Hydration state does not affect selected body temperature during gravidity or gravidity duration in pythons (Antaresia childreni).

The embryonic development of many ectothermic species are highly sensitive to temperature and typically have a higher thermal optima than do most other physiological processes. Thus, female ectotherms often maintain a higher and more carefully controlled body temperature when she is supporting developing embryos (early development in oviparous species, throughout development in viviparous species). Considering the positive correlation between body temperature and evaporative water loss, this response could potentially exacerbate female water imbalance in water-limited environments, suggesting that female water balance and egg development may be in conflict. Using Children's pythons (Antaresia childreni), we hypothesized that water deprivation reduces thermophily during gravidity. We split reproductive females into two thermal treatments: those provided with a continuously available thermal gradient of 25-45 °C and those kept at a constant 31 °C. We also had seven non-reproductive females that were provided a thermal gradient. Within each thermal treatment group, we alternatingly assigned females to either have or not have water throughout gravidity. We found that reproduction increased female body temperature, but this increase was not affected by water regime. Reproduction also increased plasma osmolality, and lack of water during gravidity exacerbated this effect. We also found that thermal treatment, but not water regime, significantly influenced gravidity duration, with females given a thermogradient having a shorter gravidity duration, likely as a result of having a higher average body temperature than did the females provided constant heat. Finally, we found that females provided water throughout gravidity had greater clutch masses than did females without water. Further research is needed to improve scientific understanding of the interactions among water balance, body temperature, and various physiological performances.

Weaver ants regulate the rate of prey delivery during collective vertical transport.

The collective transport of massive food items by ant teams is a striking example of biological cooperation, but it remains unclear how these decentralized teams coordinate to overcome the various challenges associated with transport. Previous research has focused on transport across horizontal surfaces and very shallow inclines, disregarding the complexity of natural foraging environments. In the ant Oecophylla smaragdina, prey are routinely carried up tree trunks to arboreal nests. Using this species, we induced collective transport over a variety of angled surfaces with varying prey masses to investigate how ants respond to inclines. We found that weight and incline pose qualitatively different challenges during transport. Prey were carried over vertical and inclined surfaces faster than across horizontal surfaces, even though inclines were associated with longer routes and a higher probability of dropping the load. This additional speed was associated with more transporters being allocated to loads on steeper inclines and not with the persistence of individual ants. Ant teams also regulated a stable prey delivery rate (rate of return per transporter) across all treatments. Our proposed constrained optimization model suggests a possible explanation for these results; theoretically, prey intake rate at the colony level is maximized when the allocation of transporters yields a similar prey delivery rate across loads.

Coordination of movement via complementary interactions of leaders and followers in termite mating pairs.

In collective animal motion, coordination is often achieved by feedback between leaders and followers. For stable coordination, a leader's signals and a follower's responses are hypothesized to be attuned to each other. However, their roles are difficult to disentangle in species with highly coordinated movements, hiding potential diversity of behavioural mechanisms for collective behaviour. Here, we show that two Coptotermes termite species achieve a similar level of coordination via distinct sets of complementary leader-follower interactions. Even though C. gestroi females produce less pheromone than C. formosanus, tandem runs of both species were stable. Heterospecific pairs with C. gestroi males were also stable, but not those with C. formosanus males. We attributed this to the males' adaptation to the conspecific females; C. gestroi males have a unique capacity to follow females with small amounts of pheromone, while C. formosanus males reject C. gestroi females as unsuitable but are competitive over females with large amounts of pheromone. An information-theoretic analysis supported this conclusion by detecting information flow from female to male only in stable tandems. Our study highlights cryptic interspecific variation in movement coordination, a source of novelty for the evolution of social interactions.

Complex Relationship between Tunneling Patterns and Individual Behaviors in Termites.

AbstractThe nests built by social insects are complex group-level structures that emerge from interactions among individuals following simple behavioral rules. Nest patterns vary among species, and the theory of complex systems predicts that there is no simple one-to-one relationship between variation in collective patterns and variation in individual behaviors. Therefore, a species-by-species comparison of the actual building process is essential to understand the mechanism producing diverse nest patterns. Here, we compare tunnel formation of three termite sp ecies and reveal two mechanisms producing interspecific variation: in one, a common behavioral rule yields distinct patterns via parameter tuning, and in the other, distinct rules produce similar patterns. We found that two related species transport sand in the same way using mandibles but build tunnels with different degrees of branching. The variation arises from different probabilities of choosing between two behavioral options at crowded tunnel faces: excavating the sidewall to make a new branch or waiting for clearance to extend the current tunnel. We further discovered that a third species independently evolved low-branched patterns using different building rules, namely, a bucket brigade that can excavate a crowded tunnel. Our findings emphasize the importance of direct comparative study of collective behaviors at both individual and group levels.

Division of labour promotes the spread of information in colony emigrations by the ant Temnothorax rugatulus.

The fitness of group-living animals often depends on how well members share information needed for collective decision-making. Theoretical studies have shown that collective choices can emerge in a homogeneous group of individuals following identical rules, but real animals show much evidence for heterogeneity in the degree and nature of their contribution to group decisions. In social insects, for example, the transmission and processing of information is influenced by a well-organized division of labour. Studies that accurately quantify how this behavioural heterogeneity affects the spread of information among group members are still lacking. In this paper, we look at nest choices during colony emigrations of the ant Temnothorax rugatulus and quantify the degree of behavioural heterogeneity of workers. Using clustering methods and network analysis, we identify and characterize four behavioural castes of workers-primary, secondary, passive and wandering-covering distinct roles in the spread of information during an emigration. This detailed characterization of the contribution of each worker can improve models of collective decision-making in this species and promises a deeper understanding of behavioural variation at the colony level.

Route learning during tandem running in the rock ant Temnothorax albipennis.

Many animals use information from conspecifics to change their behavior in adaptive ways. When a rock ant, Temnothorax albipennis, finds food, she returns to her colony and uses a method called tandem running to lead nestmates, one at a time, from the nest to the food. In this way, naive ants can learn the location of a food source. Less clear is whether they also learn navigational cues that guide them from nest to food, although this is often assumed. We tested this idea by tracing the routes of individually marked ants as they followed tandem runs to a feeder, returned to the nest, and later traveled independently back to the food. Our results show, for the first time, that tandem run followers learn specific routes from their leaders. Independent journeys back to the food source were significantly more similar to the routes on which the ants had been led, compared with the routes taken by other tandem runs. In contrast, the homeward journey did not resemble the tandem run route. These results are consistent with followers memorizing visual cues during the tandem run that are useful for recapitulating the outward journey, but not as effective when facing in the opposite direction on the homeward journey. We further showed that foraging routes improved through individual experience over multiple trips but not through the social transfer of route information via tandem running. We discuss our findings in relation to social learning and integration of individual and social information in ants.

Termite males enhance mating encounters by changing speed according to density.

Search theory predicts that animals evolve efficient movement patterns to enhance encounter rates with specific targets. The optimal movements vary with the surrounding environments, which may explain the observation that animals often switch their movement patterns depending on conditions. However, the effectiveness of behavioural change during search is rarely evaluated because it is difficult to examine the actual encounter dynamics. Here we studied how partner-seeking termites update their search strategies depending on the local densities of potential mates. After a dispersal flight, termites drop their wings and walk to search for a mate; when a female and a male meet, they form a female-led tandem pair and search for a favourable nesting site. If a pair is separated, they have two search options-reunite with their stray partner, or seek a new partner. We hypothesized that the density of individuals affects separation-reunion dynamics and thus the optimal search strategy. We observed the searching process across different densities and found that termite pairs were often separated but obtained a new partner quickly at high mate density. After separation, while females consistently slowed down, males increased their speed according to the density. Under high mate density, separated males obtained a partner earlier than females, who do not change movement with density. Our data-based simulations confirmed that the observed behavioural change by males contributes to enhancing encounters. Males at very low mate densities did best to move slowly and thereby reduce the risk of missing their stray partner, who is the only available mate. On the other hand, males that experienced high mate densities did better in mating encounters by moving fast because the risk of isolation is low, and they must compete with other males to find a partner. These results demonstrate that termite males adaptively update their search strategy depending on conditions. Understanding the encounter dynamics experienced by animals is key to connecting the empirical work to the idealized search processes of theoretical studies.

Inferring collective behaviour from a fossilized fish shoal.

Collective motion by animal groups can emerge from simple rules that govern each individual's interactions with its neighbours. Studies of extant species have shown how such rules yield coordinated group behaviour, but little is known of their evolutionary origins or whether extinct group-living organisms used similar rules. Here, we report evidence consistent with coordinated collective motion in a fossilized group of the extinct fish Erismatopterus levatus, and we infer possible behavioural rules that underlie it. We found traces of two rules for social interaction similar to those used by extant fishes: repulsion from close individuals and attraction towards neighbours at a distance. Moreover, the fossilized fish showed group-level structures in the form of oblong shape and high polarization, both of which we successfully reproduced in simulations incorporating the inferred behavioural rules. Although it remains unclear how the fish shoal's structure was preserved in the fossil, these findings suggest that fishes have been forming shoals by combining sets of simple behavioural rules since at least the Eocene. Our study highlights the possibility of exploring the social communication of extinct animals, which has been thought to leave no fossil record.

Symmetry breaking and pivotal individuals during the reunification of ant colonies.

Maintenance of a social group requires the ability to reach consensus when faced with divisive choices. Thus, when migrating colonies of the ant Temnothorax rugatulus split among multiple sites, they can later reunify on the basis of queen location or differences in site quality. In this study, we found that colonies can reunify even without obvious cues to break the symmetry between sites. To learn how they do so, we observed both symmetric reunifications (between identical nests) and asymmetric reunifications (between nests of unequal quality) by colonies of individually marked ants. Both reunification types were accomplished by a tiny minority that carried nestmates from the 'losing' to the 'winning' site. Reunification effort was highly skewed in asymmetric splits, where the majority of the work was done by the first ant to transport, which nearly always came from the winning site. This contrasted with symmetric splits, where the initiator did not play an outsize role and was just as likely to come from the losing site. Symmetric reunifications were also characterized by high transporter attrition, which may help to prevent deadlocks. Tandem runs were abundant in both types and were typically led by transporters as they returned to the losing site to fetch another nestmate. Few tandem followers joined the transport effort, suggesting that tandem runs do not serve to recruit transporters but may have another, as yet unidentified role. Our results underscore the potentially large contribution of highly active individuals to group behaviour, even in decentralized societies such as ant colonies.

Rational time investment during collective decision making in Temnothorax ants.

The study of rational choice in humans and other animals typically focuses on decision outcomes, but rationality also applies to decision latencies, especially when time is scarce and valuable. For example, the smaller the difference in quality between two options, the faster a rational actor should decide between them. This is because the consequences of choosing the inferior option are less severe if the options are similar. Experiments have shown, however, that humans irrationally spend more time choosing between similar options. In this study, we assessed the rationality of time investment during nest-site choice by the rock ant, Temnothorax albipennis. Previous studies have shown that collective decision-making allows ant colonies to avoid certain irrational errors. Here we show that the same is true for time investment. Individual ants, like humans, irrationally took more time to complete an emigration when choosing between two similar nests than when choosing between two less similar nests. Whole colonies, by contrast, rationally made faster decisions when the options were more similar. We discuss the underlying mechanisms of decision-making in individuals and colonies and how they lead to irrational and rational time investment, respectively.

The Psychology of Superorganisms: Collective Decision Making by Insect Societies.

Under the superorganism concept, insect societies are so tightly integrated that they possess features analogous to those of single organisms, including collective cognition. If so, colony function might fruitfully be studied using methods developed to understand individual animals. Here, we review research that uses psychological approaches to understand decision making by colonies. The application of neural models to collective choice shows fundamental similarities between how brains and colonies balance speed/accuracy trade-offs in decision making. Experimental analyses have explored collective rationality, cognitive capacity, and perceptual discrimination at both individual and colony levels. A major theme is the emergence of improved colony-level function from interactions among relatively less capable individuals. However, colonies also encounter performance costs due to their reliance on positive feedback, which generates consensus but can also amplify errors. Collective learning is a nascent field for the further application of psychological methods to colonies. The research strategy reviewed here shows how the superorganism concept can serve as more than an illustrative analogy.

A Simple Behavioral Model Predicts the Emergence of Complex Animal Hierarchies.

Social dominance hierarchies are widespread, but little is known about the mechanisms that produce nonlinear structures. In addition to despotic hierarchies, where a single individual dominates, shared hierarchies exist, where multiple individuals occupy a single rank. In vertebrates, these complex dominance relationships are thought to develop from interactions that require higher cognition, but similar cases of shared dominance have been found in social insects. Combining empirical observations with a modeling approach, we show that all three hierarchy structures-linear, despotic, and shared-can emerge from different combinations of simple interactions present in social insects. Our model shows that a linear hierarchy emerges when a typical winner-loser interaction (dominance biting) is present. A despotic hierarchy emerges when a policing interaction is added that results in the complete loss of dominance status for an attacked individual (physical policing). Finally, a shared hierarchy emerges with the addition of a winner-winner interaction that results in a positive outcome for both interactors (antennal dueling). Antennal dueling is an enigmatic ant behavior that has previously lacked a functional explanation. These results show how complex social traits can emerge from simple behaviors without requiring advanced cognition.

Ant colonies outperform individuals when a sensory discrimination task is difficult but not when it is easy.

"Collective intelligence" and "wisdom of crowds" refer to situations in which groups achieve more accurate perception and better decisions than solitary agents. Whether groups outperform individuals should depend on the kind of task and its difficulty, but the nature of this relationship remains unknown. Here we show that colonies of Temnothorax ants outperform individuals for a difficult perception task but that individuals do better than groups when the task is easy. Subjects were required to choose the better of two nest sites as the quality difference was varied. For small differences, colonies were more likely than isolated ants to choose the better site, but this relationship was reversed for large differences. We explain these results using a mathematical model, which shows that positive feedback between group members effectively integrates information and sharpens the discrimination of fine differences. When the task is easier the same positive feedback can lock the colony into a suboptimal choice. These results suggest the conditions under which crowds do or do not become wise.

Population genomic analysis of outcrossing and recombination in yeast.

The budding yeast Saccharomyces cerevisiae has been used by humans for millennia to make wine, beer and bread. More recently, it became a key model organism for studies of eukaryotic biology and for genomic analysis. However, relatively little is known about the natural lifestyle and population genetics of yeast. One major question is whether genetically diverse yeast strains mate and recombine in the wild. We developed a method to infer the evolutionary history of a species from genome sequences of multiple individuals and applied it to whole-genome sequence data from three strains of Saccharomyces cerevisiae and the sister species Saccharomyces paradoxus. We observed a pattern of sequence variation among yeast strains in which ancestral recombination events lead to a mosaic of segments with shared genealogy. Based on sequence divergence and the inferred median size of shared segments (approximately 2,000 bp), we estimated that although any two strains have undergone approximately 16 million cell divisions since their last common ancestor, only 314 outcrossing events have occurred during this time (roughly one every 50,000 divisions). Local correlations in polymorphism rates indicate that linkage disequilibrium in yeast should extend over kilobases. Our results provide the initial foundation for population studies of association between genotype and phenotype in S. cerevisiae.

A context-dependent alarm signal in the ant Temnothorax rugatulus.

Because collective cognition emerges from local signaling among group members, deciphering communication systems is crucial to understanding the underlying mechanisms. Alarm signals are widespread in the social insects and can elicit a variety of behavioral responses to danger, but the functional plasticity of these signals has not been well studied. Here we report an alarm pheromone in the ant Temnothorax rugatulus that elicits two different behaviors depending on context. When an ant was tethered inside an unfamiliar nest site and unable to move freely, she released a pheromone from her mandibular gland that signaled other ants to reject this nest as a potential new home, presumably to avoid potential danger. When the same pheromone was presented near the ants' home nest, they were instead attracted to it, presumably to respond to a threat to the colony. We used coupled gas chromatography/mass spectrometry to identify candidate compounds from the mandibular gland and tested each one in a nest choice bioassay. We found that 2,5-dimethylpyrazine was sufficient to induce rejection of a marked new nest and also to attract ants when released at the home nest. This is the first detailed investigation of chemical communication in the leptothoracine ants. We discuss the possibility that this pheromone's deterrent function can improve an emigrating colony's nest site selection performance.

Ants learn to rely on more informative attributes during decision-making.

Evolutionary theory predicts that animals act to maximize their fitness when choosing among a set of options, such as what to eat or where to live. Making the best choice is challenging when options vary in multiple attributes, and animals have evolved a variety of heuristics to simplify the task. Many of these involve ranking or weighting attributes according to their importance. Because the importance of attributes can vary across time and place, animals might benefit by adjusting weights accordingly. Here, we show that colonies of the ant Temnothorax rugatulus use their experience during nest site selection to increase weights on more informative nest attributes. These ants choose their rock crevice nests on the basis of multiple features. After exposure to an environment where only one attribute differentiated options, colonies increased their reliance on this attribute relative to a second attribute. Although many species show experience-based changes in selectivity based on a single feature, this is the first evidence in animals for adaptive changes in the weighting of multiple attributes. These results show that animal collectives, like individuals, change decision-making strategies according to experience. We discuss how these colony-level changes might emerge from individual behaviour.

Is collective nest site selection in ants influenced by the anchoring effect?

Evolutionary theory predicts that animals make decisions that maximize fitness. If so, they are expected to adhere to principles of rational choice, which a decision-maker must follow to reliably maximize net benefit. For example, evaluation of an option should not be influenced by the quality of other unchosen options. However, humans and other animals are known to evaluate a mediocre option more favorably after encountering poor options than after encountering no options, a phenomenon known as the 'anchoring effect'. Rationality is also expected in the consensus decisions of animal societies, but the anchoring effect has not previously been tested in that context. Here we show that colonies of the rock ant, Temnothorax rugatulus, demonstrate the anchoring effect during nest site selection - colonies moved more readily from a mediocre nest to a good nest when exposed to poor nests than when exposed to mediocre nests. This effect depended on both current conditions and past experience; movement probability was affected only when colonies were exposed to surrounding nests before and during the emigration. The effect was small, reaching statistical significance in only one of two experimental replicates. We discuss possible mechanisms and ultimate explanations for why colonies show this seemingly suboptimal behavior.

Protocol to obtain long movement trajectories of leaders and followers in ant tandem runs.

Tandem running in ants is a sophisticated form of communication. Precise measurement of movement coordination by the tandem pair can shed light on social interactions. Here, we describe an integrative approach to obtain long movement trajectories of a specific tandem pair within a crowd of ants. We describe a maze-like arena, video recording and editing, and movement tracking. We integrate two pieces of image-based tracking software that have distinct individual assignment strategies. This protocol aids comparative studies of recruitment communication across species. For complete details on the use and execution of this protocol, please refer to Mizumoto et al. (2023)1 and Valentini et al. (2020).2.

Functional and mechanistic diversity in ant tandem communication.

Communication is fundamental to the organization of animal societies, often resulting in the convergent evolution of similar social behavior across lineages. However, this similarity may conceal underlying functional and mechanistic differences. Here we combined network and information-theoretic analysis to quantify how tandem recruitment is distinguishable between two ant genera, Temnothorax and Diacamma. We show that Temnothorax uses tandem running to recruit additional recruiters, while Diacamma uses it principally to move the passive majority of their colony, a task that Temnothorax accomplishes with a different behavior, social carrying. Accordingly, the network structure of Diacamma tandems was dissimilar to that of Temnothorax, instead resembling the social-carrying networks in Temnothorax. Furthermore, our information-theoretical analysis on movement trajectories revealed that Diacamma tandem runs lack bidirectional information transfer, the signature of route learning in Temnothorax. By quantifying the diversity of similar communication systems, this study increases the resolution of our understanding of animal societies.

The Power of Population Effect in Temnothorax Ant House-Hunting: A Computational Modeling Approach.

The decentralized cognition of animal groups is both a challenging biological problem and a potential basis for bioinspired design. In this study, we investigated the house-hunting algorithm used by emigrating colonies of Temnothorax ants to reach consensus on a new nest. We developed a tractable model that encodes accurate individual behavior rules, and estimated our parameter values by matching simulated behaviors with observed ones on both the individual and group levels. We then used our model to explore a potential, but yet untested, component of the ants' decision algorithm. Specifically, we examined the hypothesis that incorporating site population (the number of adult ants at each potential nest site) into individual perceptions of nest quality can improve emigration performance. Our results showed that attending to site population accelerates emigration and reduces the incidence of split decisions. This result suggests the value of testing empirically whether nest site scouts use site population in this way, in addition to the well-demonstrated quorum rule. We also used our model to make other predictions with varying degrees of empirical support, including the high cognitive capacity of colonies and their rational time investment during decision-making. In addition, we provide a versatile and easy-to-use Python simulator that can be used to explore other hypotheses or make testable predictions. It is our hope that the insights and the modeling tools can inspire further research from both the biology and computer science community.