Olfactory Sensitivity Aligns with Caste Revealing Multipotential Minors and Specialized Soldier Majors in Camponotus floridanus Ants

Camponotus floridanus ant colonies are comprised of a single reproductive queen and thousands of sterile female offspring that consist of two morphologically distinct castes: smaller minors and larger majors. Minors perform most of the tasks within the colony, including brood care and food collection, whereas majors have fewer clear roles and have been hypothesized to act as a specialized solider caste associated with colony defense. The allocation of workers to these different tasks depends on the detection and processing of local information including pheromones and other chemical blends such as cuticular hydrocarbons. We examined the electrophysiological responses to general odorants, cuticular extracts, and a trail pheromone in adult minor and major C. floridanus workers, revealing that the repertoire of social behaviors is positively correlated with olfactory sensitivity. Minors in particular display primarily excitatory responses to olfactory stimuli, whereas major workers respond primarily with inhibitory signals. The notable exception to this paradigm is that both minors and majors display robust, dose-dependent excitatory responses to conspecific, non-nestmate cuticular extracts. Moreover, while both minors and majors actively aggress non-nestmate foes, majors display significantly enhanced capabilities to rapidly subdue and kill opponents. Overall, our data suggest that C. floridanus majors do indeed represent a physiologically and behaviorally specialized soldier caste and support a model in which caste-specific olfactory sensitivity plays an important role in task allocation and the regulation of social behavior in ant colonies. Significance StatementThe detection and odor coding of chemical cues are essential components of the collective behavior observed in eusocial ants. To better understand the interdependent relationship between olfactory sensitivity and the allocation of worker castes to the various tasks critical for the success of the colony, a series of behavioral assessments and an electrophysiological survey of the antennae comprising general odorants, cuticular extracts, and a trail pheromone were undertaken. These studies reveal the behavioral repertoire of minors and majors aligned with profound shifts in olfactory sensitivity and odor coding. Our data support the hypothesis that minors are multipotential workers with broad excitatory sensitivity, and majors are dedicated soldiers with a highly specialized olfactory system for the detection of non-nestmate foes.