Laboratory for Animal Social Evolution and Recognition, Department of Neurobiology and Behavior, Cornell University, Ithaca, New York, United States of America.
PLoS Genet. 2021 Sep 3;17(9):e1009474. doi: 10.1371/journal.pgen.1009474. eCollection 2021 Sep.
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.
社会互动对个体的生理和健康有很大的影响。从直接意义上讲，社会刺激通常非常显著和吸引人。从更长的时间尺度来看，竞争互动通常会导致不同的社会等级和生理行为差异。要了解初始反应如何导致社会互动的长期影响，需要研究随着时间的推移反应的变化。在这里，我们研究了社交互动对雌性 Polistes fuscatus 纸黄蜂发现者在两个时间点的转录组特征的影响，一个是 45 分钟互动结束时，另一个是 4 小时后。雌性 P. fuscatus 具有可变的面部图案，用于视觉个体识别，因此我们分别检查了视叶和非视觉大脑中的转录动态。结果表明，与视叶相比，非视觉大脑对社交互动的转录反应要强得多。对社交互动有反应的差异调节基因富集了与记忆相关的转录本。在遭遇的胜利者和失败者之间的比较表明，在互动结束时具有相似的总体转录谱，这些谱在 4 小时的过程中显著分歧，失败者表现出与纸黄蜂中的攻击性和繁殖相关的基因表达水平的变化。在巢中，与支配性发现者相比，从属发现者的攻击性较低，觅食更多，产卵较少，我们发现失败者在失去遭遇后的数小时内，非视觉大脑中的许多基因的表达水平发生了变化，包括与攻击性、工蜂行为和繁殖相关的卵黄蛋白原。这些结果突出了早期的神经基因组变化，这些变化可能有助于社会昆虫中社会地位变化的行为和生理影响。
