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.
Highlights
Comparing neuroanatomical variation among individuals within and between invertebrate and vertebrate species has proven fruitful for exploring links between brain, behavior, ecology, life history and evolution [1]
Differences in brain size and divergent patterns of brain subregion scaling among Pheidole workers result in size, age, and speciesspecific patterns of investment in functional neuropil regions, reflecting the preeminent colony-wide division of labor and interspecific sociobiological variation characteristic of this speciesrich genus
Patterns of division of labor in Pheidole are associated with brain composition, the relative sizes of olfactory input (AL) and sensory processing (MB) regions
Summary
Comparing neuroanatomical variation among individuals within and between invertebrate and vertebrate species has proven fruitful for exploring links between brain, behavior, ecology, life history and evolution [1]. In Pheidole dentata, minor workers undergo behavioral maturation during the first few weeks of adult life by adding outside-nest tasks such as foraging to their existing within-nest activities [26]. During this maturational period, P. dentata minors become more efficient at some tasks [27] and their cephalic musculature concurrently matures [28]. There is considerable variation among the ca. 1,100 Pheidole species in colony size, nesting ecology, diet, body size, subcaste investment, and in behavioral traits such as foraging mode, worker aggressiveness, and the breadth and plasticity of major worker behavior [25,32,33]
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