Collective signalling drives rapid jumping between cell states.

Development can proceed in 'fits and starts', with rapid transitions between cell states involving concerted transcriptome-wide changes in gene expression. However, it is not clear how these transitions are regulated in complex cell populations, in which cells receive multiple inputs. We address this issue using Dictyostelium cells undergoing development in their physiological niche. A continuous single cell transcriptomics time series identifies a sharp 'jump' in global gene expression marking functionally different cell states. By simultaneously imaging the physiological dynamics of transcription and signalling, we show the jump coincides with the onset of collective oscillations of cAMP. Optogenetic control of cAMP pulses shows that different jump genes respond to distinct dynamic features of signalling. Late jump gene expression changes are almost completely dependent on cAMP, whereas transcript changes at the onset of the jump require additional input. The coupling of collective signalling with gene expression is a potentially powerful strategy to drive robust cell state transitions in heterogeneous signalling environments. Based on the context of the jump, we also conclude that sharp gene expression transitions may not be sufficient for commitment.

Ant social network structure is highly conserved across species.

The ecological success of social insects makes their colony organization fascinating to scientists studying collective systems. In recent years, the combination of automated behavioural tracking and social network analysis has deepened our understanding of many aspects of colony organization. However, because studies have typically worked with single species, we know little about interspecific variation in network structure. Here, we conduct a comparative network analysis across five ant species from five subfamilies, separated by more than 100 Myr of evolution. We find that social network structure is highly conserved across subfamilies. All species studied form modular networks, with two social communities, a similar distribution of individuals between the two communities, and equivalent mapping of task performance onto the communities. Against this backdrop of organizational similarity, queens of the different species occupied qualitatively distinct network positions. The deep conservation of the two community structure implies that the most fundamental behavioural division of labour in social insects is between workers that stay in the nest to rear brood, and those that leave the nest to forage. This division has parallels across the animal kingdom in systems of biparental care and probably represents the most readily evolvable form of behavioural division of labour.

Leaderless consensus decision-making determines cooperative transport direction in weaver ants.

Animal groups need to achieve and maintain consensus to minimize conflict among individuals and prevent group fragmentation. An excellent example of a consensus challenge is cooperative transport, where multiple individuals cooperate to move a large item together. This behaviour, regularly displayed by ants and humans only, requires individuals to agree on which direction to move in. Unlike humans, ants cannot use verbal communication but most likely rely on private information and/or mechanical forces sensed through the carried item to coordinate their behaviour. Here, we investigated how groups of weaver ants achieve consensus during cooperative transport using a tethered-object protocol, where ants had to transport a prey item that was tethered in place with a thin string. This protocol allows the decoupling of the movement of informed ants from that of uninformed individuals. We showed that weaver ants pool together the opinions of all group members to increase their navigational accuracy. We confirmed this result using a symmetry-breaking task, in which we challenged ants with navigating an open-ended corridor. Weaver ants are the first reported ant species to use a 'wisdom-of-the-crowd' strategy for cooperative transport, demonstrating that consensus mechanisms may differ according to the ecology of each species.

Coupled information networks drive honeybee (Apis mellifera) collective foraging.

Collective behaviour by eusocial insect colonies is typically achieved through multiple communication networks that produce complex behaviour at the group level but often appear to provide redundant or even competing information. A classic example occurs in honeybee (Apis mellifera) colonies, where both the dance communication system and robust scent-based mechanisms contribute to the allocation of a colony's workforce by regulating the flow of experienced foragers among known food sources. Here we analysed social connectivity patterns during the reactivation of experienced foragers to familiar feeding sites to show that these social information pathways are not simply multiple means to achieve the same end but intersect to play complementary roles in guiding forager behaviour. Using artificial feeding stations, we mimicked a natural scenario in which two forager groups were simultaneously collecting from distinct patches containing different flowering species. We then observed the reactivation of these groups at their familiar feeding sites after interrupting their foraging. Social network analysis revealed that temporarily unemployed individuals interacted more often and for longer with foragers that advertised a familiar versus unfamiliar foraging site. Due to such resource-based assortative mixing, network-based diffusion analysis estimated that reactivation events primarily resulted from interactions among bees that had been trained to the same feeding station and less so from different-feeder interactions. Both scent- and dance-based interactions strongly contributed to reactivation decisions. However, each bout of dance-following had an especially strong effect on a follower's likelihood of reactivation, particularly when dances indicated locations familiar to followers. Our findings illustrate how honeybee foragers can alter their social connectivity in ways that are likely to enhance collective outcomes by enabling foragers to rapidly access up-to-date information about familiar foraging sites. In addition, our results highlight how reliance on multiple communication mechanisms enables social insect workers to utilise flexible information-use strategies that are robust to variation in the availability of social information.

Group phenotypic composition drives task performances in ants.

Differences in individual behaviour within a group can give rise to functional dissimilarities between groups, particularly in social animals. However, how individual behavioural phenotypes translate into the group phenotype remains unclear. Here, we investigate whether individual behavioural type affects group performance in a eusocial species, the ant Aphaenogaster senilis. We measured individual behavioural traits and created groups of workers with similar behavioural type, either high-exploratory or low-exploratory workers. We tested these groups in four different, ecologically relevant, tasks: reaction to an intruder, prey retrieval from a maze, nest relocation and tool use. We show that, compared to groups of low-exploratory workers, groups of high-exploratory workers were more aggressive towards intruders, more efficient in collecting prey, faster in nest relocation and more likely to perform tool use. Our results demonstrate a strong link between individual and collective behaviour in ants. This supports the 'behavioural type hypothesis' for group dynamics, which suggests that an individual's behaviour in a social environment reflects its own behavioural type. The average behavioural phenotype of a group can therefore be predicted from the behavioural types of individual group members.

Assessing Variations in Positional Performance across Age Groups and during Matches in Youth Association Football Competitions.

This study aimed to explore how positional performance varies across different youth age groups and during matches in football competitions. The study encompassed 160 male outfield youth football players (n = 80, under-13, U13; n = 80, under-15, U15) who belonged to the starting line-up and played the entire first half of each match. The players' positional data were gathered through the global positional system for each of the eight matches performed by each age group. The frequency of near-in-phase synchronization based on speed displacements, spatial exploration index, and the distance to the nearest teammate and opponent were used as variables. Additionally, each match half was segmented into three equal parts to assess changes over time and used as a period factor along with age group. The results indicated that U13 players showed a significant decrease (from small to large ES) in synchronization speed and spatial exploration index throughout the first half of the match, along with a decrease in the distance to the nearest opponent. In contrast, U15 players exhibited most changes during the third segment of the half, with a decrease in speed synchronization and spatial exploration, but an increase in the distance and regularity to the nearest opponent. Comparing both age groups revealed significant differences in speed synchronization across the entire half of the match and within each segmented period (from small to large ES), with U13 consistently showing higher values. The study highlights that long durations in 11 vs. 11 matches might not provide an appropriate learning environment in the U13 age group. Conversely, the U15 group displayed better capacity for tactical adjustments over time, suggesting a higher level of tactical maturity. Overall, these findings emphasize the importance of adapting youth football training and competition structures to the developmental needs and capabilities of different age groups to optimize learning and performance outcomes.

Behavioural differences underlie toxicity and predation variation in blooms of Prymnesium parvum.

Much of the evolutionary ecology of toxic algal blooms (TABs) remains unclear, including the role of algal toxins in the adaptive 'strategies' of TAB-forming species. Most eukaryotic TABs are caused by mixotrophs that augment autotrophy with organic nutrient sources, including competing algae (intraguild predation). We leverage the standing diversity of TABs formed by the toxic, invasive mixotroph Prymnesium parvum to identify cell-level behaviours involved in toxin-assisted predation using direct observations as well as comparisons between genetically distinct low- and high-toxicity isolates. Our results suggest that P. parvum toxins are primarily delivered at close range and promote subsequent prey capture/consumption. Surprisingly, we find opposite chemotactic preferences for organic (prey-derived) and inorganic nutrients between differentially toxic isolates, respectively, suggesting behavioural integration of toxicity and phagotrophy. Variation in toxicity may, therefore, reflect broader phenotypic integration of key traits that ultimately contribute to the remarkable flexibility, diversity, and success of invasive populations.

Manipulating nest architecture reveals three-dimensional building strategies and colony resilience in honeybees.

Form follows function throughout the development of an organism. This principle should apply beyond the organism to the nests they build, but empirical studies are lacking. Honeybees provide a uniquely suited system to study nest form and function throughout development because we can image the three-dimensional structure repeatedly and non-destructively. Here, we tracked nest-wide comb growth in six colonies over 45 days (control colonies) and found that colonies have a stereotypical process of development that maintains a spheroid nest shape. To experimentally test if nest structure is important for colony function, we shuffled the nests of an additional six colonies, weekly rearranging the comb positions and orientations (shuffled colonies). Surprisingly, we found no differences between control and shuffled colonies in multiple colony performance metrics-worker population, comb area, hive weight and nest temperature. However, using predictive modelling to examine how workers allocate comb to expand their nests, we show that shuffled colonies compensate for these disruptions by accounting for the three-dimensional structure to reconnect their nest. This suggests that nest architecture is more flexible than previously thought, and that superorganisms have mechanisms to compensate for drastic architectural perturbations and maintain colony function.

Collective synchrony of mating signals modulated by ecological cues and social signals in bioluminescent sea fireflies.

Individuals often employ simple rules that can emergently synchronize behaviour. Some collective behaviours are intuitively beneficial, but others like mate signalling in leks occur across taxa despite theoretical individual costs. Whether disparate instances of synchronous signalling are similarly organized is unknown, largely due to challenges observing many individuals simultaneously. Recording field collectives and ex situ playback experiments, we describe principles of synchronous bioluminescent signals produced by marine ostracods (Crustacea; Luxorina) that seem behaviorally convergent with terrestrial fireflies, and with whom they last shared a common ancestor over 500 Mya. Like synchronous fireflies, groups of signalling males use visual cues (intensity and duration of light) to decide when to signal. Individual ostracods also modulate their signal based on the distance to nearest neighbours. During peak darkness, luminescent 'waves' of synchronous displays emerge and ripple across the sea floor approximately every 60 s, but such periodicity decays within and between nights after the full moon. Our data reveal these bioluminescent aggregations are sensitive to both ecological and social light sources. Because the function of collective signals is difficult to dissect, evolutionary convergence, like in the synchronous visual displays of diverse arthropods, provides natural replicates to understand the generalities that produce emergent group behaviour.

Swarm formation as backward diffusion.

Considerable progress has been made in understanding insect swarms-forms of collective animal behaviour that unlike bird flocks, fish schools and animal herds do not possess global order. Nonetheless, little is known about swarm formation. Here we posit a mechanism for the formation of insect swarms that is consistent with recent empirical observations reported by (Patel and Ouellette 2022). It correctly predicts new features of swarm formation that have not been reported on previously. Our simple analytically tractable model shows how harmonic potential wells, a characteristic feature of swarming, and so swarm cohesion, arise from diffusion and local fission-fusion dynamics and how, in accord with observations, these wells deepen over time. The overall form of these potential wells is predicted to depend on the number and spatial distribution of all individuals, making them manifestly a collective phenomenon. Finally, swarms are predicted to 'cool' (that is, condense) as they form.

Evolutionary stability of social interaction rules in collective decision-making.

Social animals can use the choices made by other members of their groups as cues in decision making. Individuals must balance the private information they receive from their own sensory cues with the social information provided by observing what others have chosen. These two cues can be integrated using decision making rules, which specify the probability to select one or other options based on the quality and quantity of social and non-social information. Previous empirical work has investigated which decision making rules can replicate the observable features of collective decision making, while other theoretical research has derived forms for decision making rules based on normative assumptions about how rational agents should respond to the available information. Here we explore the performance of one commonly used decision making rule in terms of the expected decision accuracy of individuals employing it. We show that parameters of this model which have typically been treated as independent variables in empirical model-fitting studies obey necessary relationships under the assumption that animals are evolutionarily optimised to their environment. We further investigate whether this decision making model is appropriate to all animal groups by testing its evolutionary stability to invasion by alternative strategies that use social information differently, and show that the likely evolutionary equilibrium of these strategies depends sensitively on the precise nature of group identity among the wider population of animals it is embedded within.

Thoughts from the forest floor: a review of cognition in the slime mould Physarum polycephalum.

Sensing, communication, navigation, decision-making, memory and learning are key components in a standard cognitive tool-kit that enhance an animal's ability to successfully survive and reproduce. However, these tools are not only useful for, or accessible to, animals-they evolved long ago in simpler organisms using mechanisms which may be either unique or widely conserved across diverse taxa. In this article, I review the recent research that demonstrates these key cognitive abilities in the plasmodial slime mould Physarum polycephalum, which has emerged as a model for non-animal cognition. I discuss the benefits and limitations of comparisons drawn between neural and non-neural systems, and the implications of common mechanisms across wide taxonomic divisions. I conclude by discussing future avenues of research that will draw the most benefit from a closer integration of Physarum and animal cognition research.

Performance Analysis of the Spanish Men's Top and Second Professional Football Division Teams during Eight Consecutive Seasons.

The present study aimed to analyse the performance of the Spanish men's top (LaLiga1) and second (LaLiga2) professional football division teams for eight consecutive seasons (from 2011-2012 to 2018-2019). The variables recorded were Passes, Successful Passes, Crosses, Shots, Goals, Corners, Fouls, Width, Length, Height, distance from the goalkeeper to the nearest defender (GkDef) and total distance covered (TD). The main results were that (1) LaLiga1 teams showed lower values of Length from 2013-2014, and lower values of GkDef and TD from 2014-2015; (2) LaLiga2 teams showed fewer Passes and lower values of GkDef and TD from 2014-2015, and fewer Goals and lower values of Length from 2015-2016; and (3) LaLiga1 teams showed more Passes, Successful Passes, Shots and Goals and higher values of TD compared to LaLiga2 teams during the eight-season period. This study concludes that LaLiga1 teams showed fewer final offensive actions, LaLiga2 teams showed fewer Passes and Goals and the teams of both leagues played in a space with greater density (meters by player), covering less distance as the seasons passed. The information provided in this study makes it possible to have reference values that have characterised the performance of the teams.

Comparing Synchronicity in Body Movement among Jazz Musicians with Their Emotions.

This paper presents novel preliminary research that investigates the relationship between the flow of a group of jazz musicians, quantified through multi-person pose synchronization, and their collective emotions. We have developed a real-time software to calculate the physical synchronicity of team members by tracking the difference in arm, leg, and head movements using Lightweight OpenPose. We employ facial expression recognition to evaluate the musicians' collective emotions. Through correlation and regression analysis, we establish that higher levels of synchronized body and head movements correspond to lower levels of disgust, anger, sadness, and higher levels of joy among the musicians. Furthermore, we utilize 1-D CNNs to predict the collective emotions of the musicians. The model leverages 17 body synchrony keypoint vectors as features, resulting in a training accuracy of 61.47% and a test accuracy of 66.17%.

Synchronisation of glycolytic activity in yeast cells.

Glycolysis is the central metabolic pathway of almost every cell and organism. Under appropriate conditions, glycolytic oscillations may occur in individual cells as well as in entire cell populations or tissues. In many biological systems, glycolytic oscillations drive coherent oscillations of other metabolites, for instance in cardiomyocytes near anorexia, or in pancreas where they lead to a pulsatile release of insulin. Oscillations at the population or tissue level require the cells to synchronize their metabolism. We review the progress achieved in studying a model organism for glycolytic oscillations, namely yeast. Oscillations may occur on the level of individual cells as well as on the level of the cell population. In yeast, the cell-to-cell interaction is realized by diffusion-mediated intercellular communication via a messenger molecule. The present mini-review focuses on the synchronisation of glycolytic oscillations in yeast. Synchronisation is a quorum-sensing phenomenon because the collective oscillatory behaviour of a yeast cell population ceases when the cell density falls below a threshold. We review the question, under which conditions individual cells in a sparse population continue or cease to oscillate. Furthermore, we provide an overview of the pathway leading to the onset of synchronized oscillations. We also address the effects of spatial inhomogeneities (e.g., the formation of spatial clusters) on the collective dynamics, and also review the emergence of travelling waves of glycolytic activity. Finally, we briefly review the approaches used in numerical modelling of synchronized cell populations.

Intergenerational genotypic interactions drive collective behavioural cycles in a social insect.

Many social animals display collective activity cycles based on synchronous behavioural oscillations across group members. A classic example is the colony cycle of army ants, where thousands of individuals undergo stereotypical biphasic behavioural cycles of about one month. Cycle phases coincide with brood developmental stages, but the regulation of this cycle is otherwise poorly understood. Here, we probe the regulation of cycle duration through interactions between brood and workers in an experimentally amenable army ant relative, the clonal raider ant. We first establish that cycle length varies across clonal lineages using long-term monitoring data. We then investigate the putative sources and impacts of this variation in a cross-fostering experiment with four lineages combining developmental, morphological and automated behavioural tracking analyses. We show that cycle length variation stems from variation in the duration of the larval developmental stage, and that this stage can be prolonged not only by the clonal lineage of brood (direct genetic effects), but also of the workers (indirect genetic effects). We find similar indirect effects of worker line on brood adult size and, conversely (but more surprisingly), indirect genetic effects of the brood on worker behaviour (walking speed and time spent in the nest).

Self-organization and information transfer in Antarctic krill swarms.

Antarctic krill swarms are one of the largest known animal aggregations, and yet, despite being the keystone species of the Southern Ocean, little is known about how swarms are formed and maintained. Understanding the local interactions between individuals that provide the basis for these swarms is fundamental to knowing how swarms arise in nature, and what potential factors might lead to their breakdown. Here, we analysed the trajectories of captive, wild-caught krill in 3D to determine individual-level interaction rules and quantify patterns of information flow. Our results demonstrate that krill align with near neighbours and that they regulate both their direction and speed relative to the positions of groupmates. These results suggest that social factors are vital to the formation and maintenance of swarms. Furthermore, krill operate a novel form of collective organization, with measures of information flow and individual movement adjustments expressed most strongly in the vertical dimension, a finding not seen in other swarming species. This research represents a vital step in understanding the fundamentally important swarming behaviour of krill.

The visual coupling between neighbours explains local interactions underlying human 'flocking'.

Patterns of collective motion in bird flocks, fish schools and human crowds are believed to emerge from local interactions between individuals. Most 'flocking' models attribute these local interactions to hypothetical rules or metaphorical forces and assume an omniscient third-person view of the positions and velocities of all individuals in space. We develop a visual model of collective motion in human crowds based on the visual coupling that governs pedestrian interactions from a first-person embedded viewpoint. Specifically, humans control their walking speed and direction by cancelling the average angular velocity and optical expansion/contraction of their neighbours, weighted by visibility (1 - occlusion). We test the model by simulating data from experiments with virtual crowds and real human 'swarms'. The visual model outperforms our previous omniscient model and explains basic properties of interaction: 'repulsion' forces reduce to cancelling optical expansion, 'attraction' forces to cancelling optical contraction and 'alignment' to cancelling the combination of expansion/contraction and angular velocity. Moreover, the neighbourhood of interaction follows from Euclid's Law of perspective and the geometry of occlusion. We conclude that the local interactions underlying human flocking are a natural consequence of the laws of optics. Similar perceptual principles may apply to collective motion in other species.

The social transmission of stress in animal collectives.

The stress systems are powerful mediators between the organism's systemic dynamic equilibrium and changes in its environment beyond the level of anticipated fluctuations. Over- or under-activation of the stress systems' responses can impact an animal's health, survival and reproductive success. While physiological stress responses and their influence on behaviour and performance are well understood at the individual level, it remains largely unknown whether-and how-stressed individuals can affect the stress systems of other group members, and consequently their collective behaviour. Stressed individuals could directly signal the presence of a stressor (e.g. via an alarm call or pheromones), or an acute or chronic activation of the stress systems could be perceived by others (as an indirect cue) and spread via social contagion. Such social transmission of stress responses could then amplify the effects of stressors by impacting social interactions, social dynamics and the collective performance of groups. As the neuroendocrine pathways of the stress response are highly conserved among vertebrates, transmission of physiological stress states could be more widespread among non-human animals than previously thought. We therefore suggest that identifying the extent to which stress transmission modulates animal collectives represents an important research avenue.

Defensive shimmering responses in Apis dorsata are triggered by dark stimuli moving against a bright background.

Giant honeybees, including the open-nesting Asian giant honeybee Apis dorsata, display a spectacular collective defence behaviour - known as 'shimmering' - against predators, which is characterised by travelling waves generated by individual bees flipping their abdomens in a coordinated and sequential manner across the bee curtain. We examined whether shimmering is visually mediated by presenting moving stimuli of varying sizes and contrasts to the background (dark or light) in bright and dim ambient light conditions. Shimmering was strongest under bright ambient light, and its strength declined under dim light in this facultatively nocturnal bee. Apis dorsata shimmered only when presented with the darkest stimulus against a light background, but not when this condition was reversed (light stimulus against dark background). This response did not attenuate with repeated exposure to the stimuli, suggesting that shimmering behaviour does not undergo habituation. We suggest that this is an effective anti-predator strategy in open-nesting A. dorsata colonies which are exposed to high ambient light, as flying predators are more easily detected when they appear as dark moving objects against a bright sky. Moreover, the stimulus detection threshold (smallest visual angular size) is much smaller in this anti-predatory context (1.6-3.4 deg) than in the context of foraging (5.7 deg), indicating that ecological context affects the visual detection threshold.