The Loss of Sociality Is Accompanied by Reduced Neural Investment in Mushroom Body Volume in the Sweat Bee Augochlora Pura (Hymenoptera: Halictidae).

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.

Brain differences between social castes precede group formation in a primitively eusocial bee.

Social interactions may shape brain development. In primitively eusocial insects, the mushroom body (MB), an area of the brain associated with sensory integration and learning, is larger in queens than in workers. This may reflect a strategy of neural investment in queens or it may be a plastic response to social interactions in the nest. Here, we show that nest foundresses-the reproductive females who will become queens but are solitary until their first workers are born-have larger MBs than workers in the primitively eusocial sweat bee Augochlorella aurata. Whole brain size and optic lobe size do not differ between the two groups, but foundresses also have larger antennal lobes than workers. This shows that increased neural investment in MBs precedes social group formation. Larger MBs among foundresses may reflect the increased larval nutrition provisioned to future queens and the lack of social aggression from a dominant queen upon adult emergence.

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. 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.

Reduced neural investment in post-reproductive females of the bee Ceratina calcarta.

Many insects show plasticity in the area of the brain called the mushroom bodies (MB) with foraging and social experience. MBs are paired neuropils associated with learning and memory. MB volume is typically greater in mature foragers relative to young and/or inexperienced individuals. Long-term studies show that extended experience may further increase MB volume, but long-term studies have only been performed on non-reproductive social insect workers. Here we use the subsocial bee Ceratina calcarata to test the effect of extended foraging experience on MB volume among reproductive females. Ceratina calcarata females forage to provision their immature offspring in the spring, and then again to provision their adult daughters in the late summer. We measured the volume of the MB calyces and peduncle, antennal lobes (AL), optic lobes (OL), central complex (CX), and whole brains of three groups of bees: newly emerged females, reproductive females in spring (foundresses), and post-reproductive mothers feeding their adult daughters in late summer. Post-reproductive late summer mothers had smaller MB calyces and ALs than foundresses. Moreover, among late mothers (but not other bees), wing wear, which is a measure of foraging experience, negatively correlated with both MB and OL volume. This is contrary to previously studied non-reproductive social insect workers in which foraging experience correlates postiviely with MB volume, and suggests that post-reproductive bees may reduce neural investment near the end of their lives.

Nutritional constraints on brain evolution: Sodium and nitrogen limit brain size.

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.

Queen Dominance May Reduce Worker Mushroom Body Size in a Social Bee.

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.

Butterflies Do Not Alter Conspecific Avoidance in Response to Variation in Density.

SYNOPSIS: High conspecific densities are associated with increased levels of intraspecific competition and a variety of negative effects on performance. However, changes in life history strategy could compensate for some of these effects. For instance, females in crowded conditions often have fewer total offspring, but they may invest more in each one. Such investment could include the production of larger offspring, more time spent engaging in parental care, or more choosy decisions about where offspring are placed. For animals that have a relatively immobile juvenile stage, the costs of competition can be particularly high. Females may be able to avoid such costs by investing more in individual reproductive decisions, rearing young or laying eggs in locations away from other females. We tested the hypothesis that conspecific density cues during juvenile and adult life stages lead to changes in life history strategy, including both reproduction and oviposition choices. We predicted that high-density cues during the larval and adult stages of female Pieris rapae butterflies lead to lower fecundity but higher conspecific avoidance during oviposition, compared to similar low-density cues. We used a 2×2 factorial design to examine the effects of low and high conspecific density during the larval and adult stages of butterflies on avoidance behavior and fecundity. We found that past information about conspecific density did not matter; all butterflies exhibited similar levels of fecundity and a low level of conspecific avoidance during oviposition regardless of their previous experience as larvae and adults. These results suggest that P. rapae females use a fixed, rather than flexible, conspecific avoidance strategy when making oviposition decisions, and past information about conspecific density has no effect on life history and current reproductive investment. We speculate that this may be partially because past conspecific density per se is not a reliable cue for predicting current density and levels of competition, and thus it does not affect the development of life history strategies in this system.