Isolation disrupts social interactions and destabilizes brain development in bumblebees

• Published in: Current biology 2022-06, Vol.32 (12), p.2754-2764.e5
• Main Authors: Wang, Z. Yan, McKenzie-Smith, Grace C., Liu, Weijie, Cho, Hyo Jin, Pereira, Talmo, Dhanerawala, Zahra, Shaevitz, Joshua W., Kocher, Sarah D.
• Format: Article
• Language: English
• Subjects: Animals; antennation; Bees; Brain; gene expression; machine vision; RNA-seq; Social Behavior; social insects; Social Interaction; Social Isolation
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2022.04.066

Social isolation, particularly in early life, leads to deleterious physiological and behavioral outcomes. Here, we leverage new high-throughput tools to comprehensively investigate the impact of isolation in the bumblebee, Bombus impatiens, from behavioral, molecular, and neuroanatomical perspectives. We reared newly emerged bumblebees in complete isolation, in small groups, or in their natal colony, and then analyzed their behaviors while alone or paired with another bee. We find that when alone, individuals of each rearing condition show distinct behavioral signatures. When paired with a conspecific, bees reared in small groups or in the natal colony express similar behavioral profiles. Isolated bees, however, showed increased social interactions. To identify the neurobiological correlates of these differences, we quantified brain gene expression and measured the volumes of key brain regions for a subset of individuals from each rearing condition. Overall, we find that isolation increases social interactions and disrupts gene expression and brain development. Limited social experience in small groups is sufficient to preserve typical patterns of brain development and social behavior. [Display omitted] •Isolation increases social contact but decreases specificity of interactions in bees•Isolated bees show signatures of a dysregulated brain transcriptome•Brain developmental trajectories are destabilized and stochastic in isolated bees•Limited social contact is enough to preserve typical social behavior and neurobiology Wang et al. probe the effects of early life isolation on the behavior and neurobiology of bumblebees. Isolation increases social contact but alters the type and specificity of social interactions. Isolation also alters brain development and gene expression, but even limited social experience can preserve typical social behaviors and neurobiology.