<i>hox</i> gene expression predicts tetrapod-like axial regionalization in the skate, <i>Leucoraja erinacea</i>.

Abstract

The axial skeleton of tetrapods is organized into distinct anteroposterior regions of the vertebral column (cervical, trunk, sacral, and caudal), and transitions between these regions are determined by colinear anterior expression boundaries of <i>Hox5/6</i>, <i>-9</i>, <i>-10</i>, and <i>-11</i> paralogy group genes within embryonic paraxial mesoderm. Fishes, conversely, exhibit little in the way of discrete axial regionalization, and this has led to scenarios of an origin of <i>Hox</i>-mediated axial skeletal complexity with the evolutionary transition to land in tetrapods. Here, combining geometric morphometric analysis of vertebral column morphology with cell lineage tracing of <i>hox</i> gene expression boundaries in developing embryos, we recover evidence of at least five distinct regions in the vertebral skeleton of a cartilaginous fish, the little skate (<i>Leucoraja erinacea</i>). We find that skate embryos exhibit tetrapod-like anteroposterior nesting of <i>hox</i> gene expression in their paraxial mesoderm, and we show that anterior expression boundaries of <i>hox5/6</i>, <i>hox9</i>, <i>hox10</i>, and <i>hox11</i> paralogy group genes predict regional transitions in the differentiated skate axial skeleton. Our findings suggest that <i>hox-</i>based axial skeletal regionalization did not originate with tetrapods but rather has a much deeper evolutionary history than was previously appreciated.