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

The degree of phenotypic diversity within social species has previously been associated with more complex genetic regulation both in cis and trans contexts. 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, which has also been reported in Hymenoptera. We also find that genes under selection support neotenic caste determination. We find there are key differences in Blattodea TF regulation in comparison with Hymenoptera with contractions in TF gene families and no compensatory change in TF DNA binding motifs either in frequency or diversity in TF promoter regions. Furthermore, we show that an increase in social complexity leads to greater diversity in TF activating domains, one of the evolutionary and structural building blocks of TFs, meanwhile, DNA-binding domains, undergo very little change. This study highlights similarities in social transitions between Hymenoptera and Blattodea, with evidence of large changes in transcriptional regulation followed by lineage specific adaptations. Our results indicate that the transcriptional diversity linked to social complexity is not attributable to transcription factors, but is instead likely driven by an alternative mechanism..