Brain Transcriptional Profiles of Male Alternative Reproductive Tactics and Females in Bluegill Sunfish

Abstract

Bluegill sunfish (Lepomis macrochirus) are one of the classic systems for studying male alternative reproductive tactics (ARTs) in teleost fishes. In this species, there are two distinct life histories: parental and cuckolder, encompassing three reproductive tactics, parental, satellite, and sneaker. The parental life history is fixed, whereas individuals who enter the cuckolder life history transition from sneaker to satellite tactic as they grow. For this study, we used RNAseq to characterize the brain transcriptome of the three male tactics and females during spawning to identify gene ontology (GO) categories and potential candidate genes associated with each tactic. We found that sneaker males had higher levels of gene expression differentiation compared to the other two male tactics. Sneaker males also had higher expression in ionotropic glutamate receptor genes, specifically AMPA receptors, compared to other males, which may be important for increased spatial working memory while attempting to cuckold parental males at their nests. Larger differences in gene expression also occurred among male tactics than between males and females. We found significant expression differences in several candidate genes that were previously identified in other species with ARTs and suggest a previously undescribed role for cAMP-responsive element modulator (crem) in influencing parental male behaviors during spawning.

Fig 1. Alternative reproductive tactics of bluegill sunfish.

This figure has been modified from Gross and Charnov [35] and Neff and Knapp [36]. Ages are based on data from Gross and Charnov [35] but may differ among populations [33].

Fig 2. Heatmap of transcripts differentially expressed in at least one group comparison.

Only transcripts with a log2 fold change of 1.5 or greater are included in the heatmap, representing 1,400 transcripts. Count values were averaged within each group and are scaled by row. Sneak = sneaker males, Sat = satellite males, Parent = parental males, Fem = females, NS_P = non-spawning parental males.

Fig 3. Biological process GO terms enriched by genes with higher expression in sneaker males compared to all other groups.

Boxes of similar color are grouped into the same GO term hierarchy. Box size reflects the–log10 p-value of the GO term.

Fig 4. UpSet graph displaying the number of differentially expressed transcripts among groups.

For each comparison, the number on top of each bar represents the number of differentially expressed transcripts (intersection size). The comparison in question is indicated by the dots or connected dots below its respective bar. Set size indicates the total number of transcripts for each comparison.