Dynamic neurogenomic responses to social interactions and dominance outcomes in female paper wasps

Abstract

Social interactions have large effects on individual physiology and fitness. In the immediate sense, social stimuli are often highly salient and engaging. Over longer time scales, competitive interactions often lead to distinct social ranks and differences in physiology and behavior. Understanding how initial responses lead to longer-term effects of social interactions requires examining the changes in responses over time. Here we examined the effects of social interactions on transcriptomic signatures at two times, at the end of a 45-minute interaction and 4 hours later, in female Polistes fuscatus paper wasp foundresses. Female P. fuscatus have variable facial patterns that are used for visual individual recognition, so we separately examined the transcriptional dynamics in the optic lobe and the non-visual brain. Results demonstrate much stronger transcriptional responses to social interactions in the non-visual brain compared to the optic lobe. Differentially regulated genes in response to social interactions are enriched for memory-related transcripts. Comparisons between winners and losers of the encounters revealed similar overall transcriptional profiles at the end of an interaction, which significantly diverged over the course of 4 hours, with losers showing changes in expression levels of genes associated with aggression and reproduction in paper wasps. On nests, subordinate foundresses are less aggressive, do more foraging and lay fewer eggs compared to dominant foundresses and we find losers shift expression of many genes in the non-visual brain, including vitellogenin, related to aggression, worker behavior, and reproduction within hours of losing an encounter. These results highlight the early neurogenomic changes that likely contribute to behavioral and physiological effects of social status changes in a social insect.

Fig 1. Overview of experimental design and RNAseq data.

(A) The experiment consisted of generating two groups of wild-caught wasps that either engaged in a recent social experience or remained nonsocial. Half of each group was sacrificed at the end of a 45-minute interaction period with the other half held in individual containers for 4 hours until they were then sacrificed. RNA was extracted separately from the combined optic lobes (purple) and the remainder of the brain, called ‘brain’ throughout (green). In other figures, we show the part the tissue the data is derived from with the relevant icon. Here and in subsequent figures, red wasp symbols are used to indicate winners, blue wasp symbols for losers, and grey wasps for control individuals that did not have social interactions.

Fig 2. Behavioral interactions.

(A) Trials were characterized by initially increasing and then decreasing rates of aggression. Most of the aggression within the trials took place in the first few minutes. (B) The number of aggressive acts and the overall intensity as measured by the summed aggression are highly correlated. (C) Across trials, one individual was more aggressive in terms the number of acts, the summed intensity or acts, or an index of the average intensity of the acts. Here the number of acts between the more aggressive individuals (i.e., winners) are shown on the x-axis relative the number of aggressive acts committed by the less aggressive individuals (i.e. losers) on the y-axis. The line shows the 1:1 relationship. The positive relationship between aggression between individuals in the trials suggests are possible role for mutual escalation in shaping contest behavior.

Fig 3. Social interactions influence neurogenomic signatures more in the central brain than in the optic lobes.

(A) Brain region is the strongest separator of the data in a principal component analysis. Recent social experience has a stronger effect on the samples from the central brain compared to the optic lobes in the PCA. (B) Hundreds of genes (n = 742, FDR < 0.1) are differentially expressed as a result of social interactions in the combined dataset of both time points and tissues. (C) The effects of social interactions are stronger in the central brain compared the optic lobes. At both early and late time points there are hundreds of genes differentially expressed (FDR < 0.1) between social and nonsocial groups. The following codes are used in the axis legend: ES = early social, EN = early nonsocial, LS = late social, LN = late nonsocial. (D-E) The volcano plots show the log2 fold change between social (up) and nonsocial (down) on the x-axis and the -log10 P value on the y-axis. The red and blue striped wasp symbol indicates that the data includes all socially interacting wasps. Panel D shows data for the central brain, while panel E shows data for the optic lobes.

Fig 4. Similar overall neurogenomic responses in winners and losers.

(A) There is significantly more overlap than expected by chance between the DEGs for winners and losers compared to each other as well as both winners and losers compared to all individuals with recent social experience (P < 2e-16). Note, the circle sizes are not to scale. The numbers within each section indicate the number of genes shared in each area of overlap. (B) The difference in log2 fold change in gene expression for all genes with a mean normalized expression count of 100 or greater for nonsocial individuals are correlated for winners and losers. Both panels show analyses from the entire dataset with both brain regions and time points combined.

Fig 5. Greater divergence in loser brain transcriptomes over time.

(A) Focusing on only the central brain dataset, the log2 fold change in gene expression differences between nonsocial individuals and winners and losers are well correlated at the earlier time point. (B) At the later time point, there is substantially less correlation between winner and loser responses relative to nonsocial individuals. (C) Gene correlation modules are organized into two meta-modules, which are associated with late winners and late losers respectively. The top panel shows a dendrogram with the colors labeled and social outcomes labeled. The boxes have been added to highlight the two meta-modules. The bottom panel shows a heatmap showing the relationships among modules. Higher correlations are show by warmer red colors with modules with low or not correlations shown in blue. The two meta-modules highlighted in the dendrogram have been highlighted here with black outlines.

Fig 6. Shifts in winner and loser gene expression over time.

(A) There are more dramatic shifts in the responses of losers compared to winners over time. The scatter plot shows the log2 fold change between early and late winners on the x-axis against the similar early to late comparison for losers on the y-axis. Thus, genes in the upper right quadrant are those that increase over time in both winners and losers, while those the upper left quadrant increase in losers but decrease in winners. The greater spread along the y- compared to x-axis shows that there are larger changes in loser gene expression profiles over time compared to winners. There is a weak but significant negative correlation suggesting that some genes that increase in losers tend to decrease in winner and vice versa. Notable genes are highlighted. Data points are color-coded according to the legend. (B) The panels show the mean normalized count of expression for losers, winners and nonsocial individuals at early and late sampling points. Lines are drawn connecting the points between groups of the same social outcome. Note that the y-axis scale is different for each gene and depends on the dynamic range of the specific gene. For example, arrestin shows a much smaller change in expression across groups than takeout-like 1, which is expressed at very low levels in nonsocial controls but expressed much more highly in wasps that engaged in social interactions.