Sociogenomics of social organization: mechanistic and evolutionary underpinnings of caste development and facial recognition in paper wasps

Abstract

Sociogenomics is an emerging field that employs genomics to address the evolution and underlying mechanisms regulating social living. Studies on highly social (often called eusocial) insects have contributed to advances in sociogenomics. Eusocial insects exhibit extreme cooperation characterized by a division of labor with reproductive queen and non-reproductive worker castes. Eusociality has evolved multiple times within the insect order Hymenoptera (ants, bees, and wasps), and my work represents a major leap forward in the development of genomic resources for wasps, with a focus on the model genus Polistes. It has been proposed that there are conserved genetic mechanisms underlying the evolution of eusociality (genetic hypothesis), but this hypothesis has yet to be tested using comparative studies across all three major social lineages. I investigated genetic mechanisms underpinning caste development across three lineages (honey bees, fire ants, and paper wasps) using comparative transcriptomics, and I found greater evidence for a relatively loose genetic toolkit of shared molecular pathways and biological functions, rather than specific genes. To provide further insights into how castes evolve, there is also a need for mechanistic studies of caste determination in primitively eusocial insects like Polistes, which have morphologically similar behavioral castes. Therefore, I tested nourishment as an environmental factor driving developmental plasticity of paper wasp caste and observed that nourishment manipulation biased gene expression toward worker-like expression patterns. Additionally, new genetically and experimentally tractable model systems for sociogenomics are vital for studying complex social behavioral traits. Polistes are poised to be an excellent model for one such trait facial recognition since a species of wasps (P. fuscatus) is the only insect known to possess this ability. By comparing brain gene expression during staged social interactions for two paper wasp species with (P. fuscatus) and without (P. metricus) facial recognition, I found that differences in calcium signaling and dominance-related genes may be important for individual memory recall. Memory recall is not necessarily limited to facial