Division of Labor in the Hyperdiverse Ant Genus Pheidole Is Associated with Distinct Subcaste- and Age-Related Patterns of Worker Brain Organization

Abstract

The evolutionary success of ants and other social insects is considered to be intrinsically linked to division of labor among workers. The role of the brains of individual ants in generating division of labor, however, is poorly understood, as is the degree to which interspecific variation in worker social phenotypes is underscored by functional neurobiological differentiation. Here we demonstrate that dimorphic minor and major workers of different ages from three ecotypical species of the hyperdiverse ant genus Pheidole have distinct patterns of neuropil size variation. Brain subregions involved in sensory input (optic and antennal lobes), sensory integration, learning and memory (mushroom bodies), and motor functions (central body and subesophageal ganglion) vary significantly in relative size, reflecting differential investment in neuropils that likely regulate subcaste- and age-correlated task performance. Worker groups differ in brain size and display patterns of altered isometric and allometric subregion scaling that affect brain architecture independently of brain size variation. In particular, mushroom body size was positively correlated with task plasticity in the context of both age- and subcaste-related polyethism, providing strong, novel support that greater investment in this neuropil increases behavioral flexibility. Our findings reveal striking levels of developmental plasticity and evolutionary flexibility in Pheidole worker neuroanatomy, supporting the hypothesis that mosaic alterations of brain composition contribute to adaptive colony structure and interspecific variation in social organization.

Lifespan behavioural and neural resilience in a social insect

“…The CC is being increasingly implicated in integrative functions as well as motor output [54], and maintenance of the OL neuropil with increasing age could be particularly important to extranidal task performance. Pheidole dentata have relatively small eyes and OLs [31] which could contribute to lower levels of redundancy in these circuits and hence greater importance for their protection. High variability in the proportion of apoptotic cells in the CC likely stems from the small number of cells that comprise this region, causing a small absolute change in the number of dying cells to more strongly influence this proportion.…”

“…Mean counts per calyx (lateral or medial) and means of both calyces were analysed with a oneway ANOVA. Counts were converted to MG per mm 3 using calyx neuropil measurements from Muscedere & Traniello [31].…”

“…Minor workers expand their task repertoires from eclosion to approximately three weeks of age [23] while their brains undergo synaptic remodelling [28] and serotonergic systems that influence behavioural development and task performance mature [25,[29][30][31]. How do workers age behaviourally, and do age-related and brainbased neuroanatomical and neurochemical changes occur that could negatively impact lifespan task performance?…”

Investment in higher order central processing regions is not constrained by brain size in social insects

“…Using as our proxy for brain size, the volume of brain neuropil less the volume of the measured structure or structures, which we term RB [33], bivariate relationships between the C, OL, AL and AL þ OL volume with brain size were found to be moderate to strong (r 2 range: 0.32-0.97), with log-log SMA slope point estimates ranging from 0.78 to 2.01 (electronic supplementary material, were not (although, in the latter two cases, these did not result in significant deviations from isometry for the combined volume of the AL þ OL).…”

“…Even less attention has been given to the scaling of the major primary sensory input neuropils-the antennal (AL) and optic lobes (OL)-which process olfactory and visual afferent information, respectively, and supply the mushroom body calyces (C) in hymenopterans. Understanding how these aspects of brain composition affect worker behaviour and division of labour has been a prominent goal of social insect research, and significant interspecific variation in brain composition associated with task performance has begun to be identified in ants [21,33,47,50] and wasps [51]. Absolute brain size was recently proposed to constrain the evolution of the organization of the functional module comprising the C, AL and OL in polistine wasps [49]; interspecific comparisons suggested that small-brained wasps have lower ratios of C volume to the combined volume of the AL þ OL (C/AO hereafter) owing to positive allometry between C and brain size and negative allometry between AL þ OL and brain size.…”