Evolutionary neurobiology of exceptionally polymorphic ants
Gordon, Darcy Greer
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In polymorphic social insects, morphologically differentiated workers (subcastes) are thought to increase ergonomic efficiency by performing specialized tasks, thus enhancing colony-level fitness consequences of division of labor. Worker behavioral performance is thus considered to be coupled with morphology through selection for division of labor as an adaptive response to environmental challenges. Selective forces shape neuroanatomy by acting on behavior, presumably enabled by brain size and circuitry. Morphologically and behaviorally differentiated worker phenotypes are therefore predicted to reflect neuroanatomical differentiation in patterns of brain investment, and cellular organization in the brain is predicted to evolve in association with social roles. The extent to which morphology, brain structure, and behavior are coupled in insect societies within and across reproductive castes and worker subcastes, however, is unclear. Ant species that show exceptional worker size variation offer excellent systems to examine the adaptive evolution of physical subcastes, task specialization, and the social brain. Species from two sister myrmicine ant genera, Pheidole and Cephalotes, that exhibit remarkable variation in worker size and apparent task specialization were used as models to test hypotheses concerning the integration of morphology, neuroanatomy, and behavior within and between castes and worker subcastes. Investigations of the basal Pheidole rhea suggest the ancestral social organization of this genus was characterized by minor workers and polymorphic soldiers that have diverged in morphology and brain scaling relationships, but overlap in behavioral repertoire, aspects of task performance, and synaptic organization. In both P. dentata and P. morrisi, which differ in morphological and neuroanatomical specialization of subcastes, patterns of synaptic organization were consistent with experience-related synaptic pruning in association with age-, subcaste-, and species-specific behavioral differences. Similar patterns indicative of synaptic remodeling were found in Cephalotes varians, an exemplar of morphological and behavioral specialization. C. varians also displayed brain scaling relationships consistent with caste and subcaste neuroecology, supporting the developmental origin of soldiers as queen-worker intermediates. Together, these studies suggest relationships between morphological, neuroanatomical, and behavioral traits, and the extent of their specialization, vary in unexpected ways within and across myrmicine ant taxa.