Brain energy metabolism as an underlying basis of slow and fast cognitive phenotypes in honeybees.

In the context of slow-fast behavioral variation, fast individuals are hypothesized to be those who prioritize speed over accuracy while slow individuals are those which do the opposite. Since energy metabolism is a critical component of neural and cognitive functioning, this predicts such differences in cognitive style to be reflected at the level of the brain. We tested this idea in honeybees by first classifying individuals into slow and fast cognitive phenotypes based on a learning assay and then measuring their brain respiration with high-resolution respirometry.

Metabolic scaling as an emergent outcome of variation in metabolic rate.

The allometric scaling of metabolic rate and what drives it are major questions in biology with a long history. Since the metabolic rate at any level of biological organization is an emergent property of its lower-level constituents, it is an outcome of the intrinsic heterogeneity among these units and the interactions among them. However, the influence of lower-level heterogeneity on system-level metabolic rate is difficult to investigate, given the tightly integrated body plan of unitary organisms.

Metabolic Rate Diversity Shapes Group Performance in Honeybees.

AbstractThe metabolic theory of ecology posits that the functional properties at any level of biological organization are a function of the metabolic rate (MR) of its constituent units, although we know little about how heterogeneity among them shapes group-level performance. Using honeybees as a model system, we leveraged the differences in MR associated with "slow" and "fast" malate dehydrogenase alleles to breed genetic lines with low MR and high MR, respectively, and created four experimental groups with different phenotypic compositions. We then measured MR, energetic intake, thermoregulation, and survival of these groups in low- and high-resource conditions.

Interindividual variation in the use of social information during learning in honeybees.

Slow-fast differences in cognition among individuals have been proposed to be an outcome of the speed-accuracy trade-off in decision-making. Based on the different costs associated with acquiring information via individual and social learning, we hypothesized that slow-fast cognitive differences would also be tied to the adoption of these different learning modes. Since foragers in honeybee colonies likely have both these information acquisition modes available to them, we chose to test them for interindividual differences in individual and social learning.

Nesting ecology does not explain slow-fast cognitive differences among honeybee species.

Slow-fast behavioral and life history differences have been tied to slow-fast variation in cognition that is part of the general speed-accuracy tradeoff. While there is growing evidence for such cognitive variation and its association with behavior and life history at the intraspecific level, it is unknown if a similar relationship extends to the interspecific level. Since interspecific differences in cognition have been shown to be a function of ecology and life history, such differences should be reflected in multiple traits that comprise the slow-fast cognitive axis.

Interindividual variation in learning ability in honeybees.

Performance on different cognitive tasks could either be positively correlated in an individual as a measure of general intelligence or costs related to specific aspects of cognition could give rise to specialized cognitive phenotypes. Social living offers the potential for individual specialization in learning and a cooperative group can benefit from a diversity of learning phenotypes. However, there is little empirical data regarding the nature of such interindividual variation in learning abilities in honeybees, a classic model of animal cognition.

Spare to share? How does interindividual variation in metabolic rate influence food sharing in the honeybee?

A central benefit of group living is the cooperative acquisition and sharing of resources but the costs associated with these processes can set up a potential conflict between individual and group level fitness. Within a honeybee colony, the task of resource acquisition is relegated to the foragers and any interindividual differences in their metabolic rate and the consequent carbohydrate demand may pose a constraint on the amount of resources they can contribute to the colony. We investigated whether the carbohydrate demand of a forager is a function of her metabolic rate and if this impacts the amount of food she shares with the nestmates.

Inter-individual variation in nutrient balancing in the honeybee (Apis mellifera).

The Geometric Framework approach in nutritional ecology postulates that animals attempt to balance the consumption of different nutrients rather than simply maximizing energetic gain. The intake target with respect to each nutrient maximizes fitness in a specific dimension and any difference between individuals in intake target therefore represents alternative behavioral and fitness maximization strategies. Nutritional interactions are a central component of all social groups and any inter-individual variation in intake target should therefore have a significant influence on social dynamics.

Starving honeybees lose self-control.

Impulsivity, the widespread preference for a smaller and more immediate reward over a larger and more delayed reward, is known to vary across species, and the metabolic and social hypotheses present contrasting explanations for this variation. However, this presents a paradox for an animal such as the honeybee, which is highly social, yet has a high metabolic rate. We test between these two competing hypotheses by investigating the effect of hunger on impulsivity in bees isolated from their social environment.

Infected honeybee foragers incur a higher loss in efficiency than in the rate of energetic gain.

Parasites, by altering the nutritional and energetic state of their hosts, can significantly alter their foraging behaviour. In honeybees, an infection with Nosema ceranae has been shown to lower the energetic state of individual bees, bringing about changes in behaviours associated with foraging. Comparing the foraging trip times, hive times in between trips, and the crop contents of uninfected and infected foragers as they depart on foraging trips and return from them, this study examined how any differences in these variables influence alternative foraging currencies.

Energetic cost of learning and memory can cause cognitive impairment in honeybees.

The energetic cost of cognitive functions can lead to either impairments in learning and memory, or to trade-offs with other functions, when the amount of available energy is limited. However, it has been suggested that, under such conditions, social groups such as honeybees might be able to ward off cognitive impairments in individual bees by adjusting resource allocation at the colony level. Using two complementary experiments, one that tests the effect of learning on subsequent energetic state and survival, and another that tests the effect of energetic state on learning and retention, we show that individual bees pay a significant energetic cost for learning and therefore suffer from significant cognitive deficits under energetic stress.

Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers.

Parasites by drawing nutrition from their hosts can exert an energetic stress on them. Honeybee foragers with their high metabolic demand due to flight are especially prone to such a stress when they are infected. We hypothesized that infection by the microsporidian gut parasite Nosema ceranae can lower the hemolymph sugar level of an individual forager and uncouple its energetic state from its normally tight correlation with the colony energetic state.

Behavioural fever in infected honeybees: parasitic manipulation or coincidental benefit?

Infection by a parasite often induces behavioural changes in the host and these changes may benefit either the host or the parasite. However, whether these changes are active host defence mechanisms or parasitic manipulations or simply incidental byproducts of the infection is not always clear. It has been suggested that understanding the proximate mechanisms of these changes as well as comparative studies could help distinguish these alternatives better.

Energetic stress in the honeybee Apis mellifera from Nosema ceranae infection.

Parasites are dependent on their hosts for energy to reproduce and can exert a significant nutritional stress on them. Energetic demand placed on the host is especially high in cases where the parasite-host complex is less co-evolved. The higher virulence of the newly discovered honeybee pathogen, Nosema ceranae, which causes a higher mortality in its new host Apis mellifera, might be based on a similar mechanism.

Receiver bias for exaggerated signals in honeybees and its implications for the evolution of floral displays.

Mechanistic models of animal signals posit the occurrence of biases on the part of receivers that could be potentially exploited by signallers. Such biases are most obvious when animals are confronted with exaggerated versions of signals they normally encounter. Signalling systems operating in plant-pollinator interactions are among the most highly coevolved, with plants using a variety of floral signals to attract pollinators.

Experimentally induced change in infectious period affects transmission dynamics in a social group.

A key component of any epidemiological model is the infectious period, which greatly affects the dynamics and persistence of an infection. Social organization, leading to behavioural and spatial heterogeneities among potential susceptibles, interacts with infectious period to create different risk categories within a group. Using the honeybee (Apis mellifera) colony as a social model, a protocol that creates different infectious periods in individual bees and another that follows the diffusion of a transmittable tracer within a colony, we show experimentally how a short infectious period results in an epidemic process with low prevalence confined only to individuals at the outer edge of a group, while a long infectious period results in high prevalence distributed more universally among all the group members.

Sampling and decision rules used by honey bees in a foraging arena.

Animals must continuously choose among various available options to exploit the most profitable resource. They also need to keep themselves updated about the values of all available options, since their relative values can change quickly due to depletion or exploitation by competitors. While the sampling and decision rules by which foragers profitably exploit a flower patch have attracted a great deal of attention in theory and experiments with bumble bees, similar rules for honey bee foragers, which face similar foraging challenges, are not as well studied.

The role of colony organization on pathogen transmission in social insects.

Social organisms are especially vulnerable to pathogens due to the homogeneity of the colony, and the close proximity and extensive interactions among its members. However, the social organization of these groups also offers the potential to provide an effective barrier against the transmission of pathogens within the colony. Social insects with their elaborate colony organizations provide an ideal model system to develop and test this hypothesis.