Serotonin modulates worker responsiveness to trail pheromone in the ant Pheidole dentata

Abstract

As social insect workers mature, outside-nest tasks associated with foraging and defense are typically performed at higher frequencies. Foraging in ants is often a pheromonally mediated collective action performed by mature workers; age-dependent differences in olfactory response thresholds may therefore proximately regulate task repertoire development. In the ant Pheidole dentata, foraging activity increases with chronological age in minor workers, and is chemically controlled. The onset of foraging in minor workers is accompanied by marked neuroanatomical and neurochemical changes, including synaptic remodeling in olfactory regions of the brain, proliferation of serotonergic neurons, and increased brain titers of monoamines, notably serotonin. We examined the linkage of serotonin and olfactory responsiveness by assaying trail-following performance in mature P. dentata minor workers with normal serotonin levels, or serotonin levels experimentally lowered by oral administration of the serotonin synthesis inhibitor α-methyltryptophan (AMTP). By assessing responsiveness to standardized pheromone trails, we demonstrate that trail-following behaviors are significantly reduced in serotonin-depleted workers. AMTP-treated individuals were less likely to initiate trail following, and oriented along pheromone trails for significantly shorter distances than untreated, similar-age workers. These results demonstrate for the first time that serotonin modulates olfactory processes and/or motor functions associated with cooperative foraging in ants.

Lifespan behavioural and neural resilience in a social insect

“…Nevertheless, the CC showed significantly lower levels of apoptosis than the RCB. Titres of 5HT-a neuromodulator significant for olfactory social functions in P. dentata [25]-and DA increased with age, rather than showing senescence-associated declines [37,55]. DA can have neurotrophic functions, and 5HT and DA may interact to promote circuit development and neuroplasticity [34] as well as modulate sensory [56,57] and motor function [58,59], perhaps contributing to the preservation of task performance in ageing workers.…”

“…(ii) Pheromone trail-following ability To determine if workers experienced age-related declines in sensorimotor functions associated with the perception of trail pheromone and trail-following ability, individual ants were presented with artificial pheromone trails at concentrations of 1, 0.1 or 0.01 poison glands per trail [25]. Minor workers did not follow trails at 0.001 glands per trail.…”

“…Biogenic amine titres of individual brains were measured using high-performance liquid chromatography with electrochemical detection as described in Muscedere et al [25] by an experimenter blind to worker age. Details are provided in the electronic supplementary material.…”

“…The ant Pheidole dentata has served as a model to explore the evolution and ecology of social structure, as well as the neurobiological underpinnings of agerelated worker behaviour [22][23][24][25][26][27]. Minor workers expand their task repertoires from eclosion to approximately three weeks of age [23] while their brains undergo synaptic remodelling [28] and serotonergic systems that influence behavioural development and task performance mature [25,[29][30][31].…”

“…Minor workers expand their task repertoires from eclosion to approximately three weeks of age [23] while their brains undergo synaptic remodelling [28] and serotonergic systems that influence behavioural development and task performance mature [25,[29][30][31]. How do workers age behaviourally, and do age-related and brainbased neuroanatomical and neurochemical changes occur that could negatively impact lifespan task performance?…”