Elva J. H. Robinson

Crystal Structure of the SOS Cell Division Inhibitor Sula and in Complex with Ftsz

SulA halts cell division in Escherichia coli by binding to the major component of the division machinery FtsZ. We have solved the crystal structure of SulA alone and in complex with FtsZ from Pseudomonas aeruginosa. SulA is expressed when the SOS response is induced. This is a mechanism to inhibit cell division and repair DNA in the event of DNA damage. FtsZ is a tubulin-like protein that forms polymers, with the active-site GTPase split across two monomers. One monomer provides the GTP-binding site and the other, through its T7 loop nucleotide hydrolysis. Our structures show that SulA is a dimer, and that SulA inhibits cell division neither by binding the nucleotide-binding site nor by inducing conformational changes in FtsZ. Instead, SulA binds the T7 loop surface of FtsZ, opposite the nucleotide-binding site, blocking polymer formation. These findings explain why GTP hydrolysis and polymer turnover are required for SulA inhibition.

Insect communication: ‘No entry’ signal in ant foraging

Forager ants lay attractive trail pheromones to guide nestmates to food, but the effectiveness of foraging networks might be improved if pheromones could also be used to repel foragers from unrewarding routes. Here we present empirical evidence for such a negative trail pheromone, deployed by Pharaohs ants (Monomorium pharaonis) as a ‘no entry’ signal to mark an unrewarding foraging path. This finding constitutes another example of the sophisticated control mechanisms used in self-organized ant colonies.

Radio tagging reveals the roles of corpulence, experience and social information in ant decision making

Ant colonies are factories within fortresses (Oster and Wilson 1978). They run on resources foraged from an outside world fraught with danger. On what basis do individual ants decide to leave the safety of the nest? We investigated the relative roles of social information (returning nestmates), individual experience and physiology (lipid stores/corpulence) in predicting which ants leave the nest and when. We monitored Temnothorax albipennis workers individually using passive radio-frequency identification technology, a novel procedure as applied to ants. This method allowed the matching of individual corpulence measurements to activity patterns of large numbers of individuals over several days. Social information and physiology are both good predictors of when an ant leaves the nest. Positive feedback from social information causes bouts of activity at the colony level. When certain social information is removed from the system by preventing ants returning, physiology best predicts which ants leave the nest and when. Individual experience is strongly related to physiology. A small number of lean individuals are responsible for most external trips. An individual’s nutrient status could be a useful cue in division of labour, especially when public information from other ants is unavailable.

Flexible task allocation and the organization of work in ants

Flexibility in task performance is essential for a robust system of division of labour. We investigated what factors determine which social insect workers respond to colony-level changes in task demand. We used radio-frequency identification technology to compare the roles of corpulence, age, spatial location and previous activity (intra-nest/extra-nest) in determining whether worker ants (Temnothorax albipennis) respond to an increase in demand for foraging or brood care. The less corpulent ants took on the extra foraging, irrespective of their age, previous activity or location in the nest, supporting a physiological threshold model. We found no relationship between ants that tended the extra brood and corpulence, age, spatial location or previous activity, but ants that transported the extra brood to the main brood pile were less corpulent and had high previous intra-nest activity. This supports spatial task-encounter and physiological threshold models for brood transport. Our data suggest a flexible task-allocation system allowing the colony to respond rapidly to changing needs, using a simple task-encounter system for generalized tasks, combined with physiologically based response thresholds for more specialized tasks. This could provide a social insect colony with a robust division of labour, flexibly allocating the workforce in response to current needs.

Do ants make direct comparisons

Many individual decisions are informed by direct comparison of the alternatives. In collective decisions, however, only certain group members may have the opportunity to compare options. Emigrating ant colonies (Temnothorax albipennis) show sophisticated nest-site choice, selecting superior sites even when they are nine times further away than the alternative. How do they do this? We used radio-frequency identification-tagged ants to monitor individual behaviour. Here we show for the first time that switching between nests during the decision process can influence nest choice without requiring direct comparison of nests. Ants finding the poor nest were likely to switch and find the good nest, whereas ants finding the good nest were more likely to stay committed to that nest. When ants switched quickly between the two nests, colonies chose the good nest. Switching by ants that had the opportunity to compare nests had little effect on nest choice. We suggest a new mechanism of collective nest choice: individuals respond to nest quality by the decision either to commit or to seek alternatives. Previously proposed mechanisms, recruitment latency and nest comparison, can be explained as side effects of this simple rule. Colony-level comparison and choice can emerge, without direct comparison by individuals.

A simple threshold rule is sufficient to explain sophisticated collective decision-making.

Decision-making animals can use slow-but-accurate strategies, such as making multiple comparisons, or opt for simpler, faster strategies to find a ‘good enough’ option. Social animals make collective decisions about many group behaviours including foraging and migration. The key to the collective choice lies with individual behaviour. We present a case study of a collective decision-making process (house-hunting ants, Temnothorax albipennis), in which a previously proposed decision strategy involved both quality-dependent hesitancy and direct comparisons of nests by scouts. An alternative possible decision strategy is that scouting ants use a very simple quality-dependent threshold rule to decide whether to recruit nest-mates to a new site or search for alternatives. We use analytical and simulation modelling to demonstrate that this simple rule is sufficient to explain empirical patterns from three studies of collective decision-making in ants, and can account parsimoniously for apparent comparison by individuals and apparent hesitancy (recruitment latency) effects, when available nests differ strongly in quality. This highlights the need to carefully design experiments to detect individual comparison. We present empirical data strongly suggesting that best-of-n comparison is not used by individual ants, although individual sequential comparisons are not ruled out. However, by using a simple threshold rule, decision-making groups are able to effectively compare options, without relying on any form of direct comparison of alternatives by individuals. This parsimonious mechanism could promote collective rationality in group decision-making.

Physiology as a caste-defining feature

Abstract.Division of labour is a key factor in the ecological success of social insects. Groups of individuals specializing on a particular behaviour are known as castes and are usually distinguished by morphology or age. Physiology plays a key role in both these types of caste, in either the developmental physiology which determines morphology, or the temporal changes in physiology over an insect’s life. Physiological correlates of morphological or temporal caste include differences in gland structure, secretory products, leanness, neuroanatomy and neurochemistry. However, purely physiological castes could also occur. Physiological castes are discrete groups of same-age same-size individuals with particular physiological competencies, or groups of individuals with similar physiology crossing age or size groups. A stable physiological caste occurs in the monomorphic Pharaoh’s ant, where some ants can detect old pheromone trails and retain this specialization over time. These ants differ physiologically from other workers, and the differences arise before eclosion. More temporary physiological castes occur in the ant Ectatomma where brood care specialists have more developed ovarioles than other same-aged workers, and in the honeybee where nurses, wax-workers and soldiers all differ physiologically from same-aged nestmates. Physiology is an important aspect of caste, not only in its contribution to age-related and morphological castes, but also in its own right as a caste grouping factor. While age and morphological differences make caste structures accessible for study, more cryptic physiological castes may play just as important a role in division of labour.

An agent-based model to investigate the roles of attractive and repellent pheromones in ant decision making during foraging

Pharaohs ants organise their foraging system using three types of trail pheromone. All previous foraging models based on specific ant foraging systems have assumed that only a single attractive pheromone is used. Here we present an agent-based model based on trail choice at a trail bifurcation within the foraging trail network of a Pharaohs ant colony which includes both attractive (positive) and repellent (negative) trail pheromones. Experiments have previously shown that Pharaohs ants use both types of pheromone. We investigate how the repellent pheromone affects trail choice and foraging success in our simulated foraging system. We find that both the repellent and attractive pheromones have a role in trail choice, and that the repellent pheromone prevents random fluctuations which could otherwise lead to a positive feedback loop causing the colony to concentrate its foraging on the unrewarding trail. An emergent feature of the model is a high level of variability in the level of repellent pheromone on the unrewarding branch. This is caused by the repellent pheromone exerting negative feedback on its own deposition. We also investigate the dynamic situation where the location of the food is changed after foraging trails are established. We find that the repellent pheromone has a key role in enabling the colony to refocus the foraging effort to the new location. Our results show that having a repellent pheromone is adaptive, as it increases the robustness and flexibility of the colonys overall foraging response.

Can ant colonies choose a far-and-away better nest over an in-the-way poor one?

Nest choice in the ant Temnothorax albipennis is a model system for investigating collective decision making. Previous research has demonstrated the sophistication of this decentralized system, yet such studies have focused on binary choices in which alternative nest sites are equidistant from the colonys original nest. In nature, for example, a poor nest might be closer than a better one. Hence, to investigate the collective decision-making system of these ants further, we challenged colonies with a choice between a distant high-quality nest and a much closer and collinear poorer one. Colonies successfully emigrated to the better nest when it was two, three or even nine times further away than the collinear poorer one. Most often, colonies started emigrating simultaneously to both nests, and then they redirected all traffic exclusively to the better, more distant one. We show that this is a good strategy for minimizing exposure and risk. In principle these ants might compensate for distance effects by increasing recruitment latencies and quorum thresholds at nearby poor nests so that they are better able to find and use distant better ones. However, the simplest explanation is that scouts are more likely to begin to look elsewhere, at all stages of the decision-making and emigration process, whenever and wherever they have initially found a low-quality nest.

Experience, corpulence and decision making in ant foraging

SUMMARY Social groups are structured by the decisions of their members. Social insects typically divide labour: some decide to stay in the nest while others forage for the colony. Two sources of information individuals may use when deciding whether to forage are their own experience of recent task performance and their own physiology, e.g. fat reserves (corpulence). The former is primarily personal information; the latter may give an indication of the food reserves of the whole colony. These factors are hard to separate because typically leaner individuals are also more experienced foragers. We designed an experiment to determine whether foraging specialisation is physiological or experience based (or both). We invented a system of automatic doors controlled by radio-tag information to manipulate task access and decouple these two sources of information. Our results show that when information from corpulence and recent experience conflict, ants behave only in accordance with their corpulence. However, among ants physiologically inclined to forage (less corpulent ants), recent experience of success positively influenced their propensity to forage again. Hence, foraging is organised via long-term physiological differences among individuals resulting in a relatively stable response threshold distribution, with fine-tuning provided by short-term learning processes. Through these simple rules, colonies can organise their foraging effort both robustly and flexibly.