Edwards, N. D. | bioRxiv Science

bioRxiv2023

Age and Task Modulate Olfactory Sensitivity in the Florida Carpenter Ant Camponotus floridanus

Age-related changes in behavior and sensory perception have been observed in a wide variety of animal species. In ants and other eusocial insects, workers often progress through an ordered sequence of olfactory-driven behavioral tasks. Notably, these behaviors are plastic, and workers adapt and rapidly switch tasks in response to changing environmental conditions. In the Florida carpenter ant, smaller minors typically perform most of the work needed to maintain the colony while the larger majors are specialized for nest defense and rarely engage in these routine tasks. Here, we investigate the effects of age and task group on olfactory responses to a series of odorant blends in minor and major worker castes. Consistent with their respective roles within the colony, we observed significant age-associated shifts in the olfactory responses of minors as they transitioned between behavioral states, whereas the responses of majors remained consistently low regardless of age. Furthermore, we identified a unitary compound, 3-methylindole, which elicited significantly higher responses and behavioral aversion in minor nurses than in similarly aged foragers suggesting that this compound may play an important role in brood care. Taken together, our results suggest that age- and task-associated shifts in olfactory physiology may play a critical role in the social organization of ant colonies. Simple SummaryFlorida carpenter ants (Camponotus floridanus) live in colonies comprised of thousands of workers. The smallest workers, known as minors, engage in routine tasks such as nursing and foraging while the largest workers, known as majors, are thought to be soldiers specialized for defending the nest. How ant colonies allocate their workforce to address the dynamic and ever-changing needs of the colonies remains an open question in the field, but current evidence suggests that ant social behavior likely results from a combination of genetic/epigenetic, physiological, and systems-level processes. Here, we extend these studies by investigating the role of olfactory sensitivity in regulating ant behavior. Minor workers exhibited significant shifts in olfactory sensitivity and odor coding as they aged and switched tasks. The olfactory sensitivity of majors, however, remained relatively stable as they aged. From these studies, we also identified a single compound, 3-methylindole, which elicited significantly higher olfactory responses and aversive behavior in nurses compared to foragers, suggesting that this chemical may have a role in brood care. Overall, these studies support the hypothesis that changes in olfactory sensitivity play an important role in regulating social behavior in ants.

neuroscience↗

bioRxiv2022

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.

evolutionary biology↗