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. We discuss the implications of such cognitive impairments for the recent observations of bees disappearing from their colonies as well as for social life in general.

The mushroom body (MB) is an area of the insect brain involved in learning, memory, and sensory integration. Here, we used the sweat bee Megalopta genalis (Halictidae) to test for differences between queens and workers in the volume of the MB calyces. We used confocal microscopy to measure the volume of the whole brain, MB calyces, optic lobes, and antennal lobes of queens and workers. Queens had larger brains, larger MB calyces, and a larger MB calyces:whole brain ratio than workers, suggesting an effect of social dominance in brain development. This could result from social interactions leading to smaller worker MBs, or larger queen MBs. It could also result from other factors, such as differences in age or sensory experience. To test these explanations, we next compared queens and workers to other groups. We compared newly emerged bees, bees reared in isolation for 10 days, bees initiating new observation nests, and bees initiating new natural nests collected from the field to queens and workers. Queens did not differ from these other groups. We suggest that the effects of queen dominance over workers, rather than differences in age, experience, or reproductive status, are responsible for the queen-worker differences we observed. Worker MB development may be affected by queen aggression directly and/or manipulation of larval nutrition, which is provisioned by the queen. We found no consistent differences in the size of antennal lobes or optic lobes associated with differences in age, experience, reproductive status, or social caste.

Being choosy can allow animals to find and identify the best resources or safest locations to rear offspring. Despite these benefits, individuals vary in the degree to which they are choosy. One explanation is that choosiness represents a costly form of offspring investment and is part of a suite of life history trade-offs. We examined trade-offs between choosiness and fecundity in the cabbage white butterfly, Pieris rapae. To test the prediction that choosiness is negatively correlated with fecundity, we presented female cabbage whites with an array of host plant leaves that varied in nutrient content and conspecific density. Butterflies preferentially laid eggs on leaves with higher nutrient content and fewer conspecific models. In addition, butterflies that were choosier with regard to plant nutrition also tended to be choosy in terms of conspecific density. Choosy females were less fecund, with fecundity measured as the sum of eggs laid over three days and remaining mature eggs in their abdomen. These results are consistent with the idea that life history trade-offs include investment in costly behavioural traits that require time and energy, such as choosiness or cognition.

Nutrition has been hypothesized as an important constraint on brain evolution. However, it is unclear whether the availability of specific nutrients or the difficulty of locating high-quality diets limits brain evolution, especially over long periods of time. We found that dietary nutrient content predicted brain size across 42 species of butterflies. Brain size, relative to body size, was associated with the sodium and nitrogen content of a species' diet. There was no evidence that host plant apparency (measured by plant height) was related to brain evolution. The timing of diet shifts across species varied from 3.5 to 90 million years ago, but nutritional constraints did not lessen over time as species adapted to a diet. Although nutrition was linked to overall brain volume, there was no evidence that nutrition was related to the relative size of individual brain regions. Laboratory rearing experiments confirmed the underlying assumption of most comparative studies that the majority of interspecific trait variation stems from genetically based differences across species rather than developmental plasticity. This study highlights a novel role of sodium and nitrogen in brain evolution, which is additionally interesting given current anthropogenic change in the availability of these nutrients.

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Social behavior has been predicted to select for increased neural investment (the social brain hypothesis) and also to select for decreased neural investment (the distributed cognition hypothesis). Here, we use two related bees, the social Augochlorella aurata (Smith) (Hymenoptera: Halictidae) and the related Augochlora pura (Say), which has lost social behavior, to test the contrasting predictions of these two hypotheses in these taxa. We measured the volumes of the mushroom body (MB) calyces, a brain area shown to be important for cognition in previous studies, as well as the optic lobes and antennal lobes. We compared females at the nest foundress stage when both species are solitary so that brain development would not be influenced by social interactions. We show that the loss of sociality was accompanied by a loss in relative neural investment in the MB calyces. This is consistent with the predictions of the social brain hypothesis. Ovary size did not correlate with MB calyx volume. This is the first study to demonstrate changes in mosaic brain evolution in response to the loss of sociality.

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