Date Published: March 27, 2019
Publisher: Public Library of Science
Author(s): Darcy Greer Gordon, Alejandra Zelaya, Ignacio Arganda-Carreras, Sara Arganda, James F. A. Traniello, Fabio S. Nascimento.
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.
Adaptive morphology and neuroarchitecture support specialized behavior in complex social systems [1–5]. In the eusocial Hymenoptera, females exhibit a primary reproductive division of labor into fertile (queen) and sterile (worker) castes that potentially have identical genomes . In most species, queens are morphologically and behaviorally adapted for dispersal by flight; dealate inseminated queens then transition from nest establishment and nursing behaviors during colony foundation to reproduction [7,8]. These state changes in behavior are associated with neurobiological changes in the brain [9,10]. Division of labor also concerns the differentiation of sterile workers into physical subcastes that show task specializations [11–18]. The brains of workers in different subcastes as well as those of queens and workers may be distinguished by the relative proportion of neuropil in functionally specialized brain regions that correlate with morphological and behavioral differentiation [19–23].
Contrary to our body-size based prediction, C. varians gyne brains were significantly larger than those of soldiers and minors, which did not differ. However, our predictions regarding brain substructure scaling across castes and subcastes were supported: minors invested proportionally more in MBs and gynes had absolutely and relatively larger OLs and CXs. Soldier brain structure appeared to be intermediate between that of minors and gynes. Although the three groups separated neuroanatomically in multivariate space, significant differences were found only when group identity was specified a priori in discriminate analysis, indicating greater overlap in brain structure between castes and subcastes, but differences in relative volumes of the OLs and MBs.