A typical relaxation of structural constraints in Hox gene clusters of squamates

Hox genes control many aspects of embryonic development in metazoans. Previous analyses of this gene family has revealed a surprising diversity in terms of gene number and organization between various animal species. In vertebrates, Hox genes are grouped into tightly organized clusters, originally claimed to be devoid of repetitive sequences. Here, we report the genomic organization of the posterior Hox loci (from Hox13 to Hox10) present in reptiles including the green anole lizard (Anolis carolinensis) and the corn snake (Pantherophis guttatus), and show that squamates have massively accumulated transposable elements, leading to gene clusters larger in size when compared to other vertebrates. In addition, we show the disappearance of highly conserved regulatory sequences within both the HoxA and HoxD clusters, as well as the rapid evolution of Hox coding regions within the squamata lineages. Finally, in parallel with these modifications in the genomic organization of squamata Hox clusters, we observe specific alterations in the expression patterns of posterior Hox genes during corn snake somitogenesis. Because transposable elements are major sources of genetic variations, we speculate that their insertion into Hox gene clusters, not reported so far for other vertebrates, may have associated with the evolution of the spectacular realm of morphological variations in the body plans of squamates.