Reduced regulatory complexity associated with the evolutionary transition to sociality from cockroaches to termites despite evolutionary parallels with Hymenoptera

Abstract

In social species, the phenotypic diversity within a single species has often been associated with more complex genetic regulation. Transcription factors (TFs) being key to genetic regulation, have been studied in the origins of eusociality in Hymenoptera (Bees, Ants and Wasps) but less so in Blattodea (Cockroaches and Termites). Here we show that the social transition in Blattodea, from cockroaches to termites, displays similar patterns of regulatory change to those found in Hymenoptera. Specifically, by analysing 3 cockroach and 5 termite genomes, we find more TF families with relaxed selection compared to intensified selection and lineage-specific gene family expansions in termites. We also find that genes under selection support neotenic caste determination. There are key differences in TF regulation in comparison with Hymenoptera with contractions in TF gene families and reduced diversity in enriched DNA binding motifs of TFs. Furthermore, we show that with increased social complexity TF activating domain diversity, one of the evolutionary and structural building blocks of TFs, decreases with gene family size while DNA binding domain diversity and number increases. This study highlights similarities in social transitions between Hymenoptera and Blattodea, with evidence of large changes in transcriptional regulation followed by lineage specific adaptations. We also show that phenotypic diversity in termites does not necessitate greater transcriptional complexity.