Development of the vertebra and fin skeleton in the lamprey and its implications for the homology of vertebrate vertebrae.

BACKGROUND: Although vertebrae are the defining character of vertebrates, they are found only in rudimentary form in extant agnathans. In addition, the vertebrae of agnathans possess several unique features, such as elastin-like molecules as the main matrix component and late (post-metamorphosis) differentiation of lamprey vertebrae. In this study, by tracing the developmental process of vertebrae in lamprey, we examined the homology of vertebrae between lampreys and gnathostomes. RESULTS: We found that the lamprey somite is first subdivided mediolaterally, with myotome cells differentiating medially and non-myotome cells emerging laterally. Subsequently, collagen-positive non-myotome cells surround the myotome. This pattern of somitogenesis is rather similar to that in amphioxi and sheds doubt on the presence of a sclerotome, in terms of mesenchyme cells induced by a signal from the notochord, in lamprey. Further tracing of non-myotome cell development revealed that fin cartilage develops in ammocoete larvae approximately 35 mm in body length. The development of the fin cartilage occurs much earlier than that of the vertebra whose development proceeds during metamorphosis. CONCLUSION: We propose that the homology of vertebrae between agnathans and gnathostomes should be discussed carefully, because the developmental process of the lamprey vertebra is different from that of gnathostomes.

Development of the lamprey velum and implications for the evolution of the vertebrate jaw.

BACKGROUND: The vertebrate jaw is thought to have evolved through developmental modification of the mandibular arch. An extant jawless vertebrate, the lamprey, possesses a structure called "velum"-a mandibular arch derivative-in addition to the oral apparatus. This leads us to assess the velum's possible contribution to the evolution of jaws. RESULTS: The velar muscles develop from progenitor cells distinct from those from which the oral muscles develop. In addition, the oral and velar regions originate from the different sub-population of the trigeminal neural crest cells (NCCs): the former region receives NCCs from the midbrain, whereas the latter region receives NCCs from the anterior hindbrain. The expression of patterning genes (eg, DlxA and MsxA) is activated at a later developmental stage in the velum compared to the oral region, and more importantly, in different cells from those in the oral region. CONCLUSION: The lamprey mandibular arch consists of two developmental units: the anterior oral unit and the posterior velar unit. Because structural elements of the lamprey velum may be homologous to the jaw, the evolution of vertebrate jaws may have occurred by the velum being released from its functional roles in feeding or respiration in jawless vertebrates.

Identification of a unique lamprey gene with tandemly repeated sequences and pharyngeal chondrocyte-specific expression.

Recent studies have revealed a common cartilage genetic regulatory network among vertebrates, cephalochordates, and arthropods. It has been proposed that this network was originally established for the dense connective tissues of ancestral invertebrates and subsequently recruited for chondrocyte differentiation in various lineages. This reasoning prompted questions about whether the evolution of cartilage from dense connective tissues occurred in the common ancestors of vertebrates. Alternatively, the evolution of cartilage may have occurred independently in agnathans and in gnathostomes, because extant agnathans (cyclostomes) are known to possess a matrix composition different from that of gnathostomes. Here, we identified the gene which is likely to encode one of the matrix proteins unique to lamprey cartilage, which we designated pharymprin. Pharymprin shows specific expression in larval pharyngeal chondrocytes. Like lamprins, which are the known matrix proteins of lamprey trabecular cartilage, pharymprin is also composed of repeated sequences. However, the repeated sequence is distinct from that of lamprins. The presence of two distinct matrix proteins in lamprey cartilage supports the hypothesis that true cartilage evolved independently in cyclostomes and gnathostomes.