Coevolution of pathogens and cultural practices: a new look at behavioral heterogeneity in epidemics

The effect of heterogeneity within populations on the spread of infectious diseases has been a recent focus of research. Such heterogeneity may be, for example, spatial, temporal or behavioral in form. Generally, models that include population subdivision have assumed that individuals are permanently assigned to given behavioral states represented by the subpopulations. We consider a simple epidemic model in which a behavioral trait affects disease transmission, and this trait may be transferred among hosts as a consequence of social interaction. This creates a situation where the frequencies of different behavioral traits and disease states as well as their associations may change over time. We consider the impact of the culturally transmitted trait on the criterion for initial spread of the disease. We also explore the evolution of cultural traits in response to pathogen dynamics and show some conditions under which behavioral traits that reduce transmission evolve. We find that behaviors increasing the risk of infection can also evolve when they are inherently favored or when there is sufficient clustering of contacts between like behaviors.     

A neurodynamic account of spontaneous behaviour

The current article suggests that deterministic chaos self-organized in cortical dynamics could be responsible for the generation of spontaneous action sequences. Recently, various psychological observations have suggested that humans and primates can learn to extract statistical structures hidden in perceptual sequences experienced during active environmental interactions. Although it has been suggested that such statistical structures involve chunking or compositional primitives, their neuronal implementations in brains have not yet been clarified. Therefore, to reconstruct the phenomena, synthetic neuro-robotics experiments were conducted by using a neural network model, which is characterized by a generative model with intentional states and its multiple timescales dynamics. The experimental results showed that the robot successfully learned to imitate tutored behavioral sequence patterns by extracting the underlying transition probability among primitive actions. An analysis revealed that a set of primitive action patterns was embedded in the fast dynamics part, and the chaotic dynamics of spontaneously sequencing these action primitive patterns was structured in the slow dynamics part, provided that the timescale was adequately set for each part. It was also shown that self-organization of this type of functional hierarchy ensured robust action generation by the robot in its interactions with a noisy environment. This article discusses the correspondence of the synthetic experiments with the known hierarchy of the prefrontal cortex, the supplementary motor area, and the primary motor cortex for action generation. We speculate that deterministic dynamical structures organized in the prefrontal cortex could be essential because they can account for the generation of both intentional behaviors of fixed action sequences and spontaneous behaviors of pseudo-stochastic action sequences by the same mechanism.     

«Active» selection may participate in the evolution of primates

Selection pressures in the evolution of morphological characters which are exclusive to primates were discussed. While the evolutionary change in some morphological characters of primates can be explained by natural or sexual selection, there are also morphological characters of primates, such as some regions of neocortices, which are involved in social interactions and whose evolutionary changes can hardly be explained by natural or sexual selection alone. Furthermore, recent studies have demonstrated that relative sizes of brain, neocortex and some thalamic nuclei of brains differ significantly by social structure in primates. Based on these and other findings, we propose here that “active” selection pressures may have favored a variety of morphological characters related to social interactions, the selection pressures which are derived from social interactions and are operative within animals or troops. The introduction of concept of active selection will be useful in developing conceptual frameworks for understanding of the mechanism of evolution of primates, in particular, of hominids.     

Understanding primate brain evolution

We present a detailed reanalysis of the comparative brain data for primates, and develop a model using path analysis that seeks to present the coevolution of primate brain (neocortex) and sociality within a broader ecological and life-history framework. We show that body size, basal metabolic rate and life history act as constraints on brain evolution and through this influence the coevolution of neocortex size and group size. However, they do not determine either of these variables, which appear to be locked in a tight coevolutionary system. We show that, within primates, this relationship is specific to the neocortex. Nonetheless, there are important constraints on brain evolution; we use path analysis to show that, in order to evolve a large neocortex, a species must first evolve a large brain to support that neocortex and this in turn requires adjustments in diet (to provide the energy needed) and life history (to allow sufficient time both for brain growth and for 'software' programming). We review a wider literature demonstrating a tight coevolutionary relationship between brain size and sociality in a range of mammalian taxa, but emphasize that the social brain hypothesis is not about the relationship between brain/neocortex size and group size per se; rather, it is about social complexity and we adduce evidence to support this. Finally, we consider the wider issue of how mammalian (and primate) brains evolve in order to localize the social effects.     

Social plasticity in fish: integrating mechanisms and function

Social plasticity is a ubiquitous feature of animal behaviour. Animals must adjust the expression of their social behaviour to the nuances of daily social life and to the transitions between life‐history stages, and the ability to do so affects their Darwinian fitness. Here, an integrative framework is proposed for understanding the proximate mechanisms and ultimate consequences of social plasticity. According to this framework, social plasticity is achieved by rewiring or by biochemically switching nodes of the neural network underlying social behaviour in response to perceived social information. Therefore, at the molecular level, it depends on the social regulation of gene expression, so that different brain genomic and epigenetic states correspond to different behavioural responses and the switches between states are orchestrated by signalling pathways that interface the social environment and the genotype. At the evolutionary scale, social plasticity can be seen as an adaptive trait that can be under positive selection when changes in the environment outpace the rate of genetic evolutionary change. In cases when social plasticity is too costly or incomplete, behavioural consistency can emerge by directional selection that recruits gene modules corresponding to favoured behavioural states in that environment. As a result of this integrative approach, how knowledge of the proximate mechanisms underlying social plasticity is crucial to understanding its costs, limits and evolutionary consequences is shown, thereby highlighting the fact that proximate mechanisms contribute to the dynamics of selection. The role of teleosts as a premier model to study social plasticity is also highlighted, given the diversity and plasticity that this group exhibits in terms of social behaviour. Finally, the proposed integrative framework to social plasticity also illustrates how reciprocal causation analysis of biological phenomena (i.e. considering the interaction between proximate factors and evolutionary explanations) can be a more useful approach than the traditional proximate–ultimate dichotomy, according to which evolutionary processes can be understood without knowledge on proximate causes, thereby black‐boxing developmental and physiological mechanisms.     

Beyond Contagion: Reality Mining Reveals Complex Patterns of Social Influence

Contagion, a concept from epidemiology, has long been used to characterize social influence on people’s behavior and affective (emotional) states. While it has revealed many useful insights, it is not clear whether the contagion metaphor is sufficient to fully characterize the complex dynamics of psychological states in a social context. Using wearable sensors that capture daily face-to-face interaction, combined with three daily experience sampling surveys, we collected the most comprehensive data set of personality and emotion dynamics of an entire community of work. From this high-resolution data about actual (rather than self-reported) face-to-face interaction, a complex picture emerges where contagion (that can be seen as adaptation of behavioral responses to the behavior of other people) cannot fully capture the dynamics of transitory states. We found that social influence has two opposing effects on states: adaptation effects that go beyond mere contagion, and complementarity effects whereby individuals’ behaviors tend to complement the behaviors of others. Surprisingly, these effects can exhibit completely different directions depending on the stable personality or emotional dispositions (stable traits) of target individuals. Our findings provide a foundation for richer models of social dynamics, and have implications on organizational engineering and workplace well-being.     

Dynamics of the interaction of hypothalamic, reticular and limbic structures and the neocortex as affected by corticosteroids

The neurophysiological analysis of the hypothalamo-reticulo-lambic structures and neocortex and dynamics of their relationship simultaneously with the content determination of the corticosteroids in rats and rabbits blood under the influence of hydrocortisone and 11-deoxycorticosterone has been carried out. It has been shown that the hypothalamo-reticulo-limbic system are involved under the action of adrenal hormones. Under the influence of corticosteroids the dynamics of changes of these structures ensuring the functions of hypophysal-adrenal complex are condition to transfer the neuroendocrine system into the new state forming definite behavioral reactions to support homeostasis.     

Understanding Behavioral Traditions in Primates: Are Current Experimental Approaches Too Focused on Food?

Recently, several researchers have highlighted the neglect of social behaviors relative to food-related behaviors in experimental research on social learning in primates, despite the significant number of apparent social traditions reported in the field. Here we aim to highlight the discrepancy between the relative number of nonfood-related behavioral traditions reported in the wild and food-related ones, and the almost exclusive investigation of food-related behaviors in an experimental context. First we discuss aspects of social and communicative customs that make them especially interesting. Then we consider reasons why experimental approaches are crucial to developing a full understanding of behavioral traditions observed in the wild. We report the results of a systematic literature survey in which we assessed the perceived discrepancy quantitatively. We also argue that the existing experimental literature, with its typical reliance on food as a motivator, may not be sufficient to elucidate the mechanisms underlying nonfood traditions, such as social conventions. Finally, we suggest new directions for the experimental investigation of social learning in primates, hoping to stimulate experimental research investigating social and communicative behavioral traditions.     

Comprehensive analysis of locomotion dynamics in the protochordate Ciona intestinalis reveals how neuromodulators flexibly shape its behavioral repertoire

Vertebrate nervous systems can generate a remarkable diversity of behaviors. However, our understanding of how behaviors may have evolved in the chordate lineage is limited by the lack of neuroethological studies leveraging our closest invertebrate relatives. Here, we combine high-throughput video acquisition with pharmacological perturbations of bioamine signaling to systematically reveal the global structure of the motor behavioral repertoire in the Ciona intestinalis larvae. Most of Ciona’s postural variance can be captured by 6 basic shapes, which we term “eigencionas.” Motif analysis of postural time series revealed numerous stereotyped behavioral maneuvers including “startle-like” and “beat-and-glide.” Employing computational modeling of swimming dynamics and spatiotemporal embedding of postural features revealed that behavioral differences are generated at the levels of motor modules and the transitions between, which may in part be modulated by bioamines. Finally, we show that flexible motor module usage gives rise to diverse behaviors in response to different light stimuli.

Vertebrate nervous systems can generate a remarkable diversity of behaviors, but how did these evolve in the chordate lineage? A study of the protochordate Ciona intestinalis reveals novel insights into how a simple chordate brain uses neuromodulators to control its behavioral repertoire.     

The orchestration of conscious experience by subcortical structures

It is argued that conscious emotional feelings can not be adequately explained by just particular circuits or coherent activations within the brain, as is conventionally believed; nor by activations representing environmental stimuli going to the brain. According to the model suggested herein, the limbic system responds to sensory and other inputs according to how closely they are associated with built‐in rewards or punishments. It does this by (a) activating the autonomic nervous system so that it prepares the body to acquire a reward or avoid a punishment, and (b) also activating the prefrontal cortex (PFC). The PFC activations are temporally correlated with the autonomic activations and the feedback to them, so that they become identified with the autonomic attempts to acquire (a reward) or avoid (a punishment). The PFC circuit thus acquires a valence. The valence, along with arousal in a given context, underlies conscious emotional feelings. The model is related to: (a) how attention progresses along networks within working memory; (b) how a single, unified percept is formed; (c) how both value‐based and cognitive‐based responses are formulated; and (d) how the stream of consciousness is put together and driven forward. These concepts are integrated into a scenario of the orchestration of conscious experience and behaviour by subcortical‐limbic system structures interacting with the cortex, and are shown to be consistent with much of the literature.     

Historical and ecological controls on phylogenetic diversity in Californian plant communities

An unresolved controversy regarding social behaviors is exemplified when natural selection might lead to behaviors that maximize fitness at the social-group level but are costly at the individual level. Except for the special case of groups of clones, we do not have a general understanding of how and when group-optimal behaviors evolve, especially when the behaviors in question are flexible. To address this question, we develop a general model that integrates behavioral plasticity in social interactions with the action of natural selection in structured populations. We find that group-optimal behaviors can evolve, even without clonal groups, if individuals exhibit appropriate behavioral responses to each other's actions. The evolution of such behavioral responses, in turn, is predicated on the nature of the proximate behavioral mechanisms. We model a particular class of proximate mechanisms, prosocial preferences, and find that such preferences evolve to sustain maximum group benefit under certain levels of relatedness and certain ecological conditions. Thus, our model demonstrates the fundamental interplay between behavioral responses and relatedness in determining the course of social evolution. We also highlight the crucial role of proximate mechanisms such as prosocial preferences in the evolution of behavioral responses and in facilitating evolutionary transitions in individuality.     

Internal dynamics determine the cortical response to thalamic stimulation

Although spontaneous activity occurs throughout the neocortex, its relation to the activity produced by external or sensory inputs remains unclear. To address this, we used calcium imaging of mouse thalamocortical slices to reconstruct, with single-cell resolution, the spatiotemporal dynamics of activity of layer 4 in the presence or absence of thalamic stimulation. We found spontaneous neuronal coactivations corresponded to intracellular UP states. Thalamic stimulation of sufficient frequency (>10 Hz) triggered cortical activity, and UP states, indistinguishable from those arising spontaneously. Moreover, neurons were activated in identical and precise spatiotemporal patterns in thalamically triggered and spontaneous events. The similarities between cortical activations indicate that intracortical connectivity plays the dominant role in the cortical response to thalamic inputs. Our data demonstrate that precise spatiotemporal activity patterns can be triggered by thalamic inputs and indicate that the thalamus serves to release intrinsic cortical dynamics.     

Complexities of Using Wild versus Captive Activity Budget Comparisons for Assessing Captive Primate Welfare

Activity budget comparisons between groups or individuals in the wild and those in captivity are commonly used to determine the range of wild-type behaviors that nonhuman animals in captivity perform. These comparisons are conducted with the view that individuals displaying a greater range of wild-type behaviors have enhanced welfare. Such comparisons have a greater appeal when it comes to primates because increased levels of anthropomorphism toward primates lead to welfare concerns. However, the validity of such comparisons has not been assessed. From the reviewed literature, some of the main complexities identified when defining “good welfare” using activity budgets were the ideas of behavioral motivation and adaptation, obstacles when using the wild as a benchmark for good welfare, study methods causing possible variances in behavior, and social and environmental factors. It is proposed that such influencing factors would be controlled for adequately in future studies with the use of multiple indices to measure welfare and methods that infer positive emotional states. It is hoped we can then build evidence of an animal’s emotional state and allow welfare to be inferred to a higher degree.     

Stochastic state transitions give rise to phenotypic equilibrium in populations of cancer cells

Cancer cells within individual tumors often exist in distinct phenotypic states that differ in functional attributes. While cancer cell populations typically display distinctive equilibria in the proportion of cells in various states, the mechanisms by which this occurs are poorly understood. Here, we study the dynamics of phenotypic proportions in human breast cancer cell lines. We show that subpopulations of cells purified for a given phenotypic state return towards equilibrium proportions over time. These observations can be explained by a Markov model in which cells transition stochastically between states. A prediction of this model is that, given certain conditions, any subpopulation of cells will return to equilibrium phenotypic proportions over time. A second prediction is that breast cancer stem-like cells arise de novo from non-stem-like cells. These findings contribute to our understanding of cancer heterogeneity and reveal how stochasticity in single-cell behaviors promotes phenotypic equilibrium in populations of cancer cells.     

A control theoretic model of the forearm

In this paper, a control theoretic model of the forearm is developed and analyzed, and a computational method for predicting muscle activations necessary to generate specified motions is described. A detailed geometric model of the forearm kinematics, including the carrying angle and models of how the biceps and the supinator tendons wrap around the bones, is used. Also, including a dynamics model, the final model is a system of differential equations where the muscle activations play the role of control signals. Due to the large number of muscles, the problem of finding muscle activations is redundant, and this problem is solved by an optimization procedure. The computed muscle activations for ballistic movements clearly recaptures the triphasic ABC (Activation-Braking-Clamping) pattern. It is also transparent, from the muscle activation patterns, how the muscles cooperate and counteract in order to accomplish desired motions. A comparison with previously reported experimental data is included and the model predictions can be seen to be partially in agreement with the experimental data.     

Assessments made easier: examining the use of a rating-based questionnaire to capture behavioral data in rehabilitant orangutans (Pongo pygmaeus morio)

Rehabilitation and release are commonly used for confiscated, surrendered, and rescued primates. To improve release efficacy it is important to generate accurate behavioral profiles of release candidates. Research on primates traditionally uses observer ratings to measure individual differences. This method is easily implemented, but its validity has been questioned. We evaluated whether observer ratings reflect behavioral data indicating forest adaptation in 18 free-ranging rehabilitant orangutans (Pongo pygmaeus morio). In 2017, we used a species-specific questionnaire to measure how often orangutans engaged in behaviors linked to living successfully in the wild (e.g., nest building) and the extent to which they express personality traits that may influence forest adaptation. We collected 11 months of observational data on 17 of the orangutans concurrently to validate the questionnaire items, and collected further questionnaire data for 16 of the individuals in 2019. We used regularized exploratory factor analysis (REFA) and parallel analysis to condense the ratings and determine that two factors could be reliably extracted. We conducted another REFA using the observational data, and calculated factor congruence coefficients following procrustean rotation. The first of the two factors represented forest skills and human aversion, and was congruent with observational data. The second factor reflected boldness, sociability, and exploration, and was not congruent with observational data. Ratings correlated significantly with observations for all five questionnaire items reflecting adaptation to forest life, and for three of seven items reflecting personality traits. We conclude that ratings can be a valid approach to obtain individual-based behavioral information reflecting forest adaptation in free-ranging rehabilitant orangutans, and may be particularly useful in summarizing behaviors relevant to forest adaptation that are otherwise challenging to gather in primates.

     

Perspectives and prospects

The study of the nonhuman primates offers great opportunities for the development of an experimental anthropology. Whether one is concerned with variations in sutures, in locomotor patterns or the distribution of genetic polymorphisms, study of the nonhuman primates may offer clues. Whether one is interested in adaptation to desert, to tropic heat, or to cold, the nonhuman primate offers a far greater range of variations than man. For many problems they are the laboratory animals of choice, and their exploitation is necessary if we are ever to have an experimental physical anthropology. Interest in the nonhuman primates brings us into touch with many other sciences, as has been shown at this symposium. But I would particularly stress how it strengthens the relations of the parts of anthropology. The social system, communication, learning, these problems are important to all of anthropology, and the study of evolution, and particularly of our nearest relatives, has much to offer to the understanding of man and his behaviors.     

Testing for personality consistency across naturally occurring behavioral contexts in sanctuary chimpanzees (Pan troglodytes)

Personality is both a reflection of the bio-behavioral profile of individuals and a summary of how they typically interact with their physical and social world. Personality is usually defined as having distinct behavioral characteristics, which are assumed to be consistent over time and across contexts. Like other mammals, primates have individual differences in personality. Although temporal consistency is sometimes measured in primates, and contextual consistency is sometimes measured across experimental contexts, it is rare to measure both in the same individuals and outside of experimental settings. Here, we aim to measure both temporal and contextual consistency in chimpanzees, assessing their personality with behavioral observations from naturally occurring contexts (i.e., real-life settings). We measured personality-based behaviors in 22 sanctuary chimpanzees, in the contexts of feeding, affiliation, resting, and solitude, across two time periods, spanning 4 years. Of the 22 behaviors recorded, about 64% were consistent across two to four contexts and 50% were consistent over time. Ten behaviors loaded significantly onto three trait components: explorativeness, boldness-sociability, and anxiety-sociability, as revealed by factor analysis. Like others, we documented individual differences in the personality of chimpanzees based on reliably measured observations in real-life contexts. Furthermore, we demonstrated relatively strong, but not absolute, temporal, and contextual consistency in personality-based behaviors. We also found another aspect of individual differences in personality, specifically, the extent to which individual chimpanzees show consistency. Some individuals showed contextual and temporal consistency, whereas others show significant variation across behaviors, contexts, and/or time. We speculate that the relative degree of consistency in personality may vary within chimpanzees. It may be that different primate species vary in the extent to which individuals show consistency of personality traits. Our behavioral-based assessment can be used with wild populations, increasing the validity of personality studies, facilitating comparative studies and potentially being applicable to conservation efforts.