Evolutionary Transitions in Social Behavior are Associated With Convergent and Partially Reversible Expansions of Transcription Factor Binding Sites

The evolution of sociality involves shifts in physiology and behavior, most notably the emergence of a reproductive division of labor. Within social colonies, these distinct behavioral phenotypes arise from differential regulation of a shared genome. Changes in transcription factor (TF) binding motifs are one potential mechanism underpinning this plasticity, with prior studies suggesting that social species exhibit expansions in TF binding sites. However, it remains unclear whether motif expansions are reversed when sociality is lost. Here we analyze predicted TF motif occurrences across gene promoters in 42 bee species spanning millions of years of evolutionary divergence and multiple independent gains and losses of sociality. We compare motif presence across species to test whether motif expansions are a convergent feature of social evolution and whether their presence secondarily decreases when social behavior is lost. Our findings are consistent with previous research, demonstrating an expansion of TF motifs in lineages which have gained sociality. However, contrary to expectation, we do not observe genome-wide motif contractions in lineages which have secondarily lost social behavior. Despite this overall pattern, we still identify several motifs, promoter regions, and specific motif-promoter pairs which exhibit complementary changes with both gains and losses of sociality. These regulatory targets are enriched for similar organismal functions, providing strong candidates for further study. Our results lend additional support to the hypothesis that novel phenotypes may arise through modification of existing gene regulatory networks.