Magnitude-sensitive reaction times reveal non-linear time costs in multi-alternative decision-making.

Optimality analysis of value-based decisions in binary and multi-alternative choice settings predicts that reaction times should be sensitive only to differences in stimulus magnitudes, but not to overall absolute stimulus magnitude. Yet experimental work in the binary case has shown magnitude sensitive reaction times, and theory shows that this can be explained by switching from linear to multiplicative time costs, but also by nonlinear subjective utility. Thus disentangling explanations for observed magnitude sensitive reaction times is difficult. Here for the first time we extend the theoretical analysis of geometric time-discounting to ternary choices, and present novel experimental evidence for magnitude-sensitivity in such decisions, in both humans and slime moulds. We consider the optimal policies for all possible combinations of linear and geometric time costs, and linear and nonlinear utility; interestingly, geometric discounting emerges as the predominant explanation for magnitude sensitivity.

Steering self-organisation through confinement.

Self-organisation is the spontaneous emergence of spatio-temporal structures and patterns from the interaction of smaller individual units. Examples are found across many scales in very different systems and scientific disciplines, from physics, materials science and robotics to biology, geophysics and astronomy. Recent research has highlighted how self-organisation can be both mediated and controlled by confinement. Confinement is an action over a system that limits its units' translational and rotational degrees of freedom, thus also influencing the system's phase space probability density; it can function as either a catalyst or inhibitor of self-organisation. Confinement can then become a means to actively steer the emergence or suppression of collective phenomena in space and time. Here, to provide a common framework and perspective for future research, we examine the role of confinement in the self-organisation of soft-matter systems and identify overarching scientific challenges that need to be addressed to harness its full scientific and technological potential in soft matter and related fields. By drawing analogies with other disciplines, this framework will accelerate a common deeper understanding of self-organisation and trigger the development of innovative strategies to steer it using confinement, with impact on, e.g., the design of smarter materials, tissue engineering for biomedicine and in guiding active matter.

Learning in single cell organisms.

The survival of all species requires appropriate behavioral responses to environmental challenges. Learning is one of the key processes to acquire information about the environment and adapt to changing and uncertain conditions. Learning has long been acknowledged in animals from invertebrates to vertebrates but remains a subject of debate in non-animal systems such a plants and single cell organisms. In this review I will attempt to answer the following question: are single cell organisms capable of learning? I will first briefly discuss the concept of learning and argue that the ability to acquire and store information through learning is pervasive and may be found in single cell organisms. Second, by focusing on habituation, the simplest form of learning, I will review a series of experiments showing that single cell organisms such as slime molds and ciliates display habituation and follow most of the criteria adopted by neuroscientists to define habituation. Then I will discuss disputed evidence suggesting that single cell organisms might also undergo more sophisticated forms of learning such as associative learning. Finally, I will stress out that the challenge for the future is less about whether or not to single cell organisms fulfill the definition of learning established from extensive studies in animal systems and more about acknowledging and understanding the range of behavioral plasticity exhibited by such fascinating organisms.

Phenotypic variability predicts decision accuracy in unicellular organisms.

When deciding between different options, animals including humans face the dilemma that fast decisions tend to be erroneous, whereas accurate decisions tend to be relatively slow. Recently, it has been suggested that differences in the efficacy with which animals make a decision relate closely to individual behavioural differences. In this paper, we tested this hypothesis in a unique unicellular organism, the slime mould Physarum polycephalum. We first confirmed that slime moulds differed consistently in their exploratory behaviour from 'fast' to 'slow' explorers. Second, we showed that slow explorers made more accurate decisions than fast explorers. Third, we demonstrated that slime moulds integrated food cues in time and achieved higher accuracy when sampling time was longer. Lastly, we showed that in a competition context, fast explorers excelled when a single food source was offered, while slow explorers excelled when two food sources varying in quality were offered. Our results revealed that individual differences in accuracy were partly driven by differences in exploratory behaviour. These findings support the hypothesis that decision-making abilities are associated with behavioural types, even in unicellular organisms.

Self-organized traffic via priority rules in leaf-cutting ants.

Ants, termites and humans often form well-organized and highly efficient trails between different locations. Yet the microscopic traffic rules responsible for this organization and efficiency are not fully understood. In previous experimental studies with leaf-cutting ants (Atta colombica), a set of local priority rules were isolated and it was proposed that these rules govern the temporal and spatial organization of the traffic on the trails. Here we introduce a model based on these priority rules to investigate whether they are sufficient to produce traffic similar to that observed in the experiments on both a narrow and a wider trail. We establish that the model is able to reproduce key characteristics of the traffic on the trails. In particular, we show that the proposed priority rules induce de-synchronization into clusters of inbound and outbound ants on a narrow trail, and that priority-type dependent segregated traffic emerges on a wider trail. Due to the generic nature of the proposed priority rules we speculate that they may be used to model traffic organization in a variety of other ant species.

Symmetry breaking and inter-clonal behavioural variability in a slime mould.

Cells are dynamic systems capable of switching from isotropic growth to polarized growth even in the absence of any pre-existing external asymmetry. Here, we study this process of symmetry breaking in the acellular slime mould Physarum polycephalum. In these experiments, slime moulds could grow on two identical opposed sources of calcium. We highlighted a positive correlation between growth dynamic, level of symmetry breaking and calcium concentration. We identified three populations of slime moulds within our clonal lineage with similar symmetry breaking behaviours but different motility characteristics. These behavioural differences between slime moulds emerged in the absence of any environmental differences. Such behavioural plasticity could generate cellular diversity, which can be critical for survival.

Parsing the life-shortening effects of dietary protein: effects of individual amino acids.

High-protein diets shorten lifespan in many organisms. Is it because protein digestion is energetically costly or because the final products (the amino acids) are harmful? To answer this question while circumventing the life-history trade-off between reproduction and longevity, we fed sterile ant workers on diets based on whole proteins or free amino acids. We found that (i) free amino acids shortened lifespan even more than proteins; (ii) the higher the amino acid-to-carbohydrate ratio, the shorter ants lived and the lower their lipid reserves; (iii) for the same amino acid-to-carbohydrate ratio, ants eating free amino acids had more lipid reserves than those eating whole proteins; and (iv) on whole protein diets, ants seem to regulate food intake by prioritizing sugar, while on free amino acid diets, they seem to prioritize amino acids. To test the effect of the amino acid profile, we tested diets containing proportions of each amino acid that matched the ant's exome; surprisingly, longevity was unaffected by this change. We further tested diets with all amino acids under-represented except one, finding that methionine, serine, threonine and phenylalanine are especially harmful. All together, our results show certain amino acids are key elements behind the high-protein diet reduction in lifespan.

Direct transfer of learned behaviour via cell fusion in non-neural organisms.

Cell fusion is a fundamental phenomenon observed in all eukaryotes. Cells can exchange resources such as molecules or organelles during fusion. In this paper, we ask whether a cell can also transfer an adaptive response to a fusion partner. We addressed this question in the unicellular slime mould Physarum polycephalum, in which cell-cell fusion is extremely common. Slime moulds are capable of habituation, a simple form of learning, when repeatedly exposed to an innocuous repellent, despite lacking neurons and comprising only a single cell. In this paper, we present a set of experiments demonstrating that slime moulds habituated to a repellent can transfer this adaptive response by cell fusion to individuals that have never encountered the repellent. In addition, we show that a slime mould resulting from the fusion of a minority of habituated slime moulds and a majority of unhabituated ones still shows an adaptive response to the repellent. Finally, we further reveal that fusion must last a certain time to ensure an effective transfer of the behavioural adaptation between slime moulds. Our results provide strong experimental evidence that slime moulds exhibit transfer of learned behaviour during cell fusion and raise the possibility that similar phenomena may occur in other cell-cell fusion systems.

Habituation in non-neural organisms: evidence from slime moulds.

Learning, defined as a change in behaviour evoked by experience, has hitherto been investigated almost exclusively in multicellular neural organisms. Evidence for learning in non-neural multicellular organisms is scant, and only a few unequivocal reports of learning have been described in single-celled organisms. Here we demonstrate habituation, an unmistakable form of learning, in the non-neural organism Physarum polycephalum In our experiment, using chemotaxis as the behavioural output and quinine or caffeine as the stimulus, we showed that P. polycephalum learnt to ignore quinine or caffeine when the stimuli were repeated, but responded again when the stimulus was withheld for a certain time. Our results meet the principle criteria that have been used to demonstrate habituation: responsiveness decline and spontaneous recovery. To distinguish habituation from sensory adaptation or motor fatigue, we also show stimulus specificity. Our results point to the diversity of organisms lacking neurons, which likely display a hitherto unrecognized capacity for learning, and suggest that slime moulds may be an ideal model system in which to investigate fundamental mechanisms underlying learning processes. Besides, documenting learning in non-neural organisms such as slime moulds is centrally important to a comprehensive, phylogenetic understanding of when and where in the tree of life the earliest manifestations of learning evolved.

Drosophila females trade off good nutrition with high-quality oviposition sites when choosing foods.

Animals, from insects to humans, select foods to regulate their acquisition of key nutrients in amounts and balances that maximise fitness. In species in which the nutrition of juveniles depends on parents, adults must make challenging foraging decisions that simultaneously address their own nutrient needs as well as those of their progeny. Here, we examined how the fruit fly Drosophila melanogaster, a species in which individuals eat and lay eggs in decaying fruits, integrate feeding decisions (individual nutrition) and oviposition decisions (offspring nutrition) when foraging. Using cafeteria assays with artificial diets varying in concentrations and ratios of protein to carbohydrates, we show that D. melanogaster females exhibit complex foraging patterns, alternating between laying eggs on high carbohydrate foods and feeding on foods with different nutrient contents depending on their own nutritional state. Although larvae showed faster development on high protein foods, both survival and learning performance were higher on balanced foods. We suggest that the apparent mismatch between the oviposition preference of females for high carbohydrate foods and the high performances of larvae on balanced foods reflects a natural situation where high carbohydrate ripened fruits gradually enrich in proteinaceous yeast as they start rotting, thereby yielding optimal nutrition for the developing larvae. Our findings that animals with rudimentary parental care uncouple feeding and egg-laying decisions in order to balance their own diet and provide a nutritionally optimal environment to their progeny reveal unsuspected levels of complexity in the nutritional ecology of parent-offspring interactions.

Resistance to nutritional stress in ants: when being fat is advantageous.

In ants, nutrient acquisition for the whole colony relies on a minority of workers, the foragers, which are often old and lean. Some studies have shown that the link between age, physiology and foraging activity is more flexible than once thought, especially in response to colony or environmental perturbations. This great plasticity offers the intriguing possibility to disentangle the effect of age, behaviour and physiology on the ants' abilities to cope with nutritional stresses. In this paper, we first looked at the capacity of groups of foragers and inner-nest workers to resist starvation and macronutrient imbalance. Second, we investigated whether behavioural task reversion modified the tolerance to nutritional stresses and by extension, changed mortality rate. We found that inner-nest workers live longer than foragers under nutritional stresses but not under optimal conditions. The reversion from foraging to inner-nest activities is followed by an increase in fat content and longevity. Finally, we demonstrated that changes in fat content associated with behavioural transition are highly flexible and strongly correlated to tolerance of nutritional stress. Our results have considerable implications for our understanding of the population dynamics of social insects under adverse nutritional conditions.

Phenotypic variability in unicellular organisms: from calcium signalling to social behaviour.

Historically, research has focused on the mean and often neglected the variance. However, variability in nature is observable at all scales: among cells within an individual, among individuals within a population and among populations within a species. A fundamental quest in biology now is to find the mechanisms that underlie variability. Here, we investigated behavioural variability in a unique unicellular organism, Physarum polycephalum. We combined experiments and models to show that variability in cell signalling contributes to major differences in behaviour underpinning some aspects of social interactions. First, following thousands of cells under various contexts, we identified distinct behavioural phenotypes: 'slow-regular-social', 'fast-regular-social' and 'fast-irregular-asocial'. Second, coupling chemical analysis and behavioural assays we found that calcium signalling is responsible for these behavioural phenotypes. Finally, we show that differences in signalling and behaviour led to alternative social strategies. Our results have considerable implications for our understanding of the emergence of variability in living organisms.

Symmetry restoring bifurcation in collective decision-making.

How social groups and organisms decide between alternative feeding sites or shelters has been extensively studied both experimentally and theoretically. One key result is the existence of a symmetry-breaking bifurcation at a critical system size, where there is a switch from evenly distributed exploitation of all options to a focussed exploitation of just one. Here we present a decision-making model in which symmetry-breaking is followed by a symmetry restoring bifurcation, whereby very large systems return to an even distribution of exploitation amongst options. The model assumes local positive feedback, coupled with a negative feedback regulating the flow toward the feeding sites. We show that the model is consistent with three different strains of the slime mold Physarum polycephalum, choosing between two feeding sites. We argue that this combination of feedbacks could allow collective foraging organisms to react flexibly in a dynamic environment.

Slime mold uses an externalized spatial "memory" to navigate in complex environments.

Spatial memory enhances an organism's navigational ability. Memory typically resides within the brain, but what if an organism has no brain? We show that the brainless slime mold Physarum polycephalum constructs a form of spatial memory by avoiding areas it has previously explored. This mechanism allows the slime mold to solve the U-shaped trap problem--a classic test of autonomous navigational ability commonly used in robotics--requiring the slime mold to reach a chemoattractive goal behind a U-shaped barrier. Drawn into the trap, the organism must rely on other methods than gradient-following to escape and reach the goal. Our data show that spatial memory enhances the organism's ability to navigate in complex environments. We provide a unique demonstration of a spatial memory system in a nonneuronal organism, supporting the theory that an externalized spatial memory may be the functional precursor to the internal memory of higher organisms.

Fungal infection alters collective nutritional intake of ant colonies.

In animals, parasitic infections impose significant fitness costs.1,2,3,4,5,6 Infected animals can alter their feeding behavior to resist infection,7,8,9,10,11,12 but parasites can manipulate animal foraging behavior to their own benefits.13,14,15,16 How nutrition influences host-parasite interactions is not well understood, as studies have mainly focused on the host and less on the parasite.9,12,17,18,19,20,21,22,23 We used the nutritional geometry framework24 to investigate the role of amino acids (AA) and carbohydrates (C) in a host-parasite system: the Argentine ant, Linepithema humile, and the entomopathogenic fungus, Metarhizium brunneum. First, using 18 diets varying in AA:C composition, we established that the fungus performed best on the high-amino-acid diet 1:4. Second, we found that the fungus reached this optimal diet when given various diet pairings, revealing its ability to cope with nutritional challenges. Third, we showed that the optimal fungal diet reduced the lifespan of healthy ants when compared with a high-carbohydrate diet but had no effect on infected ants. Fourth, we revealed that infected ant colonies, given a choice between the optimal fungal diet and a high-carbohydrate diet, chose the optimal fungal diet, whereas healthy colonies avoided it. Lastly, by disentangling fungal infection from host immune response, we demonstrated that infected ants foraged on the optimal fungal diet in response to immune activation and not as a result of parasite manipulation. Therefore, we revealed that infected ant colonies chose a diet that is costly for survival in the long term but beneficial in the short term-a form of collective self-medication.

Amoeboid organism solves complex nutritional challenges.

A fundamental question in nutritional biology is how distributed systems maintain an optimal supply of multiple nutrients essential for life and reproduction. In the case of animals, the nutritional requirements of the cells within the body are coordinated by the brain in neural and chemical dialogue with sensory systems and peripheral organs. At the level of an insect society, the requirements for the entire colony are met by the foraging efforts of a minority of workers responding to cues emanating from the brood. Both examples involve components specialized to deal with nutrient supply and demand (brains and peripheral organs, foragers and brood). However, some of the most species-rich, largest, and ecologically significant heterotrophic organisms on earth, such as the vast mycelial networks of fungi, comprise distributed networks without specialized centers: How do these organisms coordinate the search for multiple nutrients? We address this question in the acellular slime mold Physarum polycephalum and show that this extraordinary organism can make complex nutritional decisions, despite lacking a coordination center and comprising only a single vast multinucleate cell. We show that a single slime mold is able to grow to contact patches of different nutrient quality in the precise proportions necessary to compose an optimal diet. That such organisms have the capacity to maintain the balance of carbon- and nitrogen-based nutrients by selective foraging has considerable implications not only for our understanding of nutrient balancing in distributed systems but for the functional ecology of soils, nutrient cycling, and carbon sequestration.

Characterization of chitinases from the GH18 gene family in the myxomycete Physarum polycephalum.

BACKGROUND: Physarum polycephalum is an unusual macroscopic myxomycete expressing a large range of glycosyl hydrolases. Among them, enzymes from the GH18 family can hydrolyze chitin, an important structural component of the cell walls in fungi and in the exoskeleton of insects and crustaceans. METHODS: Low stringency sequence signature search in transcriptomes was used to identify GH18 sequences related to chitinases. Identified sequences were expressed in E. coli and corresponding structures modelled. Synthetic substrates and in some cases colloidal chitin were used to characterize activities. RESULTS: Catalytically functional hits were sorted and their predicted structures compared. All share the TIM barrel structure of the GH18 chitinase catalytic domain, optionally fused to binding motifs, such as CBM50, CBM18, and CBM14, involved in sugar recognition. Assessment of the enzymatic activities following deletion of the C-terminal CBM14 domain of the most active clone evidenced a significant contribution of this extension to the chitinase activity. A classification based on module organization, functional and structural criteria of characterized enzymes was proposed. CONCLUSIONS: Physarum polycephalum sequences encompassing a chitinase like GH18 signature share a modular structure involving a structurally conserved catalytic TIM barrels decorated or not by a chitin insertion domain and optionally surrounded by additional sugar binding domains. One of them plays a clear role in enhancing activities toward natural chitin. GENERAL SIGNIFICANCE: Myxomycete enzymes are currently poorly characterized and constitute a potential source for new catalysts. Among them glycosyl hydrolases have a strong potential for valorization of industrial waste as well as in therapeutic field.

Effect of queen number on colony-level nutrient regulation, food collection and performance in two polygynous ant species.

There is growing appreciation for how social interactions influence animal foraging behavior, especially with respect to key nutrients. Ants, given their eusocial nature and ability to be reared and manipulated in the laboratory, offer unique opportunities to explore how social interactions influence nutrient regulation and related processes. At the colony-level, ants simultaneously regulate their protein and carbohydrate intake; a regulation tied to the presence of larvae. However, even though 45% of the approximately 10,000 ant species are polygynous, we know little about the influence of queen number on colony-level foraging behavior and performance. Here we explored the direct effects of queen number on colony-level protein-carbohydrate regulation, food collection, survival, and brood production in two polygynous ant species (Nylanderia fulva and Solenopsis invicta). For both species we conducted choice and no-choice experiments using small experimental colonoids (20 workers) with 0, 1, or 2 queens. Both species regulated their relative intake of protein and carbohydrate around a P1:C2 mark. However, only N. fulva responded to the addition of queens, increasing overall food collection, biasing intake towards carbohydrates, and over-collecting imbalanced foods. N. fulva also exhibited reduced survival and reproduction on protein-biased foods. In contrast, S. invicta showed no response to queen number and reduced food collection on the protein-biased diet while maintaining high survival and reproduction. Our results demonstrate the potential for queens of some ant species to impact colony-level foraging and performance, with interspecific variation likely being shaped by differences in life history traits.

Audrey Dussutour.

Interview with Audrey Dussutour, who uses slime molds and ant colonies to study collective behavior and cognition at the Center for Integrative Biology in Toulouse.

Substrate and cell fusion influence on slime mold network dynamics.

The acellular slime mold Physarum polycephalum provides an excellent model to study network formation, as its network is remodelled constantly in response to mass gain/loss and environmental conditions. How slime molds networks are built and fuse to allow for efficient exploration and adaptation to environmental conditions is still not fully understood. Here, we characterize the network organization of slime molds exploring homogeneous neutral, nutritive and adverse environments. We developed a fully automated image analysis method to extract the network topology and followed the slime molds before and after fusion. Our results show that: (1) slime molds build sparse networks with thin veins in a neutral environment and more compact networks with thicker veins in a nutritive or adverse environment; (2) slime molds construct long, efficient and resilient networks in neutral and adverse environments, whereas in nutritive environments, they build shorter and more centralized networks; and (3) slime molds fuse rapidly and establish multiple connections with their clone-mates in a neutral environment, whereas they display a late fusion with fewer connections in an adverse environment. Our study demonstrates that slime mold networks evolve continuously via pruning and reinforcement, adapting to different environmental conditions.