Overview
Colonies of the red harvester ant (Pogonomyrmex barbatus) differ in how they regulate collective foraging activity in response to changes in humidity. We used transcriptomic, physiological, and pharmacological experiments to investigate the molecular basis of this ecologically important variation in collective behavior among colonies. RNA sequencing of forager brain tissue showed an association between colony foraging activity and differential expression of transcripts related to biogenic amine and neurohormonal metabolism and signaling. In field experiments, pharmacological increases in forager brain dopamine titer caused significant increases in foraging activity. Colonies that were naturally most sensitive to humidity were significantly more responsive to the stimulatory effect of exogenous dopamine. In addition, forager brain tissue significantly varied among colonies in biogenic amine content. Neurophysiological variation among colonies associated with individual forager sensitivity to humidity may reflect the heritable molecular variation on which natural selection acts to shape the collective regulation of foraging.
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Methods and contributions
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Findings and contributions
- Forager brain transcriptomes differed between colony sets with different foraging responses to dry conditions: 273 of 20,387 reference transcripts were significantly differentially expressed.
- Dopamine-treated foragers made on average 20.5% more foraging trips than control-treated nestmates in the nine-colony 2016 field experiment.
- In 2017, foragers treated with the dopamine synthesis inhibitor 3-iodotyrosine made on average 19.1% fewer foraging trips than control-treated nestmates; the study did not directly quantify the inhibitor-induced brain dopamine change.
- Colonies that reduced foraging more strongly in dry conditions responded more strongly to the stimulatory effect of exogenous dopamine.
- Colonies differed in average forager brain dopamine-to-serotonin ratio; the study did not find a significant relationship between that ratio and humidity-sensitive foraging.
Methods
- Forager brain RNA sequencing — Compared six colonies differing in sensitivity to dry conditions, using three replicate libraries per colony from three pooled dissected brains and the kallisto/sleuth pipeline.
- Field pharmacological manipulation — Compared foraging activity of dopamine-treated foragers with control-treated nestmates in field experiments over two years.
- Colony humidity sensitivity — Estimated how much each colony reduced its daily number of foraging trips per percent decrease in humidity and compared this with response to drug treatment.
- Brain biogenic amine assays — Quantified dopamine and serotonin in active forager brain tissue from the nine colonies used for field pharmacology.
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