Self-organised criticality in the evolution of a thermodynamic model of rodent thermoregulatory huddling

A thermodynamic model of thermoregulatory huddling interactions between endotherms is developed. The model is presented as a Monte Carlo algorithm in which animals are iteratively exchanged between groups, with a probability of exchanging groups defined in terms of the temperature of the environment and the body temperatures of the animals. The temperature-dependent exchange of animals between groups is shown to reproduce a second-order critical phase transition, i.e., a smooth switch to huddling when the environment gets colder, as measured in recent experiments. A peak in the rate at which group sizes change, referred to as pup flow, is predicted at the critical temperature of the phase transition, consistent with a thermodynamic description of huddling, and with a description of the huddle as a self-organising system. The model was subjected to a simple evolutionary procedure, by iteratively substituting the physiologies of individuals that fail to balance the costs of thermoregulation (by huddling in groups) with the costs of thermogenesis (by contributing heat). The resulting tension between cooperative and competitive interactions was found to generate a phenomenon called self-organised criticality, as evidenced by the emergence of avalanches in fitness that propagate across many generations. The emergence of avalanches reveals how huddling can introduce correlations in fitness between individuals and thereby constrain evolutionary dynamics. Finally, a full agent-based model of huddling interactions is also shown to generate criticality when subjected to the same evolutionary pressures. The agent-based model is related to the Monte Carlo model in the way that a Vicsek model is related to an Ising model in statistical physics. Huddling therefore presents an opportunity to use thermodynamic theory to study an emergent adaptive animal behaviour. In more general terms, huddling is proposed as an ideal system for investigating the interaction between self-organisation and natural selection empirically

Self-organised criticality in the evolution of a thermodynamic model of rodent thermoregulatory huddling

A thermodynamic model of thermoregulatory huddling interactions between endotherms is developed. The model is presented as a Monte Carlo algorithm in which animals are iteratively exchanged between groups, with a probability of exchanging groups defined in terms of the temperature of the environment and the body temperatures of the animals. The temperature-dependent exchange of animals between groups is shown to reproduce a second-order critical phase transition, i.e., a smooth switch to huddling when the environment gets colder, as measured in recent experiments. A peak in the rate at which group sizes change, referred to as pup flow, is predicted at the critical temperature of the phase transition, consistent with a thermodynamic description of huddling, and with a description of the huddle as a self-organising system. The model was subjected to a simple evolutionary procedure, by iteratively substituting the physiologies of individuals that fail to balance the costs of thermoregulation (by huddling in groups) with the costs of thermogenesis (by contributing heat). The resulting tension between cooperative and competitive interactions was found to generate a phenomenon called self-organised criticality, as evidenced by the emergence of avalanches in fitness that propagate across many generations. The emergence of avalanches reveals how huddling can introduce correlations in fitness between individuals and thereby constrain evolutionary dynamics. Finally, a full agent-based model of huddling interactions is also shown to generate criticality when subjected to the same evolutionary pressures. The agent-based model is related to the Monte Carlo model in the way that a Vicsek model is related to an Ising model in statistical physics. Huddling therefore presents an opportunity to use thermodynamic theory to study an emergent adaptive animal behaviour. In more general terms, huddling is proposed as an ideal system for investigating the interaction between self-organisation and natural selection empirically

Coordinated Movements Prevent Jamming in an Emperor Penguin Huddle

For Emperor penguins (Aptenodytes forsteri), huddling is the key to survival during the Antarctic winter. Penguins in a huddle are packed so tightly that individual movements become impossible, reminiscent of a jamming transition in compacted colloids. It is crucial, however, that the huddle structure is continuously reorganized to give each penguin a chance to spend sufficient time inside the huddle, compared with time spent on the periphery. Here we show that Emperor penguins move collectively in a highly coordinated manner to ensure mobility while at the same time keeping the huddle packed. Every 30–60 seconds, all penguins make small steps that travel as a wave through the entire huddle. Over time, these small movements lead to large-scale reorganization of the huddle. Our data show that the dynamics of penguin huddling is governed by intermittency and approach to kinetic arrest in striking analogy with inert non-equilibrium systems, including soft glasses and colloids

Modelling the emergence of rodent filial huddling from physiological huddling

Huddling behaviour in neonatal rodents reduces the metabolic costs of physiological thermoregulation. However, animals continue to huddle into adulthood, at ambient temperatures where they are able to sustain a basal metabolism in isolation from the huddle. This 'filial huddling' in older animals is known to be guided by olfactory rather than thermal cues. The present study aimed to test whether thermally rewarding contacts between young mice, experienced when thermogenesis in brown adipose fat tissue (BAT) is highest, could give rise to olfactory preferences that persist as filial huddling interactions in adults. To this end, a simple model was constructed to fit existing data on the development of mouse thermal physiology and behaviour. The form of the model that emerged yields a remarkable explanation for filial huddling; associative learning maintains huddling into adulthood via processes that reduce thermodynamic entropy from BAT-metabolism and increase information about social ordering amongst littermates

A Self-Organising Model of Thermoregulatory Huddling

Endotherms such as rats and mice huddle together to keep warm. The huddle is considered to be an example of a self-organising system, because complex properties of the collective group behaviour are thought to emerge spontaneously through simple interactions between individuals. Groups of rodent pups display two such emergent properties. First, huddling undergoes a ‘phase transition’, such that pups start to aggregate rapidly as the temperature of the environment falls below a critical temperature. Second, the huddle maintains a constant ‘pup flow’, where cooler pups at the periphery continually displace warmer pups at the centre. We set out to test whether these complex group behaviours can emerge spontaneously from local interactions between individuals. We designed a model using a minimal set of assumptions about how individual pups interact, by simply turning towards heat sources, and show in computer simulations that the model reproduces the first emergent property—the phase transition. However, this minimal model tends to produce an unnatural behaviour where several smaller aggregates emerge rather than one large huddle. We found that an extension of the minimal model to include heat exchange between pups allows the group to maintain one large huddle but eradicates the phase transition, whereas inclusion of an additional homeostatic term recovers the phase transition for large huddles. As an unanticipated consequence, the extended model also naturally gave rise to the second observed emergent property—a continuous pup flow. The model therefore serves as a minimal description of huddling as a self-organising system, and as an existence proof that group-level huddling dynamics emerge spontaneously through simple interactions between individuals. We derive a specific testable prediction: Increasing the capacity of the individual to generate or conserve heat will increase the range of ambient temperatures over which adaptive thermoregulatory huddling will emerge

How self-organization can guide evolution

Self-organization and natural selection are fundamental forces that shape the natural world. Substantial progress in understanding how these forces interact has been made through the study of abstract models. Further progress may be made by identifying a model system in which the interaction between self-organization and selection can be investigated empirically. To this end, we investigate how the self-organizing thermoregulatory huddling behaviours displayed by many species of mammals might influence natural selection of the genetic components of metabolism. By applying a simple evolutionary algorithm to a wellestablished model of the interactions between environmental, morphological, physiological and behavioural components of thermoregulation, we arrive at a clear, but counterintuitive, prediction: rodents that are able to huddle together in cold environments should evolve a lower thermal conductance at a faster rate than animals reared in isolation. The model therefore explains how evolution can be accelerated as a consequence of relaxed selection, and it predicts how the effect may be exaggerated by an increase in the litter size, i.e. by an increase in the capacity to use huddling behaviours for thermoregulation. Confirmation of these predictions in future experiments with rodents would constitute strong evidence of a mechanism by which self-organization can guide natural selection

Strategies for Hypothermia Compensation in Altricial and Precocial Newborn Mammals and Their Monitoring by Infrared Thermography

Publication history: Accepted - 18 May 2022; Published - 23 May 2022.Thermoregulation in newborn mammals is an essential species-specific mechanism of the nervous system that contributes to their survival during the first hours and days of their life. When exposed to cold weather, which is a risk factor associated with mortality in neonates, pathways such as the hypothalamic–pituitary–adrenal axis (HPA) are activated to achieve temperature control, increasing the circulating levels of catecholamine and cortisol. Consequently, alterations in blood circulation and mechanisms to produce or to retain heat (e.g., vasoconstriction, piloerection, shivering, brown adipocyte tissue activation, and huddling) begin to prevent hypothermia. This study aimed to discuss the mechanisms of thermoregulation in newborn domestic mammals, highlighting the differences between altricial and precocial species. The processes that employ brown adipocyte tissue, shivering, thermoregulatory behaviors, and dermal vasomotor control will be analyzed to understand the physiology and the importance of implementing techniques to promote thermoregulation and survival in the critical post-birth period of mammals. Also, infrared thermography as a helpful method to perform thermal measurements without animal interactions does not affect these parameters.Non

A Neural Mechanism for Capnotaxis in the Naked Mole-Rat

A Neural Mechanism for Capnotaxis in the Naked Mole-Rat The Naked Mole-Rat (NM-R) is a small hairless rodent that has thrived underground in the Horn of Africa for the past 40 million years. It was first discovered in 1847, but has only been maintained in captivity and studied as a laboratory animal over the past 40 years. To date, more than 400 scientific papers have been published on this species. This is relatively few compared to established lab animals like rats and mice, but those papers contain a trove of information that has changed our understanding of the constraints of mammalian physiology. Naked mole-rats maintain a cooperative breeding system of eusociality by suppressing the reproductive system and can tolerate prolonged periods of low oxygen. Using a combination of behavioral analysis, in vitro and in vivo electrophysiology, and molecular biology, this thesis demonstrates a capnotaxic drive toward aggregation in adult NM-R. By extending the developmental tolerance for hypercapnia which is present at birth, NM-R have come to depend upon the enhanced neuronal inhibition that CO2 provides, at the expense of adequate inhibitory tone in “normal” atmosphere. RFID tracking of whole colonies shows a majority of activity concentrated around a single nest chamber. Individuals of the colony remain in the nest with forays to the food chamber and toilet chambers. Infusing CO2 into an empty chamber showed an increase in forays through the chamber compared to no infusion and to air infusion (5.9±0.92 trips per hour, compared to 1.2±0.29 trips and 1.4±0.31 trips per hour respectively). While NM-Rs are well-equipped for a gain of CO2, I demonstrate here that they are inadequately equipped for what could be considered hypocapnia, relative to their normal environment. When adult NM-Rs were exposed to room air at 42 °C, respiration rate more than doubled (room temperature: 77±7 breaths per minute; heated: 168±18 breaths per minute, t(4)=4.7, p= 0.01). In 8 of 9 animals exposed to this simulated surface environment, signs of seizure activity (head bobbing, mouth automatisms, generalized convulsions) appeared 14.4±1.2 minutes after the chamber temperature reached 42 °C. These seizures are likely due to the loss of CO2 during hyperventilation, and subsequent brain hyperactivity due to respiratory alkalosis. As support for this, seizures were prevented with simulated nest air at 42 °C (2.5% CO2 / 21% O2 / 76.5% N2). If administered after seizure began, high amplitude cortical seizure events subsided in the EEG but seizure-related motor activity continued. This vulnerability to heated normal air, which is nearly identical to typical conditions a naked mole-rat would experience on the ground just above its burrow, are hallmarks of an “overspecialization” in this species. NM-Rs are often touted as “superheroes”, but every comic book superhero has a vulnerability. I contend that NM-R depend on the hypercapnic environment they have created in their burrows for typical brain function, and are vulnerable outside it. The extended sensitivity to hyperthermia-induced seizures into adulthood does make the NM-R a superheroic animal model of febrile seizure, however, overcoming the limitations of other animal models, which are restricted to the early postnatal period. I have established a collaboration with experts in the mechanisms of febrile seizures from the University of Helsinki to inquire whether the same mechanisms of hyperexcitability they have identified in neonatal rats and mice are implicated in the seizure susceptibility of NM-R neonates and adults, and in fact they are. We also observe neonatal levels of KCC2 (chloride potassium) neuronal symporter and an impairment of GABAergic tone. Remarkably, injection of diazepam, a positive allosteric modulator of GABA, causes seizure in normal air in nearly all adult NM-R. This phenomenon is suppressed in nest air. This work will add a neuronal requirement for hypercapnia to the growing list of remarkable NM-R traits. This understanding of how certain physiological states in NM-R render them more vulnerable to environmental conditions may yield important new insight to other species who have the same challenges at times, including our own

Sociality in the African woodland dormouse

A thesis submitted to the Faculty of Science, University of the Witwatersrand, Johannesburg in fulfilment of the requirements for the degree of Doctor of Philosophy 2017Social systems describe the social organisation, mating system and social interactions of a species, and are revealing of the nature of how animals live and the underlying mechanisms of living alone or in groups. The social system of the African woodland dormice Graphiurus murinus has not been documented. The aim of my study was to investigate sociality, the mechanisms promoting sociality, and to G. murinus along the continuum of sociality in respect of rodents. Investigations on nest sharing in free-living woodland dormice showed that sleeping associations were common in females than males but changed seasonally (females all year round; males in breeding and winter seasons), reflecting the reproductive and thermoregulatory needs. The social structure of these sleeping associations was assessed using association indices and social network analysis. Woodland dormice exhibited a web of relationships between sex and age groups, with adult female groups and juvenile groups forming strong and exclusive relationships, while male groups showed ephemeral and weak relationships. In staged dyadic encounters of same sex dyads in captivity, females were amicable and tolerated unfamiliar females, whereas males displayed low tolerance and aggression towards unfamiliar. The three-chamber paradigm tests for sociability and social preferences revealed that both adult males and females had an intrinsic motivation to be social. However, this motivation differed by sex, with females showing a greater affinity for both strangers and unfamiliar females, whereas males showed an affinity for familiar males. Observations of huddling in female dyads revealed that, under decreasing Ta, females huddled together and combined nest material, thus changing the local microclimate and the insulation capacities of nests. In addition, long-associations were maintained even after Ta was increased, revealing that thermal challenges might promote group formation and enhance familiarity amongst females. Both my field and laboratory data suggest that woodland dormice form small seasonally transient sleeping associations. In females, limited aggression, tolerance, and nest sharing and construction under low temperatures could also lead to prolonged group-living. In males, aggression towards unfamiliar males, possibly maintains intra-sexual territoriality, yet familiarity creates tolerance, leading to group-living. Group-living in this arboreal rodent is mediated by the apparently phylogenetically constrained energetic demands of thermoregulation, coupled with an inherent need to associate with conspecifics. The level of familiarity between conspecifics or the presence of social partners facilitates group formation and is shaped by prevailing ecological conditions.MT 201