Audrey Dussutour

Ant workers die young and colonies collapse when fed a high-protein diet.

A key determinant of the relationship between diet and longevity is the balance of protein and carbohydrate in the diet. Eating excess protein relative to carbohydrate shortens lifespan in solitary insects. Here, we investigated the link between high-protein diet and longevity, both at the level of individual ants and colonies in black garden ants, Lasius niger. We explored how lifespan was affected by the dietary protein-to-carbohydrate ratio and the duration of exposure to a high-protein diet. We show that (i) restriction to high-protein, low-carbohydrate diets decreased worker lifespan by up to 10-fold; (ii) reduction in lifespan on such diets was mainly due to elevated intake of protein rather than lack of carbohydrate; and (iii) only one day of exposure to a high-protein diet had dire consequences for workers and the colony, reducing population size by more than 20 per cent.

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.

Key factors for the emergence of collective decision in invertebrates.

In many species of group living invertebrates, in particular arthropods, collective decisions can emerge from the combined actions of individuals and the direct or indirect interactions between individuals. These decisions allow groups of individuals to respond quickly and accurately to changes that occur in their environment. Examples of such decisions are found in a variety of invertebrate taxa and in many different contexts, e.g., exploring a new territory, foraging for food, finding a suitable location where to aggregate or to establish a nest, defending oneself against predators, etc. In this paper we review the collective decisions that have been documented in different invertebrate taxa where individuals are known to live temporarily or permanently in social or gregarious groups. We first present some simple examples of collective decisions involving the choice between two alternatives. We then define the fundamental rules required for these collective decisions to emerge throughout the invertebrate taxon, from simple organisms such as caterpillars, to animals endowed with highly developed perceptive and cognitive capacities such as ants and bees. The presentation of these rules gives us the opportunity to illustrate one of the pitfalls of the study of collective choice in animals by showing through computer simulations how a choice between two alternatives can be misinterpreted as the result of the action of self-organized mechanisms. In the second part, we discuss the peculiarities of collective decisions in invertebrates, their properties, and characteristics. We conclude by discussing the issue of individual complexity in collective decision-making process.

Influence of Epicuticular-Wax Composition on the Feeding Pattern of a Phytophagous Insect: Implications for Host Resistance

Abstract n A white spruce, Picea glauca (Moench) Voss (Pinaceae), plantation in southern Quebec was found to contain two distinct types of trees, the first resistant and the second susceptible to attack by spruce budworm, Choristoneura fumiferana (Clemens) (Lepidoptera: Tortricidae). To identify the mechanisms of white spruce resistance to spruce budworm, we studied the role of epicuticular waxes, comparing (i) the foliar chemistry of susceptible and resistant trees and (ii) the feeding pattern of larvae at first contact with the foliage. Needles collected from resistant trees contained concentrations of the monoterpenes &agr;-pinene and myrcene that were 307% and 476%, respectively, above those found in needles collected from susceptible trees. Although there were no significant differences in probing behaviour, significantly fewer larvae transitioned from probing to feeding on resistant needles; this led to fewer feeding bouts as well as a significantly shorter first meal. Removal of waxes increased the number of individuals transitioning from probing to feeding on resistant needles; this led to more feeding bouts. Our results demonstrate that monoterpenes influence the pattern of feeding of spruce budworm larvae as well as playing an important role in white spruce resistance.

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

ABSTRACT 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. Summary: Flies uncouple feeding and egg-laying decisions to balance their diet and provide a nutritionally optimal environment for their progeny, indicating a certain complexity in the nutritional ecology of parent–offspring interactions.

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.

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

ABSTRACT 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. Highlighted Article: More fat, live longer: positive association between fat content and lifespan in ants.

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.

Collective choice in ants: the role of protein and carbohydrates ratios.

In a foraging context, social insects make collective decisions from individuals responding to local information. When faced with foods varying in quality, ants are known to be able to select the best food source using pheromone trails. Until now, studies investigating collective decisions have focused on single nutrients, mostly carbohydrates. In the environment, the foods available are a complex mixture and are composed of various nutrients, available in different forms. In this paper, we explore the effect of protein to carbohydrate ratio on ants ability to detect and choose between foods with different protein characteristics (free amino acids or whole proteins). In a two-choice set up, Argentine ants Linepithema humile were presented with two artificial foods containing either whole protein or amino acids in two different dietary conditions: high protein food or high carbohydrate food. At the collective level, when ants were faced with high carbohydrate foods, they did not show a preference between free amino acids or whole proteins, while a preference for free amino acids emerged when choosing between high protein foods. At the individual level, the probability of feeding was higher for high carbohydrates food and for foods containing free amino acids. Two mathematical models were developed to evaluate the importance of feeding probability in collective food selection. A first model in which a forager deposits pheromone only after feeding, and a second model in which a forager always deposits pheromone, but with greater intensity after feeding. Both models were able to predict free amino acid selection, however the second one was better able to reproduce the experimental results suggesting that modulating trail strength according to feeding probability is likely the mechanism explaining amino acid preference at a collective level in Argentine ants.

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.