Philosophical Transactions of the Royal Society B: Biological Sciences

Piloerection (e.g., goosebumps) is an essential thermoregulatory and social signalling mechanism in non-human animals. While humans also experience piloerection--often being perceived as an indicator of profound emotional experiences--its comparatively less effective role in thermoregulation and communication might influence our capacity to monitor its occurrence. We present three studies (total N = 617) demonstrating participants general inability to detect their own piloerection events and their lack of awareness that piloerection occurs with a similar frequency on multiple anatomical locations. Participants over-reported piloerection events with only 31.8% coinciding with observable piloerection, a bias unrelated to piloerection intensity, anatomical location, heart rate variability, or interoceptive awareness. We also discovered a self-report bias for the forearm, contradicting the observation that piloerection occurs with equal frequency on multiple anatomical locations. Finally, there was low correspondence between self-reports of being "emotionally moved" and observed piloerection. These counterintuitive findings not only highlight a disconnect between an obvious physiological response and our capacity for self-monitoring, but they underscore a fascinating divergence between human and non-human species. While piloerection is vital in non-human organisms, the connection between piloerection and psychological experience in humans may be less significant than previously assumed, possibly due to its diminished evolutionary relevance. Statement of ImpactThis research reveals a striking dissociation between an obvious physiological response-- piloerection--and human capacity for self-perception. While this highlights the limitations of relying on self-report measures, it also underscores an important divergence between humans and non-human species. We propose that the relation between piloerection and psychological experience in humans is less pronounced than in other species, potentially due to its diminished role in human evolution.

Social interactions are important for how societies function, conferring robustness and resilience to environmental changes. The structure of social interactions can shape the dynamics of information and goods transmission. In addition, the availability and type of resources that are transferred might impact the structure of interaction networks. For example, storable resources might reduce the required speed of distribution and altering interaction structure can facilitate such change. Here we use ants as a model system to examine how social interactions are impacted by group size, food availability, and food type. We compare global- and individual-level network measures across experiments in which groups of different sizes received limited or unlimited food that is either favorable and cannot be stored (carbohydrates), or unfavorable but with a potential of being stored (protein). We found that as group size increased, individuals interacted with more social partners and interaction networks became more compartmentalized. Furthermore, group compartmentalization increased when food was limited and when transferring storable goods. Our findings highlight how biological systems can adjust their interaction networks in ways that relate to their function. The study of such biological flexibility can inspire novel and important solutions to the design of robust and resilient supply chains.

While culture is widespread in the animal kingdom, human culture has been claimed to be special due to being cumulative. It is currently debated which cognitive abilities support cumulative culture, but behavioural form copying is one of the main abilities proposed. One important source of contention is the presence or absence of behaviour copying in our closest living relatives, non-human great apes (apes) – especially given that their behaviour does not show clear signs of cumulation. Those who claim that apes copy behaviour often base this claim on the existence of stable ape cultures in the wild. We developed an individual-based model to test whether ape cultural patterns can emerge in absence of any behaviour copying, when only allowing for a well-supported alternative social learning mechanism, socially mediated reinnovation, where only the frequency of reinnovation is under social influence, but the form of the behaviour is not. Our model reflects wild ape life conditions, including physiological and behavioural needs, demographic and spatial features, and possible genetic and ecological variation between populations. Our results show that, under a wide range of values of parameters, we can reproduce the defining features of wild ape cultural patterns. Overall, our results show that ape cultures can emerge and stabilise without behaviour copying. Ape cultures do not show the signatures of behaviour copying abilities, lending support to the notion that behaviour copying is, among apes, unique in the human lineage. It therefore remains an open question when and why behaviour copying evolved in hominins.Competing Interest StatementThe authors have declared no competing interest.View Full Text

AO_SCPLOWBSTRACTC_SCPLOWDivision of labour is fundamental to the functioning of societies and socially living organisms. While it has been central to their study for decades, no complete picture has emerged yet. Some of the most fascinating questions arise in the context of self-organised societies, like those of social insects, that coordinate their behaviour with completely decentralised simple decision-making performed by individuals that only have local information at their disposal. Based on empirical evidence, these collectives appear to balance task engagement globally across their whole task network for the benefit of the colony overall. How can this pro-social coordination be achieved by independently acting individuals? How is a global workforce balancing possible based on only local perception with no knowledge of the global colony status or needs? Central to solving these problems is the question how can the relevant information flow through the task network so that a changed task demand in one part of the colony can lead to adjustments in distant other parts? We detail a model that presents a potential answer to this conundrum. Our model is informed by evolutionary game theory and rests on the assumption that the perception of an individuals sensory input can evolve. We present simulation studies and a mathematical proof to show that pro-social behaviour will evolve in a collective of agents that adjust their behaviour using primitive and biologically plausible learning mechanisms if we assume an evolving perception function.

Studying life history strategies in microorganisms can help predict their performance when complex microbial communities can be categorised into groups of organisms with similar strategies. Microorganisms are typically classified as copiotroph or oligotroph, but it has been proven difficult to generalise their life history strategies to broad lineages. Here we tested if the fast-slow continuum and reproductive strategy framework of macro-organismal life histories can be applied to microorganisms. We used demographic and energy budget data from 13 microorganisms (bacteria, fungi, a protist and a plant) to examine how generation time, survivorship, growth form, age at maturity, recruitment success, and net reproductive rate structure microbial life histories. We found that 79% of microorganism life-history variation fell along two uncorrelated axes. Like macro-organisms, we found a fast-slow pace of life continuum, including shorter-lived microorganisms at one end, and longer-lived microorganisms that mature later in life at the other. Also, like macro-organisms, we found a second, reproductive strategy axis, with microorganisms with greater lifetime reproductive success and decreased mortality at older age at one end, and microorganisms with the opposite characteristics at the other end. Microorganismal life history strategies did not covary proportionally to their shared evolutionary history. Thus, whereas this work suggests that the macro-organismal fast-slow continuum and reproductive strategy framework could be realistically applied to microorganisms, their life history processes cannot be inferred from patterns in taxonomic composition. Impact statementAnimals and plants show distinct differences in their pace of life: some have high reproduction and high mortality, others low. Here we show that microorganisms display similar such life history patterns, igniting future research on microbial life history strategies. Data summarySupplemental data, R code and MatLab code are deposited in Figshare at https://doi.org/10.6084/m9.figshare.16831543.v2 [27].

Reproduction is energetically expensive for mammals, and especially so during lactation. In large-brained mammals such a primates, females invest heavily in additional feeding to fuel the costs of lactation. The evidence is more mixed in ruminant ungulates. We examine the foraging costs of lactating female feral goats living under environmentally challenging conditions in the northwest of Scotland where these effects are most likely to be exaggerated. We show, using data from three separate studies, that, compared to matched non-lactating females, lactating females do increase the time devoted to foraging, but only to a limited extent that is well below the theoretical requirements of their kids. Although they do not alter their diet, lactating females spend more time in shelter and at lower altitudes in order to reduce thermoregulatory costs. At high latitudes, the rate at which kids grow is such that females cannot afford to extend lactation much beyond two months. This will inevitably set a limit on ungulates capacity to produce large-brained offspring. HighlightsO_LILactation is costly, obliging females to increase food intake or draw on body fat C_LIO_LIAt high latitudes, goats increase foraging, but not enough to meet kids demands C_LIO_LIFemales do not forage on richer foods, but they do try to minimise thermal costs C_LIO_LIAs a result, females have high mortality after weaning when forage quality is poor C_LI

In group-living species, evolution puts a premium on the ability of individuals to track the state, whereabouts, and interactions of others. The value of social information might vary with the degree of competition within and between groups, however. We investigated male monitoring of female location in wild Guinea baboons (Papio papio). Guinea baboons live in socially tolerant multi-level societies with one-male-units comprising 1-6 females and young at the core. Using field playback experiments, we first tested whether male Guinea baboons (N=14) responded more strongly to playbacks of associated vs. non-associated females, which was the case. In the second and core experiment, we tested whether males (N=22 males, N=62 trials) keep track of the whereabouts of associated females by playing back unit females calls from locations that were either consistent or inconsistent with the actual position of the female. Contrary to predictions, males responded equally strongly in both conditions. While males seem to recognize their females by voice, they might lack the attention or motivation to track their females movement patterns. These results reinforce the view that the value of social information may vary substantially with the distribution of power in a society. While highly competitive regimes necessitate high attention to deviations from expected patterns, egalitarian societies allow for a certain degree of obliviousness.

Conventions can be defined as arbitrary and self-sustaining practices that emerge in a population and facilitate solving coordination problems. A recent study traced the formation of simple conventions in captive baboons in a touch-screen-based color-matching game. We replicated this task with human pairs under different conditions (with/without visual access to the partners screen; with/without prior information on the task structure) to assess their effects on the formation and stability of conventions. We found that more information delayed the formation of conventions (arbitrary rankings of colors that determined choices in any given color-pairing). Analysis of self-reported strategies did not reveal a clear effect of condition on levels of elicited strategic behavior. Interestingly, pairs maintained their conventions even when given visual access to their partners screen, despite the availability of an alternative, potentially simpler, cognitive strategy. In a follow-up variant of the task that paired up experienced subjects with a naive partner, conventions emerged faster but did not replicate the convention previously formed by the experienced player, demonstrating the transmission of "know-how" but not "know-what" information. We discuss the implications of our results for understanding the cognitive mechanisms necessary to support the formation, maintenance, and transmission of conventions.

BackgroundThe intestine adapts to environmental stimuli by dynamically altering its size. Infections causes shrinkage and subsequent regrowth to original intestinal dimensions, suggesting homeostasis, whereas diet can induce adaptive changes. Whether diet and infection differ in the kinetics, magnitude, or cellular mechanisms that drive intestinal resizing, and whether intestines use a fixed size "memory" versus an adaption to nutrient availability, still remains unclear. ObjectiveTo determine whether intestinal regrowth after infection reflects a fixed "memory" of a target size (homeostasis) or an adaptation to the nutritional state during regrowth, and to identify the cellular modalities that drive infection- and diet-induced resizing. DesignUsing Drosophila melanogaster as a model, we quantified intestinal size, cell size, cell number, and epithelial turnover in response to dietary shifts and oral bacterial infections, both individually and in combination. ResultsInfection-induced atrophy occurred only when the intestine was initially large, and regrowth required nutrient availability. Distinct cellular mechanisms underpinned changes in intestinal size: diet-induced growth in unchallenged intestines was mediated by enterocyte hypertrophy, whereas post-infection regrowth required intestinal stem cell (ISC) proliferation. Consistently, ISC ablation impaired regrowth only after infection. Bacteria functioned both as pathogens and nutrients, triggering intestinal shrinkage when damaging a large organ, but promoting growth when consumed by nutrient-deprived flies. ConclusionIntestinal regrowth after infection reflects a context-dependent, diet-driven adaptation, not a fixed intestinal size memory. Diet and infection engage distinct, stimulus-specific cellular programs to reshape the midgut, revealing a modular logic of organ plasticity with implications for tissue repair and metabolic regulation. Summary boxO_ST_ABSWhat is already known on this topicC_ST_ABS- Intestinal size is regulated by epithelial turnover and responds dynamically to dietary and microbial stimuli. What this study adds- Post-infection intestinal regrowth is governed by dietary input rather than an intrinsic memory of pre-infection intestinal size. - Intestinal resizing is driven by distinct cellular programs: diet-induced intestinal growth occurs independently of stem cells, while post-infection intestinal regrowth requires stem cell proliferation. - Diet, rather than microbes, is the primary driver of intestinal size, while pathogens influence the mode of size change by increasing cellular turnover. - Pathogenic microbes act as both sources of damage and nutrients, influencing organ resizing. How this study might affect research, practice, or policy- Reframes intestinal regeneration as a flexible, context-dependent adaptation rather than a fixed homeostatic process. - Identifies nutritional status as a critical determinant of recovery following intestinal injury. - Offers a conceptual framework for understanding epithelial plasticity in health and disease, emphasizing how the balance of cell size and stem cell activity coordinates adult intestinal size.

In this simulation study, we adopt the comprehensive neurocomputational approach of Active Inference (AIF) to illustrate some key concepts of Material Engagement Theory (MET) [1]. MET posits that craftwork does not require, or rely on, rich internal pre-planning, i.e., complex and highly detailed representations that occur mainly in the makers head. Instead, the maker engages materiality through thinging, where the human agent (the maker) is guided by and leverages the materiality of the artefact (such as a spinning of clay or a chunk of marble). MET assigns a crucial co-participatory role to materiality, attributing agency to it. We investigate METs claims through the widely adopted theory of AIF [2]. Our first aim is to simulate the plausibility of the (creative) thinging, adopting a simple modelling scenario. Then, we also discuss its applicability to other, more complex cases, which seem to require greater levels of pre-thinking (e.g., planning, imagining and conceptualising outcomes). We highlight how these cases, too, align with the general principle of thinging. With our AIF neurocomputational understanding, we explain that even in these situations, the predictive brains involved in the creative process attempt to minimise the complexity of their internal model. The upshot of this is that, always and everywhere, our human minds engage the materiality to make the most of the characteristic dynamics of the world surrounding us - things and processes alike.

When humans engage in joint action, they seem to so with an underlying sense of joint commitment, a feeling of mutual obligation towards their partner and a shared goal. Whether our closest living relatives, bonobos and chimpanzees, experience and understand joint commitment in the same way is subject to debate. Crucial evidence concerns how participants respond to interruptions of joint actions, particularly if they protest or attempt to reengage their reluctant or distracted partners. During dyadic interactions, bonobos and chimpanzees appear to have some sense of joint commitment, according to recent studies. Yet, data are inconsistent for triadic games with objects. We addressed this issue by engaging N=23 apes (5 adult chimpanzees, 5 infant bonobos, 13 adult bonobos) in a "tug-of-war" game with a human experimenter who abruptly stopped playing. Adult apes readily attempted to reengage the experimenter (>60% of subjects on first trial), with no group differences in the way of reengagement. Infant bonobos rarely reengaged and never did so on their first trial. Importantly, when infants reengaged passive partners, they mostly deployed (tactile) signals, yet rarely game-related behaviours (GRBs) as commonly observed in adults. These findings might explain negative results of earlier research. Bonobos and chimpanzees may thus have motivational foundations for joint commitment, although this capacity might develop over lifetime. We discuss this finding in relation to evolutionary and developmental theories on joint commitment.

Division of labour is a key feature of cooperative social systems, where task specialization among individuals enhances group efficiency. In the cooperatively breeding cichlid Neolamprologus pulcher reproductive division of labour exists, where a dominant breeding pair reproduces while subordinates help in rearing the offspring and perform various tasks to gain acceptance within the group. Larger helpers engage in territory maintenance and predator defence while smaller helpers focus on egg care and deterrence of egg predators. Here we investigated task specialisation, division of labour and the dynamics of coordination of tasks in N. pulcher groups of natural size and composition. In lab experiments, we assessed whether helpers consistently specialized in sand removal from territories or in egg predator defence when both tasks were presented simultaneously. While different size classes performed both tasks, task performance was not repeatable, and there was no clear division of labour. Dominant females did most work, with the helpers often remaining idle. Lag sequence analysis revealed that individuals were significantly more likely to take up a task if it had just been performed by another individual, rather than dividing labour between individuals - a phenomenon we term "task contagion". This suggests that individuals respond to immediate group needs, offering new insights into how cooperative breeders can adapt to changing task demands by flexible behaviour and potentially enhance group efficiency. Significance statementCooperatively breeding vertebrates exhibit complex social structures and group dynamics, one notable feature being division of labour. However, unlike eusocial insects, these vertebrates display a high degree of flexibility in task allocation among group members. In a laboratory experiment, we investigated the dynamics of task allocation and coordination in groups of the cooperatively breeding cichlid Neolamprologus pulcher. We simultaneous induced demands for both territory maintenance and territory defence against egg predators. Task performance and the degree of specialisation varied across size classes and between different groups, and were not repeatable. Using high-resolution event data, we identified a tendency for individuals to follow others in the execution of the same task, a phenomenon we have termed task contagion.

Successful biological invasions are dependent on the invader being able to grow and reproduce in the new environment. One way that microbial invaders may facilitate this is to use cooperative public goods, such as metal-binding siderophores. However, siderophore production can be exploited by non-producing cheats who benefit from production without paying any associated costs. Here, we test the importance of cooperation for the success of Pseudomonas aeruginosa invading a 5-species microbial community. We do this by comparing the success of a siderophore-producing strain, a siderophore-deficient mutant strain and a 50:50 mixed population, both in environments with weak (copper absent) and strong (copper present) siderophore requirement. We found no effect of invader type on success when siderophores were less essential for growth, but large differences when they were selectively favoured. Here the producer-cheat mix had the greatest success, with both strains having near equal fitness and reaching high densities, whilst in isolation producers had intermediate success and cheats the lowest. Similarly, resident diversity only differed across invader treatments when copper was present. In conclusion, we show that the presence of cheats can provide a larger benefit for invasion success than pure cooperator populations, but only when public goods are particularly beneficial.

Studies on collective cognition have provided many examples of decision-making benefits in terms of animals sharing information about predators, prey or resources in their environment. It has been shown how the efficient spread of adaptive information within groups can provide benefits which increase with group size. Little is known, however, to which extent groups also amplify maladaptive information such as false alarms and whether such costs reduce or even nullify the above benefits. Here, we investigated fish shoals in the wild that responded collec-tively with escape dives when attacked by birds. We analysed the response of shoals in reac-tion to hard-to-detect bird attacks and similar but harmless flybys as a function of shoal size. With increasing shoal size fish increasingly detected predator attacks (true positives) while their false alarms remained constant. Therefore, larger shoals became better at correctly clas-sifying potentially dangerous stimuli rather than becoming more sensitive to all stimuli poten-tially related to attacks. In addition, decision time decreased with increasing shoal size. Larger shoals were thus able to mitigate two major trade-offs inherent in solitary decision making: the trade-off between true and false positives and the trade-off between speed and accuracy. We report performance increases at shoal sizes of tens of thousands of fish and pose chal-lenges for the modelling of the underlying mechanisms.

Myxomycetes are multinucleate unicellular organisms. They form a plasmodium that moves by protoplasmic flow and prey on microorganisms. When encountering intraspecifics, the plasmodium has the capacity for fusion, actively approaching and fusing its cells, or avoidance, altering its direction to avoid the other individual. This is an allorecognition ability. However, it remains unclear whether the range of allorecognition extends to other species, and its ecological significance is also obscure. Here, we conduct a quantitative evaluation of contact responses from closely related species of plasmodium to clarify the recognition range of the allorecognition system in Myxomycetes. Behavioral assays demonstrate that the allorecognition system recognizes individuals within the same species while failing to recognize those of different species. The allorecognition is an extremely narrow and inward-focused mechanism, arguing for a highly specialized system of self-other recognition. Summary statementMyxomycetes plasmodium can recognize each other only if the other individuals they encounter are of the same species.

In animal groups, spatial heterogeneities shape social contact networks, thereby influencing the transmission of infectious diseases. Active modifications to the spatial environment could thus be a potent tool to mitigate epidemic risk. We tested whether Lasius niger ants modify their nest architecture in response to pathogens by introducing controlor pathogen-treated individuals into nest-digging groups, and monitoring three-dimensional nest morphogenesis over time. Pathogen exposure led to an array of architectural changes including faster nest growth, increased spacing between entrances, transmission-inhibitory changes in overall nest network topology, and reduced chamber centrality. Simulations confirmed that these changes reduced disease spread. These results provide evidence for architectural immunity in a social animal and offer insights into how spatial organisation can be leveraged to decrease epidemic susceptibility.

We present a detailed study of male associations in a roving species, the Asian elephant, using six years of data on identified, nonmusth males. Adult males spent greater proportions of their time solitarily than in mixed-sex or in all-male groups. Old (over 30 years) males were sighted more frequently with their age-peers and less frequently with young (15-30 years) males than expected at random in all-male groups. Young males were not sighted more frequently with old males than with young males, and did not disproportionately initiate associations with old males. These results suggest that male associations, in the absence of females, primarily allow for old nonmusth males to test strengths against age-peers. Social learning from older individuals did not seem to be important in male associations, unlike that observed in African savannah elephants. We also found a constraint on the sizes of all-male groups, similar to that seen in female groups in our study population, and with male group sizes being smaller than that of African savannah elephants. However, most males had a significant top associate in female absence. In mixed-sex groups, male associations occurred at random, suggesting that males were tracking female groups independently. Thus, we find some differences in male social organisation compared to the phylogenetically related African savannah elephant that occupies a similar niche, and suggest that ecological factors might have shaped the differences in these male societies.Competing Interest StatementThe authors have declared no competing interest.View Full Text

Communication networks are widespread across species, permitting information flow and facilitating social connections across space and time. In birds, communication networks are well studied in territorial species with long-range songs connecting individuals across space, where unintended listeners extract information from others signalling interactions. Yet acoustic signals also play important social roles at short range, forming communication networks that connect individuals within larger social units. Wild zebra finches (Taeniopygia castanotis) provide a unique model system to examine such communication networks in a non-territorial species with multiple males singing at shared locations in close temporal proximity. Zebra finches breed in loose colonies in the Australian arid zone, typically stay near their partner, move around in pairs or small groups, and gather at social hotspots, thus forming dynamic, potentially multi-level, societies. Here, we used the individually distinctive male song, recorded over 1,835 song bouts at two breeding sub-colonies and three social hotspots to quantify singing activity. We identified 163 males based on spectrographic similarities, verified by a deep learning model (BirdNET), and constructed communication networks based on temporal singing proximity at shared locations, social hotspots and the breeding colony. We reveal higher singing activity at social hotspots, with no dawn song and singing peaking at different times of day between breeding sites and social hotspots. Communication networks, with distinct males singing in close temporal proximity, were apparent in both contexts, with larger networks at hotspots. These networks were not strongly nested, yet many individuals met repeatedly at either the hotspot or breeding sites and some even maintained associations across breeding colonies and hotspots, providing building blocks for a multi-level society. These networks may facilitate synchronized foraging and breeding as adaptations to a harsh and unpredictable environment. Additionally, our approach offers a novel road map for widening the understanding of communication networks.

Coordinated behavior, such as hunting in lions and coordinated vigilance as antipredator behavior, are examples of benefits of group-living. Instead of asynchronous vigilance, some social species synchronize their vigilance bouts or take turns acting as sentinels. To increase our knowledge on the evolution of vigilance behavior, we studied whether vigilance is coordinated in Barbary ground squirrels, Atlantoxerus getulus. We show that vigilance was synchronized instead of taking turns. Multiple non-mutually exclusive hypotheses could explain synchronization: Barbary ground squirrels may perch because 1) neighbors are perched (copying effect), 2) perch synchrony may be an emergent property of the ecology as all squirrels may be satiated at the same time (collective behavior), or 3) the benefits are large in terms of evading ambush predators and scanning effectiveness (watch each others back). Particularly, in habitats where the field of view is obstructed by man-made structures and multiple individuals may be necessary to watch for terrestrial predators, synchronized vigilance may have greater fitness benefits than sentinel behavior. We conclude that it is essential to test assumptions of coordination and, thus, to analyze coordination to describe sentinel systems. Significance StatementVigilance behavior can be vital to an animals survival. Taking turns acting as sentinels or synchronizing vigilance bouts reduces the cost of the trade-off between feeding and predation risk. A sentinel system assumes that sentinels are vigilant from raised positions, warn group members of danger, and alternate vigilance bouts. However, the assumption of alternating vigilance bouts remains poorly tested. We tested this assumption in invasive Barbary ground squirrels. We found that instead of alternating, individuals synchronized their vigilance bouts. Perch synchrony may be 1) a response to perching group members (copying effect), 2) an emergent property of the species ecology, and 3) an adaptation to anthropogenically altered habitats (watch each others back).

Individual recognition is conceptually complex and computationally intense, leading to the general assumption that this social knowledge is solely present in vertebrates with larger brains, while miniature-brained animals in differentiating societies eschew the evolutionary pressure for individual recognition by evolving computationally less demanding class-level recognition, such as kin, social rank, or mate recognition. Arguably, this social knowledge is restricted to species with a degree of sociality (sensu [1], for a review [2]). Here we show the exception to this rule in a non-social arthropod species, the jumping spider Phidippus regius. Using a habituation - dishabituation paradigm, we visually confronted pairs of spatially separated spiders with each other and measured the interest of one spider towards the other. The spiders exhibited high interest upon initial encounter of an individual, reflected in mutual approach behaviour, but adapted towards that individual when it reoccurred in the subsequent trial, indicated by their preference of staying farther apart. In contrast, spiders exhibited a rebound from habituation, reflected in mutual approach behaviour, when a different individual occurred in the subsequent trial, indicating the ability to tell apart spiders identities. These results suggest that P. regius is capable of individual recognition based on long-term memory.