bioRxiv Science⌕ Search

Biology subjects

Samuni, L.

Publications and source records attributed to Samuni, L..

11 recordsLinked to original sources

The building blocks of social structure: simulating constraints of social network analysis for inference about group-level properties

The interdisciplinary usage of Social Network Analysis (SNA) means that, when researchers calculate global network metrics, the research interest can range from the ultimate ecological and evolutionary pressures that select for specific group-level structures or the proximate mechanisms by which those structures emerge. Despite major methodological advances, social structures measured via SNA metrics are rarely connected to the underlying forces shaped by latent individual dispositions, ecological constraints, and their interplay with group-level affordances. We build a model to simulate fission-fusion spatial association data from a specified set of parameters in order to address the "black box" of animal SNA. We broke down animal social systems into three building blocks: individual dispositions, external factors, and the social structure that emerges. Each of these building blocks was represented by one or more model parameters, which together describe a set of underlying processes that lead to different measurable features of animal social structure, which we quantified with commonly used global network metrics within an SNA framework (e.g., clustering coefficient, density, modularity). In doing so, our model directly links global network metrics to the underlying behavioural processes that generate them and demonstrates how global network metrics can be influenced by changes to their underlying behavioural processes. Holding all other parameters constant, we find that subtle changes to 1) demography (i.e., group size) and ecology (i.e., size and variability of foraging parties), 2) variation of individual behaviour and related observation bias, 3) imposed group sub-structures, and 4) observation effort, affect all network metrics calculated non-linearly and in some cases non-monotonically. Our findings indicate that failure to account for the underlying behavioural processes can bias inference drawn from SNA. This model and conceptual framework provide a novel tool with which to begin opening the black box of SNA and to systematically address the evolution of diverse group-level social structures.

animal behavior and cognition↗

Evolution of Menopause and the Mamas Boy Hypothesis

Post-reproductive lifespan is an evolutionary puzzle. In most mammals female fertility tracks survival, yet humans and a few toothed whales show survival after reproduction ends. Explaining when and why post-reproductive lifespan evolves is central to understanding the evolution of ageing, social structure, and intergenerational helping across species. Kinship-dynamics theory predicts that when males are philopatric, a females local relatedness--especially to male descendants--increases with age, potentially favoring late-life helping over continued reproduction. We develop an age-sex-structured kin-selection model to test whether a rare menopause-inducing modifier allele can invade an initially non-menopausal population through its direct effects on survival and fecundity and its indirect effects on relatives. We consider two evolutionary pathways: stop early, where reproduction ceases earlier with little change in lifespan, and live long, where lifespan extends beyond reproduction under disposable-soma trade-offs. Parameterized with demographic, dispersal, and helping-effect estimates from eight mammalian taxa, the model predicts empirically plausible ages of reproductive cessation and post-reproductive representation in humans and killer whales, but no invasion across plausible cessation ages in non-menopausal taxa. Global sensitivity analyses identify male dispersal and the effect of post-reproductive help on male survival as determinants of whether menopause evolves, motivating the "mamas boy hypothesis": menopause is most strongly favoured by selection when late-life care increases the survival and lifetime fitness of philopatric sons and grandsons.

evolutionary biology↗

Wild chimpanzee groups increase social connectivity prior to risky collective action

Cooperation is foundational to complex sociality, yet presents profound evolutionary dilemmas - costs and benefits are rarely distributed evenly and the decision to collaborate or defect can involve a complex contextual calculus. These challenges are compounded when cooperation scales from pairs to groups. Group-level cooperation is fundamental to many species success, but how is it sustained and regulated in nature? One promising route to addressing this question is to examine how individuals reorganise their affiliative interactions in anticipation of group-level cooperation. We examine such pre-cooperative reorganisation using long-term data (2013-2018) from three neighbouring groups of wild chimpanzees at the Tai National Park, Cote dIvoire, who routinely cooperate as a collective to defend their territory against other groups. We found that chimpanzees adjusted the distribution of their social contacts in anticipation of risky and proactive territorial defence by forming more broadly connected, yet more diffuse, affiliative networks. Specifically, adult chimpanzees groomed and played with more group members on days of proactive territorial defence, and this pattern was temporally-sensitive, with increased affiliation occurring before, rather than after, the cooperative act. Chimpanzees accessed a broader range of partners through increased interaction efficiency by switching between more partners with shorter interactions per partner. This pattern suggests a shared evolutionary basis of dynamic social readjustment in preparation for group-level social dilemmas in hominids, potentially providing the foundation for the formalized systems of affiliation found in human societies.

animal behavior and cognition↗

Sex differences in pant-hoot vocalizations in wild Eastern chimpanzees

Chimpanzee pant-hoots are frequently produced long-distance vocalisations that serve a number of social functions, such as to indicate coordinate travelling, food discovery, or social status. Calling often triggers replies by others, offering potential for some form of group-level decision-making through vocal exchanges. However, despite important physiological and social differences between male and female chimpanzees, pant-hoot research has traditionally focused on males, with very little known about female use. To address this gap, we collected all-occurrence behavioural data from wild adult female and male Eastern chimpanzees (Pan troglodytes schweinfurthii) in two communities in the Budongo Forest Reserve, Uganda. We show that females pant-hooted regularly, but less frequently than males and, when they did so, mostly in response to others. Response pant- hoots were more common than initiating pant-hoots in both sexes (females: 90.1%; males: 69.5%), and male and female chimpanzees responded to pant-hoots heard at a similar rate (females: 14.1%, males excluding alpha: 15.8%). Both sexes were more likely to respond to pant-hoots from within their own party, but this effect was stronger for females. The likelihood of male chimpanzees pant-hooting in response was inhibited in larger party sizes, while females response pant-hoots were not. Finally, female response pant-hoots were less common during periods of maximal oestrous as compared to other stages of their reproductive cycle. Overall, our findings demonstrate that response pant-hoots are subject to social factors, such as within-sex social competition and between-sex reproductive strategies, which affect male and female chimpanzees in different ways, a further demonstration of the high degree of audience awareness in this primate species. HighlightsO_LIChimpanzees use pant-hoots in both sex-specific and sex-non-specific ways C_LIO_LIIndividual and social factors impact likelihood of pant-hoot production C_LIO_LIOur findings suggest pant-hoots are important flexible elements of vocal behaviour for male and female chimpanzees. C_LI

animal behavior and cognition↗

Flexibility in the social structure of male chimpanzees (Pan troglodytes schweinfurthii) in the Budongo Forest, Uganda

Individuals of social species face a trade-off between the competitive costs and social benefits of group living. Species show a range of social strategies to deal with this trade-off, for example atomistic fission-fusion dynamics in which temporary social groups of varying size and membership form and re-form; or molecular fission-fusion dynamics which contain stable sets of multilevel nested subgroups. Chimpanzees are considered an archetypical atomistic fission-fusion species, using dynamic changes in day-to-day association to moderate the costs of within-group competition. It has been argued that humans highly flexible social organisation allows us to live in extremely large groups. Using four years of association data from two neighbouring communities of East African chimpanzees (Pan troglodytes schweinfurthii), we describe new levels of flexibility in chimpanzee social organisation and confirm the presence of subgrouping in a second, large community of chimpanzees. We show that males from the larger Waibira community (N males 24-31) exhibited additional levels of semi-stable subgrouping, while males from the smaller Sonso community (N males 10-13) did not. Subgroup membership showed stability across some years, but flexibility across others. Our data support the hypothesis that chimpanzees can incorporate strategies other than fission-fusion to overcome costs of social living, and that their social organisation may be closer to that of modern humans than previously described. SIGNIFICANCE STATEMENTSocial living offers benefits and costs; groups can more easily locate and defend resources, but experience increased individual competition. Many species, or individuals, flexibly adjust their social organization when faced with different competitive pressures. It is argued that humans are unique among primates in combining multigroup social organisation with fission-fusion dynamics flexibly within and across groups, and that doing so allows us to live in extremely large groups. Using four-years of association data we show new levels of flexibility in chimpanzee social organization. Males from a typically-sized community employed atomistic fission-fusion dynamics, but males in an unusually large community incorporated additional semi-stable levels of subgrouping. Our data support the hypothesis that chimpanzee males combine social organization strategies, and that doing so may allow them, like humans, to mitigate individual costs at larger community sizes.

animal behavior and cognition↗

Evaluating the efficacy of a consumer-centric method for ecological sampling: Using bonobo (Pan paniscus) feeding patterns as an instrument for tropical forest characterization

O_LICharacteristics of food availability and distribution are a key component of a species ecology. Objective measurement of food resources, such as vegetation plot sampling, do not consider aspects of selection by the consumer and therefore may produce imprecise measures of availability. Further, in most animal ecology research, traditional ecological surveying often is time-intensive and supplementary to ongoing behavioral observation. We propose a method to integrate ecological sampling of an animals environment into existing behavioral data collection systems by using the consumer as the surveyor. Here, we introduce the consumer-centric method (CCM) of assessing resource availability for its ability to measure food resource abundance, distribution, and dispersion. This method catalogues feeding locations observed during behavioral observation and uses aggregated data to characterize these ecological metrics. C_LIO_LIWe evaluated the CCM relative to traditional vegetation plot surveying using accumulated feeding locations across three years visited by a tropical frugivore, the bonobo (Pan paniscus), and compared it with data derived from over 200 vegetation plots across their 50km2+ home range. C_LIO_LIWe demonstrate that food species abundance estimates derived from the CCM are comparable to those derived from traditional vegetation plot sampling after approximately 600 observation days or 60 spatially explicit feeding locations. The agreement between the methods further improved when accounting for aspects of consumer selectivity in objective vegetation plot sampling (e.g., size minima). Estimates of density from CCM correlated with plot-derived estimates and were relatively insensitive to home range inclusion and other species characteristics, but were sensitive to sampling frequency (e.g., consumption frequency). Agreement between the methods in relative distribution of resources performed better across species than expected by chance, although measures of dispersion correlated poorly. C_LIO_LIWe demonstrate that while providing a robust measure to quantify local food availability, the CCM has an advantage over traditional sampling methods as it incorporates sampling biases relevant to the consumer. Therefore, as this method can be incorporated into existing observational data collection and does not require additional ecological surveying, it serves as a promising method for behavioral ecological data collection for animal species who re-use space and consume immobile food items. C_LI

ecology↗

Non-genetic maternal effects shape individual differences in cortisol phenotypes in wild chimpanzees

Glucocorticoids, such as cortisol, mediate homeostatic processes, allowing individuals to adjust to fluctuating environments. The regulation of circadian cortisol responses, a key homeostatic function, has been shown to be heritable. However, to understand better the role of parental care in shaping physiological functioning in long-lived mammals with protracted parental care, there is a need to disentangle genetic and non-genetic parental contributions to variation in glucocorticoid phenotypes. We used a dataset of 6,123 cortisol measures from urine samples from 170 wild chimpanzees spanning 18 years of data collection. We found consistent inter-individual differences in circadian cortisol phenotypes, with differences most apparent when considering average cortisol levels given the effect of time of day. Maternal effects explained around 10% (2-18%) variation in these average cortisol levels, while variation attributable to genetic factors was not distinguishable from zero. Our results indicate, relative to genetic effects, a qualitatively stronger influence of mothers, whether via epigenetic processes or via behavioral priming for coping with stressors, in shaping cortisol phenotypes in this species. This provides novel insight into the vital role of mothers in the developmental plasticity of long-lived mammals and, more generally, the selective pressures shaping physiological plasticity.

zoology↗

Accuracy and Precision of Social Relationship Indices

Combining interaction rates of different social behaviours into social relationship indices to represent the structure of dyadic relationships on one underlying dimension is common practice in animal sociality studies. However, the properties of these relationship indices are not well explored - mainly because, for real-world social systems, the true value of relationships is unobservable. Here, we use simulation studies to estimate the accuracy and precision of three relationship indices: the Dyadic Composite Sociality Index, the Composite Relationship Index, and the Dynamic Dyadic Sociality Index. We simulated one year of social interactions for multiple groups of 25 individuals and 4 interaction types with different properties, and tested the impact of different focal follow regimes, data densities and sampling conditions on the representation of social relationships. Accuracy and precision of social relationship indices were strongly driven by sample size, similar to simple interaction rates. Under the assumption that there was a clear, one-dimensional relationship underlying interactions, and that different interaction types constituting an index were highly correlated, indices indeed increased accuracy over single interaction rates for small sample sizes. Including uninformative constituting behaviours (i.e., those not highly correlated with the underlying relationship dimension) reduced the accuracy of all indices. The precision of each index (i.e., whether multiple simulated focal follow regimes achieve the same dyadic values for the same data) was generally poor and was driven by the precision of the least precise constituting behaviour, making them less precise than some single interaction rates. Our results showed that social relationship indices do not remove the need to have sufficient data for each individual constituting interaction type. Index quality was defined by the least accurate and precise constituting interaction type. Indices might only be useful if all constituting interaction rates are highly correlated and if there are clear indications that one dimension is sufficient to represent social relationships in a group.

zoology↗

Behavioural diversity of bonobo prey preference as a potential cultural trait

The importance of cultural processes to behavioural diversity, especially in our closest living relatives, is central for revealing the evolutionary origins of human culture. Whereas potential cultural traits are extensively investigated in chimpanzees, our other closest living relative, the bonobo, is often overlooked as a candidate model. Further, a prominent critique to many examples of proposed animal cultures is premature exclusions of environmental confounds known to shape behavioural phenotypes. We addressed these gaps by investigating variation in prey preference expression between neighbouring bonobo groups that associate and share largely overlapping home ranges. We find specific group preference for duiker or anomalure hunting that are otherwise unexplained by variation in spatial usage of hunt locations, seasonality or sizes of hunting parties. Our findings demonstrate that group-specific behaviours emerge independently of the local ecology, indicating that hunting techniques in bonobos may be culturally transmitted. We suggest that the tolerant intergroup relations of bonobos offer an ideal context to explore drivers of behavioural phenotypes, the essential investigations for phylogenetic constructs of the evolutionary origins of culture.Competing Interest StatementThe authors have declared no competing interest.View Full Text

animal behavior and cognition↗

Increased Sensitivity and Signal-to-Noise Ratio in Diffusion-Weighted MRI using Multi-Echo Acquisitions

Post-mortem diffusion MRI (dMRI) enables acquisitions of structural imaging data with otherwise unreachable resolutions - at the expense of longer scanning times. These data are typically acquired using highly segmented image acquisition strategies, thereby resulting in an incomplete signal decay before the MRI encoding continues. Especially in dMRI, with low signal intensities and lengthy contrast encoding, such temporal inefficiency translates into reduced image quality and longer scanning times. This study introduces Multi Echo (ME) acquisitions to dMRI on a human MRI system - a time-efficient approach, which increases SNR (Signal-to-Noise Ratio) and reduces noise bias for dMRI images. The benefit of the introduced ME dMRI method was validated using numerical Monte Carlo simulations and showcased on a post-mortem brain of a wild chimpanzee. The proposed Maximum Likelihood Estimation echo combination results in an optimal SNR without detectable signal bias. The combined strategy comes at a small price in scanning time (here 30% additional) and leads to a substantial SNR increase (here up to 1.9x which is equivalent to 3.6 averages) and a general reduction of the noise bias.

neuroscience↗

Long-term repeatability in social behaviours suggests stable social phenotypes in wild chimpanzees

Animals living in social groups navigate challenges when competing and cooperating with other group members. Changes in demographics, dominance hierarchies or ecological factors, such as food availability or disease prevalence, are expected to influence decision-making processes regarding social interactions. Therefore, it could be expected individuals show flexibility in social behaviour over time to maximise the fitness benefits of social living. To date, research across species has shown that stable inter-individual differences in social behaviour exist, but mostly over relatively short data collection time periods. Using data spanning over 20 years, we demonstrate that multiple social behaviours are repeatable over the long-term in wild chimpanzees, a long-lived species occupying a complex fission-fusion society. We controlled for temporal, ecological and demographic changes, limiting pseudo-repeatability. We conclude that chimpanzees living in natural ecological settings have relatively stable long-term social phenotypes over years that may be independent of life history stage or strategies. Our results add to the growing body of literature suggesting consistent individual differences in social tendencies are more likely the rule rather than the exception in group-living animals.

animal behavior and cognition↗