Soldier neural architecture is temporarily modality specialized but poorly predicted by repertoire size in the stingless bee Tetragonisca angustula

Abstract

Individual heterogeneity within societies provides opportunities to test hypotheses about adaptive neural investment in the context of group cooperation. Here, we explore neural investment in defense specialist soldiers of the eusocial stingless bee (Tetragonisca angustula) which are age subspecialized on distinct defense tasks and have an overall higher lifetime task repertoire than other sterile workers within the colony. Consistent with predicted behavioral demands, soldiers had higher relative visual (optic lobe) investment than nonsoldiers but only during the period when they were performing the most visually demanding defense task (hovering guarding). As soldiers aged into the less visually demanding task of standing guarding this difference disappeared. Neural investment was otherwise similar across all colony members. Despite having larger task repertoires, soldiers had similar absolute brain size and the smaller relative brain size compared to other workers, meaning that lifetime task repertoire size was a poor predictor of brain size. Both high behavioral specialization in stable environmental conditions and reassignment across task groups during a crisis occur in T. angustula. The differences in neurobiology we report here are consistent with these specialized but flexible defense strategies. This work broadens our understanding of how neurobiology mediates age and morphological task specialization in highly cooperative societies.

Differentiation of workers into soldiers is associated with a size reduction of higher-order brain centers in the neotropical termite Procornitermes araujoi

“…4 ). The MB is a higher-order brain neuropil responsible for multimodal processing and integration of sensory information, as well as for learning and memory 20 , 61 , 62 . In social insects, a large amount of literature shows that shifts in task allocation underlying division of labour are intimately associated with plasticity at the level of the MBs 17 , 18 , 20 , 21 , 23 .…”

“…The MB is a higher-order brain neuropil responsible for multimodal processing and integration of sensory information, as well as for learning and memory 20 , 61 , 62 . In social insects, a large amount of literature shows that shifts in task allocation underlying division of labour are intimately associated with plasticity at the level of the MBs 17 , 18 , 20 , 21 , 23 . For instance, workers of the ant Camponotus floridanus engaged in foraging show a greater investment in the MB than their nursing nestmates, while idle sisters have a significantly smaller MB than the former groups 63 .…”

“…For other social insects, behavioural specialisation clearly reflects on visual system phenotypes. For instance, hovering bees of Tetragonisca angustula are engaged in the recognition and interception of heterospecific bees, tasks relying mostly on vision, and a higher investment in the OL has been reported for these individuals 20 , 21 . In leafcutter ants, individuals that perform tasks inside the lightless galleries and outside of the nest also show different investments in the OL 26 .…”

“…Surprisingly, it is extremely scarce for one of the most speciose groups of social insects, the termites 28 , 29 . Overall, for protist-dependent termites (or also referred as to “lower termites”) and social hymenopterans, shifts in task performance are often associated with changes in the size of the mushroom bodies (MB), a brain region responsible for higher-order processing and integration of sensory information, as well as with learning and memory and decision making 17 , 18 , 20 , 21 , 23 , 28 , 29 . These findings generally indicate that a greater investment in the MB increases individual behavioural flexibility 23 , an essential feature of division of labour.…”