Evolution of the snake body form reveals homoplasy in amniote Hox gene function

• Published in: Nature (London) 2015-04, Vol.520 (7545), p.86-89
• Main Authors: Head, Jason J., Polly, P. David
• Format: Article
• Language: English
• Subjects: 631/181/2806; Animals; Cloaca; Developmental Biology; Extremities - anatomy & histology; Fossils; Gene expression; Genes, Homeobox - genetics; Genetic aspects; Hox genes; Humanities and Social Sciences; Identification and classification; letter; Lizards - anatomy & histology; Models, Biological; Morphology; multidisciplinary; Phylogeny; Physiological aspects; Sacrum; Science; Snakes - anatomy & histology; Snakes - genetics; Spine - anatomy & histology; Vertebrates
• ISSN: 0028-0836; 1476-4687
• DOI: 10.1038/nature14042

Traditionally, the vertebral column of snakes was thought to have lost regionalization; Hox regionalization is now shown to be maintained in snakes, suggesting that gradational vertebral column regionalization is primitive to amniotes. Vertebral column regionalization in the snake It had been thought that the vertebral column of snakes has lost regionalization anterior to the cloaca, either because of homogenization of body-patterning Hox gene codes or of their downstream effectors. Jason Head and David Polly turn received wisdom on its head, with a quantitative analysis of the vertebral column in snakes that shows not only is Hox regionalization maintained, but the morphology is too. This surprising finding suggests that regionalization is primitive to amniotes, even though that regionalization might be quite subtle. In which case, the more apparent regionalization in some archosaurs (crocodiles and birds) and in mammals could be a consequence of independent evolution in the Hox code, rather than representing the ancestral condition for clades with snake-like body forms. Hox genes regulate regionalization of the axial skeleton in vertebrates 1 , 2 , 3 , 4 , 5 , 6 , 7 , and changes in their expression have been proposed to be a fundamental mechanism driving the evolution of new body forms 8 , 9 , 10 , 11 , 12 , 13 , 14 . The origin of the snake-like body form, with its deregionalized pre-cloacal axial skeleton, has been explained as either homogenization of Hox gene expression domains 9 , or retention of standard vertebrate Hox domains with alteration of downstream expression that suppresses development of distinct regions 10 , 11 , 12 , 13 . Both models assume a highly regionalized ancestor, but the extent of deregionalization of the primaxial domain (vertebrae, dorsal ribs) of the skeleton in snake-like body forms has never been analysed. Here we combine geometric morphometrics and maximum-likelihood analysis to show that the pre-cloacal primaxial domain of elongate, limb-reduced lizards and snakes is not deregionalized compared with limbed taxa, and that the phylogenetic structure of primaxial morphology in reptiles does not support a loss of regionalization in the evolution of snakes. We demonstrate that morphometric regional boundaries correspond to mapped gene expression domains in snakes, suggesting that their primaxial domain is patterned by a normally functional Hox code. Comparison of primaxial osteology in fossil and modern amniotes with Hox gen