Development and evolution of the lateral plate mesoderm: Comparative analysis of amphioxus and lamprey with implications for the acquisition of paired fins

Abstract

Possession of paired appendages is regarded as a novelty that defines crown gnathostomes and allows sophisticated behavioral and locomotive patterns. During embryonic development, initiation of limb buds in the lateral plate mesoderm involves several steps. First, the lateral plate mesoderm is regionalized into the cardiac mesoderm (CM) and the posterior lateral plate mesoderm (PLPM). Second, in the PLPM, Hox genes are expressed in a collinear manner to establish positional values along the anterior–posterior axis. The developing PLPM splits into somatic and splanchnic layers. In the presumptive limb field of the somatic layer, expression of limb initiation genes appears. To gain insight into the evolutionary sequence leading to the emergence of paired appendages in ancestral vertebrates, we examined the embryonic development of the ventral mesoderm in the cephalochordate amphioxus Branchiostoma floridae and of the lateral plate mesoderm in the agnathan lamprey Lethenteron japonicum, and studied the expression patterns of cognates of genes known to be expressed in these mesodermal layers during amniote development. We observed that, although the amphioxus ventral mesoderm posterior to the pharynx was not regionalized into CM and posterior ventral mesoderm, the lateral plate mesoderm of lampreys was regionalized into CM and PLPM, as in gnathostomes. We also found nested expression of two Hox genes (LjHox5i and LjHox6w) in the PLPM of lamprey embryos. However, histological examination showed that the PLPM of lampreys was not separated into somatic and splanchnic layers. These findings provide insight into the sequential evolutionary changes that occurred in the ancestral lateral plate mesoderm leading to the emergence of paired appendages.