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

['Floria M. K. Uy', 'Laboratory For Animal Social Evolution', 'Recognition', 'Department Of Neurobiology', 'Behavior', 'Cornell University', 'Ithaca', 'New York', 'United States Of America', 'Christopher M. Jernigan']

Date: 2021-11

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.

Aggressive interactions often create inequalities–some individuals win while others lose. Winning versus losing can lead to large physiological differences between individuals, including different neurogenomic profiles between winners and losers. How this information about contest outcome leads to distinct neurogenomic profiles is poorly understood. Here we examine gene expression in response to aggressive social encounters in paper wasps, which naturally form dominance hierarchies on their nests in the wild. Shortly following encounters winners and losers have similar expression profiles, likely because similar mechanisms are engaged by social experiences. Four hours later, we find divergent neurogenomic profiles between winners and losers, with losers showing larger shifts in expression compared to winners. Many of the most dynamically expressed genes have been previously associated with dominance and caste differences in paper wasps showing how a single interaction can engage many of the same genomic networks that are involved in mediating more dramatic differences in queen-worker behavioral differences are also involved in responses shortly following social interactions.

Introduction

Social interactions can give rise to a range of immediate as well as long-lasting effects on behavior and physiology [1–4]. Regardless of the nature of the interaction or the outcome, social experiences are expected to have a number of shared effects on the physiology of those involved. Processing social information may depend on multiple cues or signals, which are likely to be processed by similar brain regions and genes within [5–7] and across species [8, 9]. In addition to social information processing, interactions can increase rates of activity and movement, especially in relation to courting or fighting [2, 8]. In recent years there has been a growing number of gene expression studies examining the neurogenomic responses to social interactions across a range of taxa including honeybees, mice and sticklebacks [8, 10, 11], finding shared elements of neurogenomic responses immediately following social challenges. Indeed, at the level of neural firing patterns, social interactions give rise to similar patterns of neural activity in bats and mice [6, 7]. Similar initial patterns of neural activation and transcriptomic changes, however, give way to divergent effects depending on the outcome of encounters. Longer-term consequences of social interactions depend on the nature and outcome of the encounters. Winning versus losing typically cause different physiological and behavioral responses [12–18]. Over repeated interactions, this can lead to profound differences in behavior, physiology, life expectancy, and fitness [4, 19–22]. Divergent social outcomes lead to different physiological responses, which may be initiated by differences in neurogenomic responses shortly following an interaction.

There have also been studies examining the effects of winning and losing rather than simply the response to social challenge per se. In zebrafish, socially driven transcriptional changes require individuals to assess the outcome of the interaction [23] (i.e., did they win or lose). In sub-social carpenter bees, repeatedly winning or losing staged contests gives rise to distinct neurogenomic profiles [16, 24]. In the ant Harpegnathos saltator, workers compete for reproductive openings upon the removal of the queen and within a few days individuals have divergent neurogenomic profiles depending on their trajectory toward either staying as a worker or becoming a reproductive gamergate [25]. Similar divergence in social behavior and neurogenomic profiles are seen among Polistes dominula paper wasp workers fighting for the dominant breeding position upon queen removal [26, 27]. Collectively, these studies demonstrate that social interactions can have immediate effects on neurogenomic profiles and that repeated interactions can have longer-term consequences for patterns of transcription in the brain that differ for winners and losers or higher- versus lower-ranking individuals. Understanding how transcriptional patterns change over time in response to different social interactions and across different taxa will help us to more clearly link social outcomes to short and long-term physiological changes.

Understanding the dynamic changes that occur between initial responses and subsequent divergence between winners and losers will help link these two areas of research. Studies examining the temporal dynamics of transcriptional responses to social challenge in stickleback and mice over the course of a few hours highlight the transient and dynamic nature of transcriptional responses [10, 11]. Detailed work on the early transcriptional responses to fighting between pairs of male beta fish demonstrates that fighting individuals have shared transcriptomic responses within the first hour after fighting [5]. The studies mentioned above have looked at dynamic responses to a social challenge from territorial or nest intrusions or more established winner-loser effects. The dynamics by which interacting individuals develop divergent transcriptomic responses over the course of a few hours has received less attention.

Here we examine the dynamic neurogenomic responses to social interactions in female Polistes fuscatus paper wasp foundresses over the course of four hours following a staged social interaction. Paper wasps are primitively eusocial insects in which females found new nests each spring after overwintering [28]. Social interactions among paper wasp foundresses lead to profound physiological differences between dominants and subordinates. Nests are initiated by a single foundress or small groups of foundresses, who form an aggression-based dominance hierarchy, which determines the extent of work and egg-laying [29, 30]. Polistine foundresses have aggressive interactions in both the pre-nesting stage as well as on the nests, where they interact aggressively with co-foundresses as well as occasional usurpers [31–34]. Wasps also reliably show aggression to other individuals in neutral arenas, providing a convenient method for studying the effects of aggression in a controlled setting [35–37]. Previous work has shown that Polistes foundresses respond rapidly to aggressive encounters by modulating juvenile hormone [18], though genome-wide transcriptomic responses have yet to be examined immediately following aggressive interactions. In established co-foundress associations, dominant and subordinate foundresses show differential expression of genes associated with aggressive behavior [38]. By comparing the temporal shifts in gene expression between winners and losers, we can potentially identify genes that are associated with the early stages of dominance hierarchy formation in paper wasps. Additionally, such analyses may generate more general insights into the neurogenomic processes by which social interactions lead to divergence in behavior and physiology.

The neurogenomic responses to social interactions in P. fuscatus are also of interest because this species recognizes individuals based on variable facial features [39, 40]. Individual recognition appears to mediate dominance interactions among groups in the lab and on natural nests [36, 39]. Individual recognition is not present in other closely related species of paper wasps [40, 41], suggesting the trait has evolved relatively recently [42]. Neurogenomic responses to operant conditioning related to face-learning have been previously studied [43], but their neurogenomic responses to social interactions have not been investigated. Wasps are known to form long-term memories of those they have interacted with [44], so examination of neural transcriptomes a few hours after the interaction has the potential to reveal insights into the neurogenomic responses related to social memory, as long-term memory formation occurs hours after initial learning has occurred [45]. Visual facial recognition is a notable feature of P. fuscatus from Ithaca, NY [39], so we were also interested in the relationship between visual processing and social interactions. Previous studies of eye morphology have suggested that the visual system may have evolved to facilitate individual recognition [46] and visual brain regions are developmentally sensitive to social isolation [47]. Additionally, analyses of selection in P. fuscatus identified visual processing genes as enriched as recent targets of positive selection in this species [42], likely in relation to social interactions and individual recognition. Given the importance of vision in social interactions for this species, we examined the effects of social interaction on the optic lobes, which contain early visual processing neuropils, as well as the non-visual brain (Fig 1, hereafter ‘optic lobe’ and ‘brain’).

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TIFF original image Download: 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. https://doi.org/10.1371/journal.pgen.1009474.g001

We designed an experiment to examine the dynamic neurogenomic responses shortly after social interactions in the optic lobe and brain (Fig 1). Wasps were filmed in a neutral arena while paired with another weight-matched individual or alone (S1 Movie). To better understand the temporal dynamics of neurogenomic responses in the hours following a social interaction, we looked at transcriptomes at two time points: immediately following a 45-minute interaction and after 4 hours of separation back in the wasps’ original housing containers (Fig 1). For each of the two time points we generated 15 social trials (n = 30 wasps) and 15 nonsocial trials (n = 15 wasps). The social trials tend to be aggressive, generating winners and losers for each trial (n = 15 winner and n = 15 losers at each time point). In total we examined the behavior of 60 wasps in social trials and 30 wasps went through nonsocial trials, though the numbers for RNAseq analyses were smaller due to some samples not generating libraries or sufficient sequencing (Table 1). In the grander scheme of paper wasp dominance relationships, both of these timepoints are very early in the time course over which a dominance hierarchy would be formed. For ease of distinguishing between the samples we refer to those taken immediately at the end of a 45-minute interaction as ‘early’ and those at 4 hours as ‘late’.

Using the RNAseq data from paper wasp foundresses, we address multiple questions. (1) How does the magnitude of neurogenomic responses differ between earlier versus more central brain regions? To the extent that responses are driven by the processing of social outcomes rather than simply response to social stimuli, we may expect larger and or more dynamic changes in more central compared to earlier brain regions, such as the optic lobe. (2) Given that paper wasps learn and remember the identities of wasps they interact with [44], is there a detectable neurogenomic signature related to memory in paper wasps following interactions? (3) How does social outcome influence the dynamics of neurogenomic responses over the course of a few hours? Recent studies suggest similar neural responses among individual during or right after social interactions [5–7], whereas others demonstrate divergent outcomes over the course of days [16, 24, 25, 27]. Therefore, we may predict that initial neurogenomic responses will be more similar immediately following social interactions and that winners and losers will diverge transcriptionally over time.

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[1] Url: https://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1009474

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