Expression patterns of threespine stickleback Hox genes and insights into the evolution of the vertebrate body axis

Abstract

Understanding the patterning mechanisms that operate to promote differentiation of individual segments along the main body axis is an important goal of both developmental and evolutionary biology. In order to gain a better insight into the role of Hox genes in generating diversity of axial plans seen in vertebrates, we have cloned 11 homeobox sequences from an acanthopterygian teleost, the threespine stickleback, and analyzed the expression of 7 of these during embryogenesis. Transcripts are observed in a variety of tissues, including the neural tube, paraxial mesoderm, lateral plate mesoderm, pectoral fins, pronephric ducts, as well as some neural crest-derived structures. Anterior limits of expression in the central nervous system and paraxial mesoderm exhibited both similarities and differences to those of mouse and zebrafish homologs. In both stickleback and zebrafish embryos expression limits within the paraxial mesoderm were detected only within the trunk region in which ribs are attached to all vertebrae. The finding of this pattern in two divergent teleosts as well as in various tetrapod species supports the hypothesis that a Hox precode was present prior to the divergence of ray-finned and lobe-finned fishes and was subsequently used to generate different types of vertebrae in tetrapods. We also describe a dynamic pattern of expression of several stickleback Hox genes associated with the development of the caudal paraxial mesoderm, which suggests uncoupling of the process of segmentation from segmental identity determination. We propose that in fishes the patterning of the tail region is under the control of a separate mechanism from the trunk, which utilizes Hox genes in a different manner.