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 points, at the end of a 45-minute interaction and 4 hours later, in female P. 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 central brain. Results demonstrate much stronger transcriptional responses to social interactions in the central 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, 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.

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.…”

Sexual coordination in a whole-brain map of prairie vole pair bonding

“…In several species, including wasps, fish, bats, mice, and humans, researchers using a variety of biological measures find that social interactions are accompanied by coordinated neural states (Hasson et al, 2012;Kingsbury et al, 2019;Kinreich et al, 2017;Long et al, 2020;Vu et al, 2020;Zhang & Yartsev, 2019). In fighting fish (Betta splendens) and paper wasps (Polistes fuscatus), shared brain-transcriptomic signatures occur in individuals immediately after competitive interactions (Uy et al, 2021;Vu et al, 2020). In Egyptian fruit bats (Rousettus aegyptiacus) and lab mice, freely interacting individuals have correlated neural activity in the frontal cortex, and increases in inter-brain correlations predict whether subsequent interactions occur (Kingsbury et al, 2019;Zhang & Yartsev, 2019).…”