Behavioral Performance and Neural Systems Are Robust to Sensory Injury in Workers of the Ant Pheidole dentata

Abstract

Miniaturized nervous systems have been thought to limit behavioral ability, and animals with miniaturized brains may be less flexible when challenged by injuries resulting in sensory deficits that impact the development, maintenance, and plasticity of small-scale neural networks. We experimentally examined how injuries to sensory structures critical for olfactory ability affect behavioral performance in workers of the ant Pheidole dentata, which have minute brains (0.01 mm³) and primarily rely on the perception and processing of chemical signals and cues to direct their social behavior. We employed unilateral antennal denervation to decrease the olfactory perception ability of workers and quantified consequential neuroanatomical and behavioral performance effects. Postablation neuroanatomical metrics revealed a 25% reduction in the volume of the antennal lobe ipsilateral to the antennal lesion relative to the contralateral lobe, indicating atrophy of the input-deprived tissue. However, antennectomy did not affect the volumes of the mushroom body or its subcompartments or the number of mushroom body synaptic complexes (microglomeruli) in either brain hemisphere. Synapsin immunoreactivity, however, was significantly higher in the ipsilateral mushroom body calyces, which could reflect presynaptic potentiation and homeostatic compensation in higher-order olfactory regions. Despite tissue loss caused by antennal lesioning and resulting unilateral sensory deprivation, the ability of workers to perform behaviors that encompass the breadth of their task repertoire and meet demands for colony labor remained largely intact. The few behavioral deficits recorded were restricted to pheromone trail-following ability, a result that was expected due to the need for bilateral olfactory input to process spatial odor information. Our macroscopic and cellular neuroanatomical measurements and assessments of task performance demonstrate that the miniaturized brains of P. dentata workers and their sensorimotor functions are remarkably robust to injury-related size reduction and remain capable of generating behaviors required to respond appropriately to chemical social signals and effectively nurse immatures, as well as participate in coordinated foraging.

Carpenter ants use diverse antennae sampling strategies to track odor trails

“…7B). This is consistent with evidence from drosophila that show adaptation within days after amputation (Wosnitza, 2013;Isakov, 2016;Muijres, 2017), as well as recent studies on ants showing robust performance across a range of olfactory behaviors after unilateral antenna amputation (Waxman, 2017). This resulting behavioral change in antennae movement may partially explain how the single antenna ant is able to maintain a level of estimated odor information similar to what one antenna of a control ant receives despite greater deviation from the trail (Fig.…”

Peripheral sensory organs vary among ant workers but variation does not predict division of labor

“…Yet, in this same species, the peripheral nervous system is not associated with worker differences in responsiveness to alarm pheromone (Robinson, 1987). Though we do find variation in T. rugatulus sensory organs, our results are consistent with those of (Waxman et al, 2017), which suggest that sensory organ differences may not have significant effects on behavior and task allocation. Rather than variation in density, variation in the size of individual sensilla or differences across individual sensilla in the number of underlying sensory neurons might affect sensory sensitivity and therefore behavior.…”

“…Recent work in Pheidole ants, for example, demonstrates that unilateral antennal ablation (i.e. resulting in the loss of roughly half of their sensilla) does not prevent workers from carrying out most of their normal task repertoire (Waxman et al, 2017). In contrast, antennal removal has significant effects on behavior in Tetragonula bees (though this was not associated with sensilla number), and in honeybees the right antenna is both more enriched with olfactory sensilla and better at recalling olfactory memories than the left.…”

Nasonia Parasitic Wasps Escape from Haller's Rule by Diphasic, Partially Isometric Brain-Body Size Scaling and Selective Neuropil Adaptations

“…This structure receives input of the antennal and optic lobes in most hymenopteran species [Gronenberg, 2001]. Part of the reduction in relative calyx volume in smaller individuals may thus have resulted from a reduced input from the smaller optic lobe, although ants did not show a decrease in mushroom body volume after a decrease in the primary sensory neuropils [Waxman et al, 2017]. Vision-or olfaction-specific calyx subunits that are visible in honeybees (i.e., lip and collar) are, however, not distinguishable in N. vitripennis.…”