Cumulative Effects of Foraging Behavior and Social Dominance on Brain Development in a Facultatively Social Bee <b><i>(Ceratina australensis)</i></b>

Abstract

In social insects, both task performance (foraging) and dominance are associated with increased brain investment, particularly in the mushroom bodies. Whether and how these factors interact is unknown. Here we present data on a system where task performance and social behavior can be analyzed simultaneously: the small carpenter bee Ceratina australensis. We show that foraging and dominance have separate and combined cumulative effects on mushroom body calyx investment. Female C. australensis nest solitarily and socially in the same populations at the same time. Social colonies comprise two sisters: the social primary, which monopolizes foraging and reproduction, and the social secondary, which is neither a forager nor reproductive but rather remains at the nest as a guard. We compare the brains of solitary females that forage and reproduce but do not engage in social interactions with those of social individuals while controlling for age, reproductive status, and foraging experience. Mushroom body calyx volume was positively correlated with wing wear, a proxy for foraging experience. We also found that, although total brain volume did not vary among reproductive strategies (solitary vs. social nesters), socially dominant primaries had larger mushroom body calyx volumes (corrected for both brain and body size variation) than solitary females; socially subordinate secondaries (that are neither dominant nor foragers) had the least-developed mushroom body calyces. These data demonstrate that sociality itself does not explain mushroom body volume; however, achieving and maintaining dominance status in a group was associated with mushroom body calyx enlargement. Dominance and foraging effects were cumulative; dominant social primary foragers had larger mushroom body volumes than solitary foragers, and solitary foragers had larger mushroom body volumes than nonforaging social secondary guards. This is the first evidence for cumulative effects on brain development by dominance and task performance.

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

“…Thus, workers may have smaller MBs as a result of maternal manipulation of nutrition and/or behavioral aggression. As mentioned above, Rehan et al () showed that subordinate foragers had smaller MBs than solitary nest foundresses; other studies did not distinguish between queens enlarging MBs through dominance versus reducing worker MBs through subordinance. Both the “enlarged dominant” and “reduced subordinate” hypotheses posit that these factors influence MB size in addition to the differences in ovarian development that result from queen dominance.…”

“…In social insects, patterns of MB development may reflect social roles (Amador‐Vargas et al , ; O'Donnell and Bulova, ; O'Donnell et al , ). In many primitively social insects, reproductives must establish dominance over subordinates and the queens or otherwise dominant individuals have larger MBs than workers or other subordinate individuals (Molina and O'Donnell, ; ; O'Donnell et al , ; ; Rehan et al , ). This is not the case in the honeybees and large‐colony ant species, where queens use chemical communication to control worker reproduction, and have smaller MBs than workers (Julian and Gronenberg, ; Ehmer and Gronenberg, ; Fahrbach, ).…”

“…Reproductive physiology may also underlie MB differences. In the bee Ceratina australensis and the paper wasp Polistes instabilis , ovary size correlates with MB volume (Molina and O'Donnell, ; Rehan et al , ). In honeybees, juvenile hormone (JH) affects MB development (Withers et al , ), and JH is associated with dominance and reproduction in primitively social insects (West‐Eberhard, ; Smith et al , ; Hamilton et al , ).…”

“…MBs may also show experience‐dependent plasticity, increasing in volume in response to complex tasks like foraging or other sensory stimuli (Withers et al , ; ; ; Gronenberg et al , ; Fahrbach et al , ; Farris et al , ; Kühn‐Bühlmann and Wehner, ; Ismail et al , ; Krofczik et al , ; Molina and O'Donnell, ; Seid and Wehner, ; Maleszka et al , ; Stieb et al , ; Jones et al , ; Amador‐Vargas et al , ; Rehan et al , ; Montgomery et al , ; Seid and Junge, ; van Dijk et al , ; Montgomery and Merrill, ). Because queens must find and establish a nest, as well as forage for the first brood, they likely have more cumulative sensory experience, and thus larger MBs than workers.…”

“…Paper wasps show a correlation between dominance status and MB size (O'Donnell et al , ; Molina and O'Donnell, ; ). In a study controlling for age, Rehan et al () showed that dominant females had larger MBs, and subordinate females smaller MBs, than solitary nest foundreses, although a study of same‐generation paper wasp nest co‐foundresses found no difference between dominants and subordinates (Ehmer et al , ). Lastly, just as queens are dominant, workers are subordinate and bullied by queen aggressive behaviors which leads to suppressed ovarian development and other physiological effects, including lower levels of JH (Smith et al , ; Hamilton et al , ).…”