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.

Caste, Sex, and Parasitism Influence Brain Plasticity in a Social Wasp

“…Males have smaller antennal lobes, which is likely due to experiencing less complex olfactory stimuli, as they do not engage in frequent chemicallybased social interactions in the colony. In contrast, reproductive females have proportionally larger antennal lobes, lips and collars, which is consistent with other studies that show sensory needs associated with division of labor, interactions among nestmates, learning and memory (Gronenberg et al, 1996;Ehmer and Hoy, 2000;O Donnell et al, 2011;Mora-Kepfer, 2014;Jernigan et al, 2021;Mertes et al, 2021;Rozanski et al, 2021;Uy et al, 2021). Thus, the social environment of female wasps has a wider range of chemical and sensory processing cues compared to males (Beani et al, 2014).…”

Isolation disrupts social interactions and destabilizes brain development in bumblebees

“…The early life environment may also impact social competence in the social insects, who live collectively in colonies ranging from a few individuals to millions 19 . A growing body of research shows that social isolation impacts the behavior and physiology of bees [20][21][22] , ants 1,2,4,23,24 , and wasps [25][26][27] . Few studies have been able to capture behavioral and neurogenomic consequences of early life social isolation in a single social animal system.…”

Evidence for a selective link between cooperation and individual recognition

“…6b). Second, we compared scaled CLR values between northern and southern populations for genes that are differentially expressed during social interactions in northern P. fuscatus 54 . Experimental evidence for differential regulation in response to social interactions suggests these genes could play a role in recognition behavior in this species.…”

“…The copyright holder for this preprint this version posted September 8, 2021. ; https://doi.org/10.1101/2021.09.07.459327 doi: bioRxiv preprint 11,935 genes, 1,088 genes were considered potentially related to the perceptual and cognitive mechanisms of individual recognition (hereafter: 'visual cognition genes'). We also categorized genes based on whether or not they showed evidence of differential expression in response to social experience based on data published in 54 . For both data sets, to statistically compare scaled CLR values between populations and gene categories, we log transformed scaled CLR values to improve linearity and fit linear mixed effects models using the lme4 package, with population (northern or southern), gene type (GO term dataset: visual cognition gene or other; differential expression dataset: yes or no), and their interaction as fixed effects, and gene identity as a random effect.…”