Overview
Natural selection on collective behavior acts on variation among colonies in behavior that is associated with reproductive success. In the red harvester ant (Pogonomyrmex barbatus), variation among colonies in the collective regulation of foraging in response to humidity is associated with colony reproductive success. We used RNA-seq to examine gene expression in the brains of foragers in a natural setting. We find that colonies differ in the expression of neurophysiologically-relevant genes in forager brains, and a fraction of these gene expression differences are associated with two colony traits: sensitivity of foraging activity to humidity, and forager brain dopamine to serotonin ratio. Loci that were correlated with colony behavioral differences were enriched in neurotransmitter receptor signaling & metabolic functions, tended to be more central to coexpression networks, and are evolving under higher protein-coding sequence constraint. Natural selection may shape colony foraging behavior through variation in gene expression.
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Methods and contributions
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Findings and contributions
- Forager brain gene expression patterns were more similar among nestmates than non-nestmates, with substantial variability within colonies as well.
- A fraction of colony expression differences were associated with humidity sensitivity of foraging and forager brain DA:5HT ratio.
- Neurotransmitter receptors as a category were significantly correlated in expression with colony sensitivity of foraging activity to humidity.
- Gene coexpression analysis identified 11 modules of loci with coordinated expression patterns across colonies.
- Genes more central to coexpression modules tended to be more correlated with colony traits and to be evolving under increased coding-sequence constraint.
Methods
- Single-forager brain RNA-seq from nine field colonies of P. barbatus — Foragers collected on one morning near Rodeo, New Mexico had single brains sequenced on Illumina HiSeq 4000, yielding 85 transcriptomes from 9 colonies.
- Expression-trait correlations with humidity sensitivity and brain DA:5HT — Gene expression was correlated with colony sensitivity of foraging to humidity and forager brain dopamine-to-serotonin ratio, at colony-mean and per-sample levels.
- PCA and linear discriminant analysis of transcriptomes by colony — PCA on TPM expression, with 30 components retained for LDA stratified by colony, tested whether forager transcriptomes carry a colony signature.
- WGCNA signed coexpression network with iterative module-density filtering — Coexpression modules were built in the R WGCNA library and iteratively filtered to retain densely interconnected modules, leaving 7085 genes.
- dN/dS against honey bee and five ant species, modeled with a GLM — Coding-sequence constraint was estimated with orthologr and related to coexpression centrality and trait correlation in a generalized linear model.
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