Brain-body allometric decoupling and degree of sociality in wasps: a phylogenetic view

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The social brain hypothesis, first proposed for primates and then expanded to other vertebrates, proposes that the transition from solitary to social life was accompanied by a brain enlargement to handle new social challenges. In contrast to vertebrates, solitary insects often present larger brains than closely related eusocial species. This is attributed to the emergence of task specialization in insect societies, which may reduce the individual's behavioral repertoire and neural tissue investment. However, phylogenetic studies on how brain complexity and social behavior coevolved in insects remain scarce. Some previous studies link greater brain volume to increased social challenges faced by certain individuals in the colony, but this does not apply to all eusocial societies. Here we investigate the relationships between social evolution and brain complexity in Vespidae wasps, emphasizing the Epiponini species and their worker-controlled colonies, using volumetric data based on a phylogenetic approach. We measured brain neuropil volumes in species with varying sociality levels (solitary, primitively eusocial, and advanced eusocial) and then mapped allometric relationships and caste differences onto a Vespidae phylogenetic tree. Our findings show that the transition to eusociality was accompanied by brain-body allometric decoupling depending on caste and lineage. Queens generally exhibit greater investment in mushroom bodies, but this difference is lost in more derived Epiponini lineages. We conclude that advanced eusociality relaxes brain-body allometric constraints, thereby promoting concerted evolution among brain regions independent of body size, especially in lineages with greater caste transition flexibility, potentially facilitating whole brain volumetric changes during caste transitions.