The Role of Dopamine in the Collective Regulation of Foraging in Harvester Ants

Abstract

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.

Keywords: Entomology; Molecular Neuroscience; Neuroscience.

Graphical abstract

Figure 1

Forager Brain Transcriptomic Differences Are Associated with Differences in Colony Behavior (A) Volcano plot representing forager brain gene expression differences between groups of colonies that vary in their sensitivity to humidity (see Transparent Methods 1A). Red transcripts are significantly differentially expressed at FDR-corrected q-value < 0.01. (B) Transcript co-expression graph. Nodes are transcripts that are colored according to mean fold-change between the 2 sets of colonies. Edges connecting nodes represent correlated expression levels across all 18 libraries. Blue nodes are transcripts upregulated in foragers from colonies that strongly reduce foraging on dry days. Orange nodes are transcripts upregulated in foragers from colonies that do not strongly reduce foraging on dry days. Gray nodes are transcripts that were evenly expressed between the 2 groups of colonies.

Figure 2

Oral Administration of Dopamine to P. barbatus Workers Significantly Raises Single Brain Dopamine Titers in a Dose- and Time-Dependent Fashion Data shown on y axis are mean ± SEM of dopamine titers in picograms per single dissected P. barbatus brain. Dopamine titer was measured 1 and 3 days after oral administration of 0 mg/mL, 3 mg/mL, and 30 mg/mL dopamine in water solution. No. of single brains measured per group is 6–9. Dopamine titer was measured by mass spectrometry with a labeled internal dopamine standard (see Transparent Methods 1B–1D).

Figure 3

Manipulation of Forager Brain Dopamine Titer Alters Foraging Activity The x axis shows colony ID. The y axis shows the percent change in foraging trips made by drug-treated foragers relative to controls (see Transparent Methods 1E). Top bars show percent increase in foraging trips made by foragers treated with 3 mg/mL dopamine; light blue bars, 2016; dark blue bars, 2017. Bottom bars show percent decrease in foraging trips made by foragers treated with 3 mg/mL 3IY, 2017.

Figure 4

Colonies Naturally More Sensitive to Humidity Are More Responsive to Dopamine x Axis represents colony. The left y axis shows sensitivity to humidity, the estimated number of fewer foraging trips made by the colony per percent decrease in humidity (see Transparent Methods 1F). The left y axis shows sensitivity to humidity, the estimated number of fewer forager trips (± SEM) made by the colony per percent decrease in relative humidity (See Transparent Methods 1F).

Figure 5

Colonies Significantly Vary in Forager Brain Biogenic Amine Content The x axis represents colony. The y axis is the average forager brain dopamine to serotonin ratio ± SEM, as measured by high-performance liquid chromatography (see Transparent Methods 1G). N = 5 samples of 2 pooled forager brains per colony.