Division of labor and brain evolution in insect societies: Neurobiology of extreme specialization in the turtle ant Cephalotes varians

Abstract

Strongly polyphenic social insects provide excellent models to examine the neurobiological basis of division of labor. Turtle ants, Cephalotes varians, have distinct minor worker, soldier, and reproductive (gyne/queen) morphologies associated with their behavioral profiles: small-bodied task-generalist minors lack the phragmotic shield-shaped heads of soldiers, which are specialized to block and guard the nest entrance. Gynes found new colonies and during early stages of colony growth overlap behaviorally with soldiers. Here we describe patterns of brain structure and synaptic organization associated with division of labor in C. varians minor workers, soldiers, and gynes. We quantified brain volumes, determined scaling relationships among brain regions, and quantified the density and size of microglomeruli, synaptic complexes in the mushroom body calyxes important to higher-order processing abilities that may underpin behavioral performance. We found that brain volume was significantly larger in gynes; minor workers and soldiers had similar brain sizes. Consistent with their larger behavioral repertoire, minors had disproportionately larger mushroom bodies than soldiers and gynes. Soldiers and gynes had larger optic lobes, which may be important for flight and navigation in gynes, but serve different functions in soldiers. Microglomeruli were larger and less dense in minor workers; soldiers and gynes did not differ. Correspondence in brain structure despite differences in soldiers and gyne behavior may reflect developmental integration, suggesting that neurobiological metrics not only advance our understanding of brain evolution in social insects, but may also help resolve questions of the origin of novel castes.

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

“…Cognitive investment within highly cooperative social groups can be distributed across individuals [1], and the question of how differences in brain investment among heterogeneous individuals within social groups relates to adaptive group function is a popular area of study [2][3][4]. Eusocial insect colonies often have pronounced task and/or morphological differentiation among colony members [5], making them excellent models for studying the effects of behavioral heterogeneity on the interplay between individual neural investment and socially coordinated function.…”

Active Inferants: An Active Inference Framework for Ant Colony Behavior

“…Only foragers were included in this model, future derivations could include worker developmental trajectories and colony-level task allocation processes (Friedman et al, 2020a ; Hayakawa et al, 2020 ). Nestmate-level behavioral heuristics are important for colony efficiency (Gordon et al, 2019 ; Kamhi et al, 2019 ; Arganda et al, 2020 ), as are truly colony-level processes (e.g., dynamic interaction patterns and nest architectures (Gordon, 2010 ; Pinter-Wollman et al, 2018 ; Lemanski et al, 2019 ) are in tight feedback with nestmate-level development and task allocation. Our model could be extended to study the role of these processes in the evolution of colony behavior, since the proposed simulation involved only agent-environment stigmergic interaction.…”

Brain Size, Metabolism, and Social Evolution

“…Limitations of volumetric correlations have been noted (Healy and Rowe, 2007 ; Logan et al, 2018 ). Studies of the structure and number of cells, synapses, and circuits may provide important neuroethological detail (Godfrey and Gronenberg, 2019 ), although comparative studies of individual neurons (Giraldo et al, 2013 ) and synaptic processing capability (Falibene et al, 2015 ; Gordon and Traniello, 2018 ; Gordon et al, 2019 ; Groh and Rössler, 2020 ) vary in degree of linkage with behavior. Volume (or mass) data are indeed required to understand scaling of cellular metrics such as synaptic density (Yilmaz et al, 2016 ) or neuromodulator titer, and can provide insight into sex-specific brain differentiation (Kiesow et al, 2020 ) and regional investment associated with social network size (Noonan et al, 2018 ).…”

“…Metabolic scaling should be considered for whole brains, functionally specialized brain compartments, workers, and colonies. Compartmental allometries can reflect variation in cognitive demands associated with division of labor (Muscedere and Traniello, 2012 ; Gordon et al, 2017 , 2019 ), but the energy needs of brain compartments associated with task specialization are unknown. Hypometric metabolic scaling at the colony level has been demonstrated: workers in larger colonies with lower mass-specific metabolic rates may perform tasks that have lower costs (Shik, 2010 ; Fewell and Harrison, 2016 ; Waters et al, 2017 ).…”