The evolution of sociality is one of the major transitions in evolution, and has evolved independently in ants, bees, wasps, termites, and the naked mole rat. Since 2009, our group has been activity involved in the genomic study on social animals and so far has contributed on the genome sequencing and analyses for over 20 social insect species, including ants, bees, and termites. The full genome comparison allows us to identify the genomic signatures that corresponding to the social evolution. These included the large-scale comparative genomics study for 10 bee species that vary in social complexity, representing multiple independent transitions in social evolution (Science 2015). We found that many important genes show evidence of neutral evolution as a consequence of relaxed selection with increasing social complexity. Independent evolutionary transitions in sociality have independent genetic underpinnings. And we also observed an increasing level of gene regulatory network during the social evolution. These results supported the prediction that changes in gene regulation are key features of evolutionary transitions in biological organization, and further reveal the convergent adaptive and nonadaptive evolutionary processes common to both the early and advanced stages of multiple independent transitions from solitary to group living. The large amount of genome sequences that we are planning to generate from GAGA project will provide comprehensive understanding of the sociality evolution in ants as well as genomic mechanisms underlying the specialized life history for of different ant lineages.

Beyond DNA level, our group is also interested in studying the epigenetic regulation mechanisms that may lead to the individual developmental plasticity in social colony. My group has performed the first methylome study in ant brains and compared gene expression and methylation profiles between queens and workers for these two highly divergent ants, discovering vital genes for differential aging between queens and workers, and neural pathways that may be important for caste differences and communication (Current Biology, 2012). We also investigated the RNA-editing regulation in ants and demonstrating that many neural pathways in the brains of adult workers and virgin queens of A. echinatior are subjected to post-transcriptional RNA-editing. Neurotransmission and circadian rhythm genes associated with the sleep/awake cycle appeared to be the two pathways most enriched with RNA-editing sites (Nature Communications, 2014).

Social insects such as ants are the most sophisticated society builders after humans and Darwinian social evolution theory increasingly emphasizes the developmental analogies between differentiation of social castes and metazoan cell-lineages. However, our understanding of the key ontogenetic caste-differentiation mechanisms is extremely limited compared to the enormous recent progress in animal developmental and neurobiology. Our group has done multiple pioneering studies on social animal genomics to address the genetic basis for the evolution of sociality. To further reveal the genetic mechanisms and the neurobiological basis underlying the caste development and the behavioral differentiation, my group has now developed the leaf-cutting ant Acromyrmex echinatior and the pharaoh ant Monomorium pharaonis as laboratory animals for functional studies. We have established several programs to address these questions from developmental, evolutionary, and neurobiological angles.

The brain is the central organ to regulate and control the expression of behaviours that are remarkably distinct between social caste phenotypes, analogous to cells in somatic organs. While metazoan development is fine-grained and regulated by complex cell-signaling feedbacks, caste differentiation allows fewer developmental pathways of sterile (“somatic”) individuals, but each of these need to have its own brain-type with specific neurobiological wiring to secure internally coherent and flexible phenotypes and optimal communication with other caste phenotypes in the same colony. Recent studies have suggested that the complex transcriptional networks regulating social behaviors are related by hormonal titers that are established early in larval development, but the gene-networks involved and their dynamic changes have hardly been explored. A major step will therefore be to systematically monitor brain gene expression of larvae of males and different female castes during individual development in order to obtain a transcriptome atlas of caste-specific expression pathways that underlie differential development of caste phenotypes.

The enormous complexity of the brain is created by its structural and cellular diversity, and ultimately governed by underlying gene regulatory networks. Obtaining a genome-wide map of transcripts across the whole brain is therefore a crucial long-term goal to understand the genetic architecture of brains. Many studies have produced transcriptomes of anatomic sub-sections of brains, but this approach fails to capture the neuronal heterogeneity and the spatial organization of the cellular transcriptomic landscape across the brain. We will construct a complete 3-dimensional brain transcriptome using unique cutting-edge in-situ sequencing (ISS) technology that can record gene activity within tissues or organs while preserving the spatial information of the composing single cell transcripts. Developing this new technology will provide a fundamentally novel and powerful tool for neuroscience research.