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

Hox genes regulate regionalization of the axial skeleton in vertebrates, and changes in their expression have been proposed to be a fundamental mechanism driving the evolution of new body forms. 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 domains9, or retention of standard vertebrate Hox domains with alteration of downstream expression that suppresses development of distinct regions. 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 gene distributions within Amniota indicates that a functional, sequentially expressed Hox code patterned a subtle morphological gradient along the anterior–posterior axis in stem members of amniote clades and extant lizards, including snakes. The highly regionalized skeletons of extant archosaurs and mammals result from independent evolution in the Hox code and do not represent ancestral conditions for clades with snake-like body forms. The developmental origin of snakes is best explained by decoupling of the primaxial and abaxial domains and by increases in somite number, not by changes in the function of primaxial Hox genes.

同源框基因（Hox genes）可调控脊椎动物中轴骨骼的区域分化，其表达变化被认为是驱动新体型演化的核心机制。具有去区域化泄殖腔前中轴骨骼的蛇形体型的起源，曾被解释为两种机制：一是同源框基因表达结构域的同质化⁹，二是保留脊椎动物标准同源框结构域，但通过改变下游表达以抑制特定区域的发育。两种模型均假定存在一个高度区域化的祖先类群，但目前尚未分析过蛇形体型类群中骨骼原轴域（primaxial domain，即椎骨、背肋区域）的去区域化程度。本研究结合几何形态测量学与最大似然分析，结果显示：与具四肢的类群相比，细长四肢退化蜥蜴及蛇类的泄殖腔前原轴域并未发生去区域化；且爬行动物原轴形态的系统发育结构，并不支持蛇类演化过程中发生了区域化程度的丢失。我们证实，形态学的区域边界与蛇类中已定位的基因表达结构域相吻合，这表明其原轴域由正常功能的同源框编码模式所调控。对比化石与现生羊膜动物的原轴骨学特征，结合羊膜动物内的同源框基因分布情况可知：在羊膜类支系的基干类群以及包括蛇类在内的现生蜥蜴中，一套具有功能的、按序列表达的同源框编码模式，沿着前后轴塑造了细微的形态梯度。现生主龙类与哺乳类的高度区域化骨骼，是同源框编码模式独立演化的结果，并不代表蛇形体型类群的祖先状态。蛇类的发育起源，最佳解释为原轴域与轴旁域（abaxial domains）的解耦以及体节数量的增加，而非原轴域同源框基因功能的改变。