Patterns of Conservation and Loss of Hox Genes in Xenacoelomorph Lineage Since Divergence From Last Common Bilaterian Ancestor

The explosion of body forms found in bilaterians is thought to be tied to the diversification of Hox transcription factors, which play a critical role in development along the anterior-posterior axis for most bilaterians. However, the evolutionary history of Hox genes in Bilateria's early branches remains unclear. Xenacoelomorpha, a clade of marine worms including Xenoturbella and the acoelomorphs Acoela and Nemertodermatida, have a simple Hox complement and are a particular group of interest. Past surveys of Hox in Xenacoelomorpha have been taxonomically limited. To address this, we analyze the homeodomains and surrounding amino acid motifs coded by Hox, ParaHox, and extended Hox genes across 40 xenacoelomorph transcriptomes and four genomes, along with representatives of other major bilaterian groups and the anthozoan Nematostella vectensis. We show that several motif annotations previously proposed to be synapomorphies of Acoela are ubiquitous across both Xenacoelomorpha and the rest of Bilateria and found new Hox content specific to Acoela and Xenoturbella. Our results reveal homology between xenacoelomorph antHox and other bilaterian Hox1 genes, though the relationships of centHox and postHox genes remain unresolved either due to rapid sequence evolution or extensive birth-death processes. Our analyses suggest that diversification of bilaterian Hox involved both extensive retention and loss of ancestral content. Hox variability between xenacoelomorphs and other bilaterians reflects selective retention of ancestral Hox content rather than affinity to either deuterostomes or protostomes and does not remove support from a monophyletic Xenacoelomorpha sister group to all other Bilateria.