Vertebrate innovations

Abstract

Vertebrate innovations include neural crest cells and their derivatives, neurogenic placodes, an elaborate segmented brain, endoskeleton, and an increase in the number of genes in the genome. Comparative molecular and developmental data give new insights into the evolutionary origins of these characteristics and the complexity of the vertebrate body.

Figure 1

What is a vertebrate? Phylogeny showing the relationship between living members of the Phylum Chordata (in bold, at top), plus the Cambrian fossils Myllokunmingia (12) (a craniate) and Haikouella (30) (a basal chordate). Some putative fossil chordates, including Pikaia and Cathaymyrus (possibly related to amphioxus) (31, 32) and the Euconodonts (25) (possible vertebrates) are omitted, as their precise relationships are less clear. Systematics reserves the taxon Vertebrata for those animals possessing vertebrae: that is, lampreys and jawed vertebrates, with hagfish excluded as a sister group. These three taxa are united by the term Craniata. Some molecular analyses, however, support monophyly of lampreys and hagfish (comprising the Cyclostomata) (33), which would make the Vertebrata paraphyletic. Here we depict the node at the base of hagfish, lampreys, and jawed vertebrates as unresolved to reflect this conflict between molecular and morphological data. We view the evolution of vertebrates as the acquisition of characters along the chordate stem lineage. These characters, established by comparison to outgroups (i.e., amphioxus and tunicates), include (i) neural crest cells and their derivatives; (ii) elaboration of placode-derived structures; (iii) elaboration of the brain, including rhombomeric segmentation; (iv) cartilage (and possibly mineralization); (v) the axial skeleton and the head skeleton; and (vi) a large increase in total number of genes in the genome. Other characters present only in jawed vertebrates, including paired appendages, hinged jaws, an adaptive immune system, and specialization of the axial skeleton along the anterior-posterior axis, were probably acquired later, on the jawed vertebrate stem lineage, and will not be considered here.

Figure 2

Reconstruction of the early Cambrian craniate Myllokunmingia (12). [Reproduced with permission from John Sibbick (Copyright 1999 John Sibbick).]

Figure 3

Mesodermal subdivision in amphioxus (A and B) compared with a schematic vertebrate (C). A and B show progressive stages in the development of amphioxus mesoderm. A ventrolateral zone of amphioxus mesoderm (red) grows down to surround the gut. Homology of this zone to the lateral plate mesoderm of vertebrates (red in C) is supported by site of origin and fate. Medial amphioxus somite cells form myotome (yellow) whereas dorsolateral cells (orange) eventually move to surround the notochord. On the basis of position of origin, these may be homologous to the myotome and dermatome of vertebrates (yellow and orange, respectively, in C), although these cells do not contribute to a dermis in amphioxus. The vertebrate sclerotome (gray in C) has no equivalent in amphioxus and is a novelty linked with the evolution of the axial skeleton. A and B are adapted from ref. .