Complete author-written abstract
Task allocation among social insect workers is an ideal framework for studying the molecular mechanisms underlying behavioural plasticity because workers of similar genotype adopt different behavioural phenotypes. Elegant laboratory studies have pioneered this effort, but field studies involving the genetic regulation of task allocation are rare. Here, we investigate the expression of the foraging gene in harvester ant workers from five age- and task-related groups in a natural population, and we experimentally test how exposure to light affects foraging expression in brood workers and foragers. Results from our field study show that the regulation of the foraging gene in harvester ants occurs at two time scales: levels of foraging mRNA are associated with ontogenetic changes over weeks in worker age, location and task, and there are significant daily oscillations in foraging expression in foragers. The temporal dissection of foraging expression reveals that gene expression changes in foragers occur across a scale of hours and the level of expression is predicted by activity rhythms: foragers have high levels of foraging mRNA during daylight hours when they are most active outside the nests. In the experimental study, we find complex interactions in foraging expression between task behaviour and light exposure. Oscillations occur in foragers following experimental exposure to 13 L : 11 D (LD) conditions, but not in brood workers under similar conditions. No significant differences were seen in foraging expression over time in either task in 24 h dark (DD) conditions. Interestingly, the expression of foraging in both undisturbed field and experimentally treated foragers is also significantly correlated with the expression of the circadian clock gene, cycle. Our results provide evidence that the regulation of this gene is context-dependent and associated with both ontogenetic and daily behavioural plasticity in field colonies of harvester ants. Our results underscore the importance of assaying temporal patterns in behavioural gene expression and suggest that gene regulation is an integral mechanism associated with behavioural plasticity in harvester ants.
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Findings and contributions
- Foraging mRNA levels are linked to changes over weeks in worker age, location, and task, and show significant daily oscillations in foragers.
- Foragers have high foraging mRNA levels during daylight hours, when they are most active outside the nest.
- Under a 13 L : 11 D light cycle, oscillations appeared in foragers but not in brood workers.
- In constant darkness (DD), foraging expression showed no significant change over time in either task.
- In both field and experimentally treated foragers, foraging expression was significantly correlated with expression of the circadian clock gene cycle.
Methods
- Field collection of Pogonomyrmex barbatus workers in five task/age groups — Workers from mature colonies near Rodeo, New Mexico were sorted into callows, brood workers, nest maintenance workers, patrollers, and foragers.
- 24 h time-of-day sampling at 4 h intervals — Ants of each task and colony were sampled every 4 h over a day and flash frozen to track daily changes in foraging gene expression.
- Light exposure experiment: 13 L : 11 D versus constant darkness — Foragers and brood workers from six field colonies were housed in artificial nest-boxes under ambient light/dark cycles or complete darkness for 24 h.
- Brain qPCR of Pbfor and cycle, normalized to PbEF1a — Whole-brain RNA was assayed by TaqMan qPCR using harvester-ant-specific primers, with elongation factor 1a as the control gene.
- Mixed-model ANOVAs and sinusoidal contrast analysis of forager expression — Expression over time was tested with mixed-model ANOVAs, and forager patterns were compared to a sinusoid approximating daily foraging activity.
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