It pays to follow the leader: Metabolic cost of flight is lower for trailing birds in small groups.

Many bird species commonly aggregate in flocks for reasons ranging from predator defense to navigation. Available evidence suggests that certain types of flocks-the V and echelon formations of large birds-may provide a benefit that reduces the aerodynamic cost of flight, whereas cluster flocks typical of smaller birds may increase flight costs. However, metabolic flight costs have not been directly measured in any of these group flight contexts [Zhang and Lauder, J. Exp. Biol. 226, jeb245617 (2023)]. Here, we measured the energetic benefits of flight in small groups of two or three birds and the requirements for realizing those benefits, using metabolic energy expenditure and flight position measurements from European Starlings flying in a wind tunnel. The starlings continuously varied their relative position during flights but adopted a V formation motif on average, with a modal spanwise and streamwise spacing of [0.81, 0.91] wingspans. As measured via CO2 production, flight costs for follower birds were significantly reduced compared to their individual solo flight benchmarks. However, followers with more positional variability with respect to leaders did less well, even increasing their costs above solo flight. Thus, we directly demonstrate energetic costs and benefits for group flight followers in an experimental context amenable to further investigation of the underlying aerodynamics, wake interactions, and bird characteristics that produce these metabolic effects.

Collective Hall current in chiral active fluids: Coupling of phase and mass transport through traveling bands.

Active fluids composed of constituents that are constantly driven away from thermal equilibrium can support spontaneous currents and can be engineered to have unconventional transport properties. Here, we report the emergence of (meta)stable traveling bands in computer simulations of aligning circle swimmers. These bands are different from polar flocks and, through coupling phase with mass transport, induce a bulk particle current with a component perpendicular to the propagation direction, thus giving rise to a collective Hall (or Magnus) effect. Traveling bands require sufficiently small orbits and undergo a discontinuous transition into a synchronized state with transient polar clusters for large orbital radii. Within a minimal hydrodynamic theory, we show that the bands can be understood as nondispersive soliton solutions fully accounting for the numerically observed properties.

Extinct and extant termites reveal the fidelity of behavior fossilization in amber.

Fossils encompassing multiple individuals provide rare direct evidence of behavioral interactions among extinct organisms. However, the fossilization process can alter the spatial relationship between individuals and hinder behavioral reconstruction. Here, we report a Baltic amber inclusion preserving a female-male pair of the extinct termite species Electrotermes affinis. The head-to-abdomen contact in the fossilized pair resembles the tandem courtship behavior of extant termites, although their parallel body alignment differs from the linear alignment typical of tandem runs. To solve this inconsistency, we simulated the first stage of amber formation, the immobilization of captured organisms, by exposing living termite tandems to sticky surfaces. We found that the posture of the fossilized pair matches trapped tandems and differs from untrapped tandems. Thus, the fossilized pair likely is a tandem running pair, representing the direct evidence of the mating behavior of extinct termites. Furthermore, by comparing the postures of partners on a sticky surface and in the amber inclusion, we estimated that the male likely performed the leader role in the fossilized tandem. Our results demonstrate that past behavioral interactions can be reconstructed despite the spatial distortion of body poses during fossilization. Our taphonomic approach demonstrates how certain behaviors can be inferred from fossil occurrences.

Selective social interactions and speed-induced leadership in schooling fish.

Animals moving together in groups are believed to interact among each other with effective social forces, such as attraction, repulsion, and alignment. Such forces can be inferred using "force maps," i.e., by analyzing the dependency of the acceleration of a focal individual on relevant variables. Here, we introduce a force map technique suitable for the analysis of the alignment forces experienced by individuals. After validating it using an agent-based model, we apply the force map to experimental data of schooling fish. We observe signatures of an effective alignment force with faster neighbors and an unexpected antialignment with slower neighbors. Instead of an explicit antialignment behavior, we suggest that the observed pattern is the result of a selective attention mechanism, where fish pay less attention to slower neighbors. This mechanism implies the existence of temporal leadership interactions based on relative speeds between neighbors. We present support for this hypothesis both from agent-based modeling as well as from exploring leader-follower relationships in the experimental data.

Direct measurement of dynamic attractant gradients reveals breakdown of the Patlak-Keller-Segel chemotaxis model.

Chemotactic bacteria not only navigate chemical gradients, but also shape their environments by consuming and secreting attractants. Investigating how these processes influence the dynamics of bacterial populations has been challenging because of a lack of experimental methods for measuring spatial profiles of chemoattractants in real time. Here, we use a fluorescent sensor for aspartate to directly measure bacterially generated chemoattractant gradients during collective migration. Our measurements show that the standard Patlak-Keller-Segel model for collective chemotactic bacterial migration breaks down at high cell densities. To address this, we propose modifications to the model that consider the impact of cell density on bacterial chemotaxis and attractant consumption. With these changes, the model explains our experimental data across all cell densities, offering insight into chemotactic dynamics. Our findings highlight the significance of considering cell density effects on bacterial behavior, and the potential for fluorescent metabolite sensors to shed light on the complex emergent dynamics of bacterial communities.

History constrains the evolution of efficient color naming, enabling historical inference.

Color naming in natural languages is not arbitrary: It reflects efficient partitions of perceptual color space [T. Regier, P. Kay, N. Khetarpal, Proc. Natl. Acad. Sci. U.S.A. 104, 1436-1441 (2007)] modulated by the relative needs to communicate about different colors [C. Twomey, G. Roberts, D. Brainard, J. Plotkin, Proc. Natl. Acad. Sci. U.S.A. 118, e2109237118 (2021)]. These psychophysical and communicative constraints help explain why languages around the world have remarkably similar, but not identical, mappings of colors to color terms. Languages converge on a small set of efficient representations.But languages also evolve, and the number of terms in a color vocabulary may change over time. Here we show that history, i.e. the existence of an antecedent color vocabulary, acts as a nonadaptive constraint that biases the choice of efficient solution as a language transitions from a vocabulary of size [Formula: see text] to [Formula: see text] terms. Moreover, as efficient vocabularies evolve to include more terms they explore a smaller fraction of all possible efficient vocabularies compared to equally sized vocabularies constructed de novo. This path dependence of the cultural evolution of color naming presents an opportunity. Historical constraints can be used to reconstruct ancestral color vocabularies, allowing us to answer long-standing questions about the evolutionary sequences of color words, and enabling us to draw inferences from phylogenetic patterns of language change.

A simple mechanism for collective decision-making in the absence of payoff information.

Animals are often faced with time-critical decisions without prior information about their actions' outcomes. In such scenarios, individuals budget their investment into the task to cut their losses in case of an adverse outcome. In animal groups, this may be challenging because group members can only access local information, and consensus can only be achieved through distributed interactions among individuals. Here, we combined experimental analyses with theoretical modeling to investigate how groups modulate their investment into tasks in uncertain conditions. Workers of the arboreal weaver ant Oecophylla smaragdina form three-dimensional chains using their own bodies to bridge vertical gaps between existing trails and new areas to explore. The cost of a chain increases with its length because ants participating in the structure are prevented from performing other tasks. The payoffs of chain formation, however, remain unknown to the ants until the chain is complete and they can explore the new area. We demonstrate that weaver ants cap their investment into chains, and do not form complete chains when the gap is taller than 90 mm. We show that individual ants budget the time they spend in chains depending on their distance to the ground, and propose a distance-based model of chain formation that explains the emergence of this tradeoff without the need to invoke complex cognition. Our study provides insights into the proximate mechanisms that lead individuals to engage (or not) in collective actions and furthers our knowledge of how decentralized groups make adaptive decisions in uncertain conditions.

Zebrafish Behavior: Opportunities and Challenges.

A great challenge in neuroscience is understanding how activity in the brain gives rise to behavior. The zebrafish is an ideal vertebrate model to address this challenge, thanks to the capacity, at the larval stage, for precise behavioral measurements, genetic manipulations, and recording and manipulation of neural activity noninvasively and at single-neuron resolution throughout the whole brain. These techniques are being further developed for application in freely moving animals and juvenile stages to study more complex behaviors including learning, decision making, and social interactions. We review some of the approaches that have been used to study the behavior of zebrafish and point to opportunities and challenges that lie ahead.

Crystallography of honeycomb formation under geometric frustration.

As honeybees build their nests in preexisting tree cavities, they must deal with the presence of geometric constraints, resulting in nonregular hexagons and topological defects in the comb. In this work, we study how bees adapt to their environment in order to regulate the comb structure. Specifically, we identify the irregularities in honeycomb structure in the presence of various geometric frustrations. We 3D-print experimental frames with a variety of constraints imposed on the imprinted foundations. The combs constructed by the bees show clear evidence of recurring patterns in response to specific geometric frustrations on these starter frames. Furthermore, using an experimental-modeling framework, we demonstrate that these patterns can be successfully modeled and replicated through a simulated annealing process, in which the minimized potential is a variation of the Lennard-Jones potential that considers only first-neighbor interactions according to a Delaunay triangulation. Our simulation results not only confirm the connection between honeycomb structures and other crystal systems such as graphene, but also show that irregularities in the honeycomb structure can be explained as the result of analogous interactions between cells and their immediate surroundings, leading to emergent global order. Additionally, our computational model can be used as a first step to describe specific strategies that bees use to effectively solve geometric mismatches while minimizing cost of comb building.

The emergence of a collective sensory response threshold in ant colonies.

SignificanceIn this study, we ask how ant colonies integrate information about the external environment with internal state parameters to produce adaptive, system-level responses. First, we show that colonies collectively evacuate the nest when the ground temperature becomes too warm. The threshold temperature for this response is a function of colony size, with larger colonies evacuating the nest at higher temperatures. The underlying dynamics can thus be interpreted as a decision-making process that takes both temperature (external environment) and colony size (internal state) into account. Using mathematical modeling, we show that these dynamics can emerge from a balance between local excitatory and global inhibitory forces acting between the ants. Our findings in ants parallel other complex biological systems like neural circuits.

Collective behavior and nongenetic inheritance allow bacterial populations to adapt to changing environments.

Collective behaviors require coordination among a group of individuals. As a result, individuals that are too phenotypically different from the rest of the group can be left out, reducing heterogeneity, but increasing coordination. If individuals also reproduce, the offspring can have different phenotypes from their parent(s). This raises the question of how these two opposing processes-loss of diversity by collective behaviors and generation of it through growth and inheritance-dynamically shape the phenotypic composition of an isogenic population. We examine this question theoretically using collective migration of chemotactic bacteria as a model system, where cells of different swimming phenotypes are better suited to navigate in different environments. We find that the differential loss of phenotypes caused by collective migration is environment-dependent. With cell growth, this differential loss enables migrating populations to dynamically adapt their phenotype compositions to the environment, enhancing migration through multiple environments. Which phenotypes are produced upon cell division depends on the level of nongenetic inheritance, and higher inheritance leads to larger composition adaptation and faster migration at steady state. However, this comes at the cost of slower responses to new environments. Due to this trade-off, there is an optimal level of inheritance that maximizes migration speed through changing environments, which enables a diverse population to outperform a nondiverse one. Growing populations might generally leverage the selection-like effects provided by collective behaviors to dynamically shape their own phenotype compositions, without mutations.

Ancestral sex-role plasticity facilitates the evolution of same-sex sexual behavior.

Recent attempts to explain the evolutionary prevalence of same-sex sexual behavior (SSB) have focused on the role of indiscriminate mating. However, in many cases, SSB may be more complex than simple mistaken identity, instead involving mutual interactions and successful pairing between partners who can detect each other's sex. Behavioral plasticity is essential for the expression of SSB in such circumstances. To test behavioral plasticity's role in the evolution of SSB, we used termites to study how females and males modify their behavior in same-sex versus heterosexual pairs. Male termites follow females in paired "tandems" before mating, and movement patterns are sexually dimorphic. Previous studies observed that adaptive same-sex tandems also occur in both sexes. Here we found that stable same-sex tandems are achieved by behavioral plasticity when one partner adopts the other sex's movements, resulting in behavioral dimorphism. Simulations based on empirically obtained parameters indicated that this socially cued plasticity contributes to pair maintenance, because dimorphic movements improve reunion success upon accidental separation. A systematic literature survey and phylogenetic comparative analysis suggest that the ancestors of modern termites lack consistent sex roles during pairing, indicating that plasticity is inherited from the ancestor. Socioenvironmental induction of ancestral behavioral potential may be of widespread importance to the expression of SSB. Our findings challenge recent arguments for a prominent role of indiscriminate mating behavior in the evolutionary origin and maintenance of SSB across diverse taxa.

Odd viscosity-induced Hall-like transport of an active chiral fluid.

Broken time-reversal and parity symmetries in active spinner fluids imply a nondissipative "odd viscosity," engendering phenomena unattainable in traditional passive or active fluids. Here we show that the odd viscosity itself can lead to a Hall-like transport when the active chiral fluid flows through a quenched matrix of obstacles, reminiscent of the anomalous Hall effect. The Hall-like velocity depends significantly on the spinner activity and longitudinal flow due to the interplay between odd viscosity and spinner-obstacle collisions. Our findings underscore the importance of odd viscosity in active chiral matter and elucidate its essential role in the anomalous Hall-like effect.

Ant Genetics: Reproductive Physiology, Worker Morphology, and Behavior.

Many exciting studies have begun to elucidate the genetics of the morphological and physiological diversity of ants, but as yet few studies have investigated the genetics of ant behavior directly. Ant genomes are marked by extreme rates of gene turnover, especially in gene families related to olfactory communication, such as the synthesis of cuticular hydrocarbons and the perception of environmental semiochemicals. Transcriptomic and epigenetic differences are apparent between reproductive and sterile females, males and females, and workers that differ in body size. Quantitative genetic approaches suggest heritability of task performance, and population genetic studies indicate a genetic association with reproductive status in some species. Gene expression is associated with behavior including foraging, response to queens attempting to join a colony, circadian patterns of task performance, and age-related changes of task. Ant behavioral genetics needs further investigation of the feedback between individual-level physiological changes and socially mediated responses to environmental conditions.

Multiple Magneto-Optical Microrobotic Collectives with Selective Control in Three Dimensions Under Water.

Inspired by natural swarms, various methods are developed to create artificial magnetic microrobotic collectives. However, these magnetic collectives typically receive identical control inputs from a common external magnetic field, limiting their ability to operate independently. And they often rely on interfaces or boundaries for controlled movement, posing challenges for independent, three-dimensional(3D) navigation of multiple magnetic collectives. To address this challenge, self-assembled microrobotic collectives are proposed that can be selectively actuated in a combination of external magnetic and optical fields. By harnessing both actuation methods, the constraints of single actuation approaches are overcome. The magnetic field excites the self-assembly of colloids and maintains the self-assembled microrobotic collectives without disassembly, while the optical field drives selected microrobotic collectives to perform different tasks. The proposed magnetic-photo microrobotic collectives can achieve independent position and path control in the two-dimensional (2D) plane and 3D space. With this selective control strategy, the microrobotic collectives can cooperate in convection and mixing the dye in a confined space. The results present a systematic approach for realizing selective control of multiple microrobotic collectives, which can address multitasking requirements in complex environments.

The role of vision and lateral line sensing for schooling in giant danios (Devario aequipinnatus).

Schooling is a collective behavior that relies on a fish's ability to sense and respond to the other fish around it. Previous work has identified 'rules' of schooling - attraction to neighbors that are far away, repulsion from neighbors that are too close and alignment with neighbors at the correct distance - but we do not understand well how these rules emerge from the sensory physiology and behavior of individual fish. In particular, fish use both vision and their lateral lines to sense each other, but it is unclear how much they rely on information from these sensory modalities to coordinate schooling behavior. To address this question, we studied how the schooling of giant danios (Devario aequipinnatus) changes when they are unable to see or use their lateral lines. We found that giant danios were able to school without their lateral lines but did not school in darkness. Surprisingly, giant danios in darkness had the same attraction properties as fish in light when they were in close proximity, indicating that they could sense nearby fish with their lateral lines. However, they were not attracted to more distant fish, suggesting that long-distance attraction through vision is important for maintaining a cohesive school. These results help us expand our understanding of the roles that vision and the lateral line play in the schooling of some fish species.

Environmental impact on visual perception modulates behavioral responses of schooling fish to looming predators.

Aggregation in social fishes has evolved to improve safety from predators. The individual interaction mechanisms that govern collective behavior are determined by the sensory systems that translate environmental information into behavior. In dynamic environments, shifts in conditions impede effective visual sensory perception in fish schools, and may induce changes in the collective response. Here, we consider whether environmental conditions that affect visual contrast modulate the collective response of schools to looming predators. By using a virtual environment to simulate four contrast levels, we tested whether the collective state of minnow fish schools was modified in response to a looming optical stimulus. Our results indicate that fish swam slower and were less polarized in lower contrast conditions. Additionally, schooling metrics known to be regulated by non-visual sensory systems tended to correlate better when contrast decreased. Over the course of the escape response, schools remained tightly formed and retained the capability of transferring social information. We propose that when visual perception is compromised, the interaction rules governing collective behavior are likely to be modified to prioritize ancillary sensory information crucial to maximizing chance of escape. Our results imply that multiple sensory systems can integrate to control collective behavior in environments with unreliable visual information.

Chemotaxis in heterogeneous environments: A multi-agent model of decentralized gathering past obstacles.

Chemotaxis, cell migration in response to chemical gradients, is known to promote self-organization of microbiological populations. However, the modeling of chemotaxis in heterogeneous environments is still limited. This study analyzes a decentralized gathering process in environments with physical as well as chemical barriers, using a multi-agent model for Disctyostelium discoideum colonies. Employing a topology-independent metric to quantify the system evolution, we study dynamical features emerging from complex social interactions. The results show that obstacles may hamper the gathering process by altering the flux of chemical signals among amoebas, acting as local topological perturbations. We also find that a minimal set of agent's rules for robust gathering does not require explicit mechanisms for obstacle sensing and avoidance; moreover, random cell movements concur in preventing multiple stable clusters and improve the gathering efficacy. Hence, we speculate that chemotactic cells can avoid obstacles without needing specialized mechanisms: tradeoffs of social interactions and individual fluctuations are sufficient to guarantee the aggregation of the whole colony past numerous obstacles.

Ants find shortest paths using simple, local rules.

Garg et al. (2023, Proceedings of the National Academy of Sciences, 120[6], e2207959120) build simulation models to understand how turtle ants collectively find efficient paths through branched networks, highlighting the importance of bidirectional traffic, leakage of ants at junctions, and the ability to increase flow as key components for efficiency. Their findings provide new, biologically realistic mechanisms that could improve applications in our own engineered networks.

Colony expansions underlie the evolution of army ant mass raiding.

The mass raids of army ants are an iconic collective phenomenon, in which many thousands of ants spontaneously leave their nest to hunt for food, mostly other arthropods. While the structure and ecology of these raids have been relatively well studied, how army ants evolved such complex cooperative behavior is not understood. Here, we show that army ant mass raiding has evolved from a different form of cooperative hunting called group raiding, in which a scout directs a small group of ants to a specific target through chemical communication. We describe the structure of group raids in the clonal raider ant, a close relative of army ants in the subfamily Dorylinae. We find evidence that the coarse structure of group raids and mass raids is highly conserved and that all doryline ants likely follow similar behavioral rules for raiding. We also find that the evolution of army ant mass raiding occurred concurrently with expansions in colony size. By experimentally increasing colony size in the clonal raider ant, we show that mass raiding gradually emerges from group raiding without altering individual behavioral rules. This suggests that increasing colony size can explain the evolution of army ant mass raids and supports the idea that complex social behaviors may evolve via mechanisms that need not alter the behavioral interaction rules that immediately underlie the collective behavior of interest.