discover Latent Social Phenotypes in Free-Ranging Macaques. Brain Sciences
2016
Franks DW, Nattrass S, Brent LJN, Whitehead H, Foote AD, Mazzi S, Ford JKB, Balcomb KC, Cant MA, Croft DP, et al (2016). The significance of postreproductive lifespans in killer whales: a comment on Robeck et al. Journal of Mammalogy, gyw021-gyw021.
Boyland N, Mlynski DT, James R, Brent LJN, Croft DP (2016). The social network structure of a dynamic group of dairy cows: from individual to group level patterns.
Applied Animal Behaviour ScienceAbstract:
The social network structure of a dynamic group of dairy cows: from individual to group level patterns
Social relationships have been shown to significantly impact individual and group success in wild animal populations, but are largely ignored in farm animal management. There are substantial gaps in our knowledge of how farm animals respond to their social environment, which varies greatly between farms but is commonly unstable due to regrouping. Fundamental to addressing these gaps is an understanding of the social network structure resulting from the patterning of relationships between individuals in a group. Here, we investigated the social structure of a group of 110 lactating dairy cows during four one-month periods. Spatial proximity loggers collected data on associations between cows, allowing us to construct social networks. First we demonstrate that proximity loggers can be used to measure relationships between cows; proximity data was significantly positively correlated to affiliative interactions but had no relationship with agonistic interactions. We measured group-level patterns by testing for community structure, centralisation and repeatability of network structure over time. We explored individual-level patterns by measuring social differentiation (heterogeneity of social associations) and assortment of cows in the network by lactation number, breed, gregariousness and milk production. There was no evidence that cows were subdivided into social communities; individuals belonged to a single cluster and networks showed significant centralisation. Repeatability of the social network was low, which may have consequences for animal welfare. Individuals formed differentiated social relationships and there was evidence of positive assortment by traits; cows associated more with conspecifics of similar lactation number in all study periods. There was also positive assortment by breed, gregariousness and milk production in some study periods. There is growing interest in the farming industry in the impact of social factors on production and welfare; this study takes an important step towards understanding social dynamics.
Abstract.
2015
Brent LJN, Franks DW, Foster EA, Balcomb KC, Cant MA, Croft DP (2015). Ecological Knowledge, Leadership, and the Evolution of Menopause in Killer Whales EDITORIAL COMMENT.
OBSTETRICAL & GYNECOLOGICAL SURVEY,
70(11), 701-702.
Author URL.
Brent LJN, Franks DW, Foster EA, Balcomb KC, Cant MA, Croft DP (2015). Ecological knowledge, leadership, and the evolution of menopause in killer whales. Current Biology, 25(6), 746-750.
Brent LJN (2015). Friends of friends: Are indirect connections in social networks important to animal behaviour?. Animal Behaviour, 103, 211-222.
Watson KK, Li D, Brent LJN, Horvath JE, Gonzalez-Martinez J, Ruiz-Lambides AV, Robinson AG, Skene JHP, Platt MLP (2015). Genetic influences on social attention in free-ranging rhesus macaques. Animal Behaviour, 103, 267-275.
Croft DP, Brent LJN, Franks DW, Cant MA (2015). The evolution of prolonged life after reproduction.
Trends in Ecology and EvolutionAbstract:
The evolution of prolonged life after reproduction
Why females of some species cease ovulation before the
end of their natural lifespan is a longstanding evolutionary
puzzle. For many species in captivity, post-reproductive
life is simply an epiphenomenon of lengthened
lifespan. Yet in natural populations of humans as well
as some cetaceans and insects, reproductive senescence
occurs much faster than somatic aging and females
exhibit prolonged post-reproductive lifespans (PRLSs).
Determining the mechanisms and functions that underpin
PRLSs has proved a significant challenge. Here we
bring together both classic and modern hypotheses
proposed to explain PRLSs and discuss their application
to both human and nonhuman animals. By taking an
integrative and broad taxonomic approach we highlight
the need to consider multiple interacting explanations
for the evolution of PRLSs.
Abstract.
Croft DP, Brent LJN, Franks DW, Cant MA (2015). The evolution of prolonged life after reproduction.
Trends in Ecology and Evolution,
30(7), 407-416.
Abstract:
The evolution of prolonged life after reproduction
© 2015 the Authors. Why females of some species cease ovulation before the end of their natural lifespan is a longstanding evolutionary puzzle. For many species in captivity, post-reproductive life is simply an epiphenomenon of lengthened lifespan. Yet in natural populations of humans as well as some cetaceans and insects, reproductive senescence occurs much faster than somatic aging and females exhibit prolonged post-reproductive lifespans (PRLSs). Determining the mechanisms and functions that underpin PRLSs has proved a significant challenge. Here we bring together both classic and modern hypotheses proposed to explain PRLSs and discuss their application to both human and nonhuman animals. By taking an integrative and broad taxonomic approach we highlight the need to consider multiple interacting explanations for the evolution of PRLSs.
Abstract.
2014
Brent L (2014). A rewarding relationship. New Scientist, 222(2970), 37-39.
Blomquist GE, Brent LJN (2014). Applying Quantitative Genetic Methods to Primate Social Behavior.
International Journal of Primatology,
35(1), 108-128.
Abstract:
Applying Quantitative Genetic Methods to Primate Social Behavior
Increasingly, behavioral ecologists have applied quantitative genetic methods to investigate the evolution of behaviors in wild animal populations. The promise of quantitative genetics in unmanaged populations opens the door for simultaneous analysis of inheritance, phenotypic plasticity, and patterns of selection on behavioral phenotypes all within the same study. In this article, we describe how quantitative genetic techniques provide studies of the evolution of behavior with information that is unique and valuable. We outline technical obstacles for applying quantitative genetic techniques that are of particular relevance to studies of behavior in primates, especially those living in noncaptive populations, e.g. the need for pedigree information, non-Gaussian phenotypes, and demonstrate how many of these barriers are now surmountable. We illustrate this by applying recent quantitative genetic methods to spatial proximity data, a simple and widely collected primate social behavior, from adult rhesus macaques on Cayo Santiago. Our analysis shows that proximity measures are consistent across repeated measurements on individuals (repeatable) and that kin have similar mean measurements (heritable). Quantitative genetics may hold lessons of considerable importance for studies of primate behavior, even those without a specific genetic focus. © 2013 Springer Science+Business Media New York.
Abstract.
Brent LJN, Semple S, MacLarnon A, Ruiz-Lambides A, Gonzalez-Martinez J, Platt ML (2014). Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output.
International Journal of Primatology,
35(1), 188-209.
Abstract:
Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output
There is growing evidence that behavioral tendencies, or "personalities," in animals are an important aspect of their biology, yet their evolutionary basis is poorly understood. Specifically, how individual variation in personality arises and is subsequently maintained by selection remains unclear. To address this gap, studies of personality require explicit incorporation of genetic information. Here, we explored the genetic basis of personality in rhesus macaques by determining the heritability of personality components and by examining the fitness consequences of those components. We collected observational data for 108 adult females living in three social groups in a free-ranging population via focal animal sampling. We applied principal component analysis to nine spontaneously occurring behaviors and identified six putative personality components, which we named Meek, Bold, Aggressive, Passive, Loner, and Nervous. All components were repeatable and heritable, with heritability estimates ranging from 0.14 to 0.35. We found no evidence of an association with reproductive output, measured either by infant survival or by interbirth interval, for any of the personality components. This finding suggests either that personality does not have fitness-related consequences in this population or that selection has acted to reduce fitness-associated variation in personality. © 2013 Springer Science+Business Media New York.
Abstract.
Dubuc C, Winters S, Allen WL, Brent LJN, Casio J, Maestripieri D, Ruiz-Lambides AV, Widdig A, Higham JP (2014). Sexually selected skin color is heritable and related to fitness in a non-human primate. Proceedings of the Royal Society of London: Biological Sciences, 281, 20141602-20141602.
Brent LJN, Melin AD (2014). The Genetic Basis of Primate Behavior: Genetics and Genomics in Field-Based Primatology. International Journal of Primatology, 35(1), 1-10.
MacLean EL, Hare B, Nun CL, Addess E, Amic F, Anderson RC, Aureli F, Baker JM, Bania AE, Barnard AM, et al (2014). The evolution of self-control.
Proceedings of the National Academy of Sciences of the United States of America,
111(20).
Abstract:
The evolution of self-control
Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.
Abstract.
Brent LJN, Chang SW, Gariepy JF, Platt ML (2014). The neuroethology of friendship. Annals of the New York Academy of Sciences, 1316, 1-17.
2013
Gilby IC, Brent LJN, Wroblewski EE, Rudicell RS, Hahn BH, Goodall J, Pusey AE (2013). Fitness benefits of coalitionary aggression in male chimpanzees.
Behavioral Ecology and Sociobiology,
67(3), 373-381.
Abstract:
Fitness benefits of coalitionary aggression in male chimpanzees
Coalitionary aggression occurs when at least two individuals jointly direct aggression at one or more conspecific targets. Scientists have long argued that this common form of cooperation has positive fitness consequences. Nevertheless, despite evidence that social bond strength (which is thought to promote coalition formation) is correlated with fitness in primates, cetaceans, and ungulates, few studies have directly examined whether coalitionary aggression improves reproductive success. We tested the hypothesis that among free-ranging chimpanzees (Pan troglodytes schweinfurthii), participation in coalitionary aggression increases reproductive output. Using 14 years of genetic and behavioral data from Gombe National Park, Tanzania, we found that coalitionary aggression increased a male's chances of (A) siring offspring, compared to other males of similar dominance rank, and (B) ascending in rank, a correlate of future reproductive output. Because male chimpanzees form coalitions with many others within a complex network, we used social network analysis to identify the types of connections correlated with these fitness benefits. The beneficiaries of coalitionary aggression were males with the highest "betweenness"-that is, those who tended to have coalition partners who themselves did not form coalitions with each other. This suggests that beyond simply recognizing third-party relationships, chimpanzees may use this knowledge to choose coalition partners. If so, this is a significant step forward in our knowledge of the adaptive value of social intelligence. Regardless of mechanism, however, this is the first evidence of genetic benefits of coalitionary aggression in this species, and therefore has important implications for understanding the evolution of cooperation. © 2012 Springer-Verlag Berlin Heidelberg.
Abstract.
Brent LJN, Heilbronner SR, Horvath JE, Gonzalez-Martinez J, Ruiz-Lambides A, Robinson AG, Pate Skene JH, Platt ML (2013). Genetic origins of social networks in rhesus macaques.
Scientific Reports,
3Abstract:
Genetic origins of social networks in rhesus macaques
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.
Abstract.
Chang SW, Brent LJN, Adams GK, Pearson J, Klein J, Watson KK, Platt ML (2013). Neuroethology of primate social behavior. Proceedings of the National Academy of Sciences of USA, 110, 10387-10394.
Dobson SD, Brent LJN (2013). On the evolution of the serotonin transporter linked polymorphic region (5-HTTLPR) in primates.
Frontiers in Human Neuroscience(NOV).
Abstract:
On the evolution of the serotonin transporter linked polymorphic region (5-HTTLPR) in primates
Some allelic variants of the serotonin transporter linked polymorphic region (5-HTTLPR) result in lower levels of expression of the serotonin transporter gene (SLC6A4). These low-expressing (LE) alleles are associated with mental-health disorders in a minority of humans that carry them. Humans are not the only primates that exhibit this polymorphism; other species, including some monkeys, also have LE and high-expressing (HE) variants of 5-HTTLPR. We propose a behavioral genetic framework to explain the adaptive evolution of this polymorphism in primates, including humans. We hypothesize that both LE and HE alleles are maintained by balancing selection in species characterized by short-term fluctuations in social competition levels. More specifically, we propose that LE carriers benefit from their hypervigilant tendencies during periods of elevated competition, whereas HE homozygotes cope best when competition levels do not deviate from the norm. Thus, both alleles have long-term benefits when competition levels tend to vary substantially over relatively short timescales within a social group. We describe this hypothesis in detail and outline a series of predictions to test it. Some of these predictions are supported by findings in the current literature, while others remain areas of future research. © 2013 Dobson and Brent.
Abstract.
Brent LJN, Semple S, MacLarnon A, Ruiz-Lambides A, Gonzalez-Martinez J, Platt ML (2013). Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output. International Journal of Primatology, 1-22.
Brent LJN, MacLarnon A, Platt ML, Semple S (2013). Seasonal changes in the structure of rhesus macaque social networks.
Behavioral Ecology and Sociobiology,
67(3), 349-359.
Abstract:
Seasonal changes in the structure of rhesus macaque social networks
Social structure emerges from the patterning of interactions between individuals and plays a critical role in shaping some of the main characteristics of animal populations. The topological features of social structure, such as the extent to which individuals interact in clusters, can influence many biologically important factors, including the persistence of cooperation, and the rate of spread of disease. Yet, the extent to which social structure topology fluctuates over relatively short periods of time in relation to social, demographic, or environmental events remains unclear. Here, we use social network analysis to examine seasonal changes in the topology of social structures that emerge from socio-positive associations in adult female rhesus macaques (Macaca mulatta). Behavioral data for two different association types (grooming and spatial proximity) were collected for females in two free-ranging groups during two seasons: the mating and birth seasons. Stronger dyadic bonds resulted in social structures that were more tightly connected (i. e. of greater density) in the mating season compared to the birth season. Social structures were also more centralized around a subset of individuals and more clustered in the mating season than those in the birth season, although the latter differences were mostly driven by differences in density alone. Our results suggest a degree of temporal variation in the topological features of social structure in this population. Such variation may feed back on interactions, hence affecting the behaviors of individuals, and may therefore be important to take into account in studies of animal behavior. © 2012 Springer-Verlag Berlin Heidelberg.
Abstract.
Brent LJN, Melin AD (2013). The Genetic Basis of Primate Behavior: Genetics and Genomics in Field-Based Primatology. International Journal of Primatology, 1-10.
2012
Buhl JS, Aure B, Ruiz-Lambides A, Gonzalez-Martinez J, Platt ML, Brent LJN (2012). Response of Rhesus Macaques (Macaca mulatta) to the Body of a Group Member That Died from a Fatal Attack.
International Journal of Primatology,
33(4), 860-871.
Abstract:
Response of Rhesus Macaques (Macaca mulatta) to the Body of a Group Member That Died from a Fatal Attack
Among animals that form social bonds, the death of a conspecific may be a significant social event, representing the loss of an ally and resulting in disruptions to the dominance hierarchy. Despite this potential biological importance, we have only limited knowledge of animals' reactions to the death of a group member. This is particularly true of responses to dead adults, as most reports describe the responses of mothers to dead infants. Here, we describe in detail and provide video evidence of the behavioral responses of a group of free-ranging rhesus macaques (Macaca mulatta) immediately after the death of a mid-ranking adult male as a result of a fatal attack. High-ranking male members of the group, suspected to have carried out the attack, dragged and bit the dead body, exhibiting a rate of aggression 20 times greater than baseline levels. Lower-ranking individuals approached and inspected the body by looking closely, smelling, and grooming the fur. There was inconclusive evidence that these rhesus macaques found the death of a conspecific stressful: Levels of grooming between group members after the fatal attack were significantly higher than baseline levels, and higher than levels of grooming after nonfatal attacks. However, when grooming levels were adjusted based on the assumption that individuals positioned close to the body, i. e. those visible to researchers, were more likely to be engaged in grooming than those positioned farther away, this difference from baseline was no longer significant. The rate of self-directed behaviors after the fatal attack was also not different from baseline. Many of the behaviors we observed directed toward the body (aggression, inspection) have been previously reported in chimpanzees and geladas, and are similar to reactions sometimes displayed by humans. As such, this report represents a potentially valuable contribution the nascent field of nonhuman primate thanatology. © 2012 Springer Science+Business Media, LLC.
Abstract.
2011
Higham JP, Hughes KD, Brent LJN, Dubuc C, Engelhardt A, Heistermann M, Maestriperi D, Santos LR, Stevens M (2011). Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques.
Proceedings of the Royal Society B: Biological Sciences,
278(1723), 3452-3458.
Abstract:
Familiarity affects the assessment of female facial signals of fertility by free-ranging male rhesus macaques
Animals signal their reproductive status in a range of sensory modalities. Highly social animals, such as primates, have access not only to such signals, but also to prior experience of other group members. Whether this experience affects how animals interpret reproductive signals is unknown. Here, we explore whether familiarity with a specific female affects a male's ability to assess that female's reproductive signals. We used a preferential looking procedure to assess signal discrimination in free-ranging rhesus macaques, a species in which female facial luminance covaries with reproductive status. We collected images of female faces throughout the reproductive cycle, and using faecal hormone analysis to determine ovulation, categorized images as coming from a female's pre-fertile, ovulating, or post-fertile period. Weprinted colour-calibrated stimuli of these faces, reproducing stimuli perceptually the same in colour and luminance to the original appearance of females. These images were presented to males who were either unfamiliar or familiar with stimuli females. Overall, males distinguished ovulatory from pre-ovulatory faces. However, a significant proportion of males did so only among males familiar with stimuli females. These experiments demonstrate that familiarity may increase a receiver's ability to use a social partner's signals to discern their reproductive status. © 2011 the Royal Society.
Abstract.
Brent LJN, Semple S, Dubuc C, Heistermann M, MacLarnon A (2011). Social capital and physiological stress levels in free-ranging adult female rhesus macaques.
Physiology and Behavior,
102(1), 76-83.
Abstract:
Social capital and physiological stress levels in free-ranging adult female rhesus macaques
Social animals with greater access to social support, i.e. higher levels of social capital, may be able to cope better with the challenges they face in their day-to-day lives, and this may be reflected in lower physiological stress levels. Here, we examine the relationship between social capital and fecal glucocorticoid (GC) levels in pregnant free-ranging adult female rhesus macaques. In addition to social capital measures based on direct connections between social partners, which have been examined previously, we use social network analysis to generate measures of social capital based on indirect connections (i.e. connections between pairs of individuals which result from their mutual direct connection to a third party). We consider social capital based on three different types of affiliative association: grooming, the exchange of affiliative vocalizations and proximity. After controlling for variables known to affect GC output in primates (e.g. month of pregnancy), GC levels of females were significantly predicted by a social network measure of indirect connectedness in the proximity network, proximity reach, in interaction with dominance rank. High ranking females had significantly lower GC levels in months in which they had low levels of proximity reach (i.e. in months in which their proximity networks were smaller and therefore more focused). The results of our study add to a growing body of evidence which suggests that social capital may be an important means by which gregarious animals cope with day-to-day challenges. Our study also joins a small body of recent research which has demonstrated that indirect connections may be important factors in the lives of social animals. © 2010 Elsevier Inc.
Abstract.
Brent LJN, Lehmann J, Ramos-Fernandez G (2011). Social networks in the study of nonhuman primates: a historical perspective. American Journal of Primatology(73), 720-730.
2010
Higham JP, Brent LJN, Dubuc C, Accamando AK, Engelhardt A, Gerald MS, Heistermann M, Stevens M (2010). Color signal information content and the eye of the beholder: a case study in the rhesus macaque.
Behavioral Ecology,
21(4), 739-746.
Abstract:
Color signal information content and the eye of the beholder: a case study in the rhesus macaque
Animal coloration has provided many classical examples of both natural and sexual selection. Methods to study color signals range from human assessment to models of receiver vision, with objective measurements commonly involving spectrometry or digital photography. However, signal assessment by a receiver is not objective but linked to receiver perception. Here, we use standardized digital photographs of female rhesus macaque (Macaca mulatta) face and hindquarter regions, combined with estimates of the timing of the female fertile phase, to assess how color varies with respect to this timing. We compare objective color measures (camera sensor responses) with models of rhesus vision (retinal receptor stimulation and visual discriminability). Due to differences in spectral separation between camera sensors and rhesus receptors, camera measures overestimated color variation and underestimated luminance variation compared with rhesus macaques. Consequently, objective digital camera measurements can produce statistically significant relationships that are probably undetectable to rhesus macaques, and hence biologically irrelevant, while missing variation in the measure that may be relevant. Discrimination modeling provided results that were most meaningful (as they were directly related to receiver perception) and were easiest to relate to underlying physiology. Further, this gave new insight into the function of such signals, revealing perceptually salient signal luminance changes outside of the fertile phase that could potentially enhance paternity confusion. Our study demonstrates how, even for species with similar visual systems to humans, models of vision may provide more accurate and meaningful information on the form and function of visual signals than objective color measures do. © the Author 2010.
Abstract.
2009
Dubuc C, Brent LJN, Accamando AK, Gerald MS, MacLarnon A, Semple S, Heistermann M, Engelhardt A (2009). Sexual skin color contains information about the timing of the fertile phase in free-ranging macaca mulatta.
International Journal of Primatology,
30(6), 777-789.
Abstract:
Sexual skin color contains information about the timing of the fertile phase in free-ranging macaca mulatta
Females of several primate species undergo cyclical changes of their sexual skin, i.e. the development of a swelling or a change in color. The relationship between intracycle probability of fertility and the size of sexual swellings is well established, but in the only study to combine an objective measure of color with endocrinological data, researchers found no evidence that swelling color contains such information. To evaluate the role of female skin color in the context of sexual signaling further, we investigated whether changes in sexual skin color contain information about the timing of the fertile phase in rhesus macaques (Macaca mulatta), a species in which adult females do not develop sexual swellings, but do express visually detectable changes in the skin color of the face and hindquarters. Using an objective and quantitative measure of color, along with detailed data on fecal progestogen and estrogen metabolite levels collected from 8 females of the Cayo Santiago colony, we show that the ratio of red to green (R/G) for facial and hindquarter skin significantly varies throughout the ovarian cycle. In addition, facial skin R/G is significantly higher during the 5-d fertile phase versus the 5-d periods immediately before or after this time, but no such pattern occurs in hindquarter R/G. This suggests that skin color change in female rhesus macaques may potentially signal information about the intracycle probability of fertility to male receivers, but that only facial skin color may signal reliable information about its timing. © 2009 Springer Science+Business Media, LLC.
Abstract.
2008
Brent LJN, Teichroeb JA, Sicotte P (2008). Preliminary assessment of natal attraction and infant handling in wild Colobus vellerosus. American Journal of Primatology, 70(1), 101-105.
2002
Brent LJN, Drapeau P (2002). Targeted 'knockdown' of channel expression in vivo with an antisense morpholino oligonucleotide.
Neuroscience,
114(2), 275-278.
Abstract:
Targeted 'knockdown' of channel expression in vivo with an antisense morpholino oligonucleotide
We have examined whether antisense morpholino oligonucleotides (morpholinos) can be used as a tool to suppress or 'knockdown' the expression of ion channels during development of the zebrafish. Because the acetylcholine receptor channel is well characterized in zebrafish and is abundant as skeletal muscle is found throughout the body, we sought to knock down its expression as a general test of the feasibility of this approach. A 25-mer morpholino was designed to target the 5′ region of the cloned α-subunit and was injected into early stage blastulae in order to trap it in all developing cells. From the time of hatching (early on the third day of development) and for a few days after, a fraction of the injected embryos were immobile, i.e. were 'morphant'. Injection of blastulae without the morpholino or with a control morpholino containing four mispaired bases did not affect the embryos. Although the morphant embryos were generally normal in appearance, they lacked staining with α-bungarotoxin or an α-subunit-specific monoclonal antibody. In whole muscle cell recordings from morphant embryos, miniature end-plate potentials were undetectable in many of the cells and in most they had a slower, immature time course. These results are consistent with a greatly reduced, dysfunctional level of expression of acetylcholine receptors in morphant embryos. Because of their stability and specificity, morpholinos should prove useful for targeted deletion of transmitter receptors and channels in developing zebrafish and possibly in other preparations. © 2002 IBRO. Published by Elsevier Science Ltd. All rights reserved.
Abstract.
