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Vertebrate Innovations Perspective Vertebrate innovations Sebastian M. Shimeld* and Peter W. H. Holland* School of Animal and Microbial Sciences, University of Reading, Whiteknights, Reading RG6 6AJ, United Kingdom 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. ll chordates, at some stage in their life of both amphioxus (5) and ascidian (6) minded specifically disrupts an early mi- Acycle, possess a hollow neural tube embryos, although the expression pattern grating cell population that contributes to dorsal to a notochord, plus lateral muscle differs in detail between taxa. Lateral spinal ganglia, without affecting later- blocks. These characters unite tunicates (in- neural plate cells in amphioxus embryos migrating neural crest cells (13). Further- cluding ascidians), amphioxus, and verte- express members of the Msx (7), more, this mutant also affects Rohon- brates in the phylum Chordata. Compara- slug͞snail (8), and Distalless (9) gene Beard cells; these are not considered to be tive molecular and developmental analyses families whereas the latter gene is also neural crest derivatives but are a dorsal have refined this anatomical picture, sug- expressed in ectoderm adjacent to (and neural population of cells involved in gesting that the neural tube of the common overgrowing) the neural plate. In ascid- mechanosensory reception (and also ancestor of chordates had three major sub- ians, Msx (10) and slug͞snail (11) homo- present in amphioxus). This genetic link divisions along the anterior-posterior axis logues are expressed in cells contributing between early-migrating neural crest and (1), was patterned along the dorsoventral to the lateral neural plate (and in some Rohon-Beard cells suggests a possible axis by hedgehog and Bmp signaling (2), and other tissues); the Pax-3͞7 gene is ex- common origin. An early step in the evo- was probably segmented (3). These data pressed in the immediately adjacent ecto- lution of neural crest, therefore, may have suggest considerable complexity of the com- derm, after earlier expression in cells been the origin of a specific dorsal neural mon ancestor of chordates. Vertebrates are fated to contribute to neural plate (3). cell population contributing to sensory more complex still, both morphologically These studies demonstrate that the rela- processing; this would predate the diver- and genetically, and are characterized by a tive spatial expression patterns of many gence of the amphioxus and vertebrate considerable number of derived features genes involved in neural crest induction lineages. The evolution of cell migration (see Fig. 1). Here we review recent molec- were already present before the evolution was probably of later evolutionary origin, PERSPECTIVE ular and developmental data that give in- of vertebrates. Evolutionary changes to as was the origin of neural crest cell lin- sight into the evolutionary origin of these the regulation of these genes, therefore, eages with primarily non-neural fates, vertebrate innovations, notably the neural have probably not contributed directly to such as melanocytes and connective crest, placodes, complex brain, skeleton, and neural crest origins. The homologues of tissue. additional genes. several other genes involved in neural crest induction have not yet been exam- Placodes. Placodes are paired ectodermal The Neural Crest. Neural crest cells are a key ined in amphioxus or tunicate embryos; it thickenings that contribute to the formation vertebrate character. They form at the will be particularly informative if any of of a number of specialized structures of the boundary between neural plate and sur- these show significant expression differ- vertebrate head. They can be divided into SPECIAL FEATURE face ectoderm and migrate to contribute ences to vertebrates. the ‘‘sensory placodes,’’ which contribute to to many of the structures considered to be It is probably inappropriate to consider the eye, ear, lateral line, and olfactory or- vertebrate novelties, including the cra- the evolution of neural crest cells as a gans, and the ‘‘neurogenic placodes,’’ which nium, branchial skeleton, and sensory single evolutionary step or a single verte- contribute sensory neurons to cranial gan- ganglia. Experimentally, trunk neural brate character. First, head and trunk glia. It is probable that the two types of crest cells can be induced from chick neural crest have different developmental placode have separate evolutionary origins. embryonic neural plate by application of fates and potentials, and it is not yet clear Sensory placodes form a variety of cell Bmp-4 or -7 proteins (4), the genes en- whether they evolved as a single cell pop- types, including neuroendocrine cells, sen- coding which are expressed by ectodermal ulation or at different times in evolution. sory neurons, ciliated sensory receptors, and cells. Neural crest cells themselves are The existence of head neural crest in early glia. They may also not be confined to marked by expression of a number of vertebrate fossils such as Myllokunmingia vertebrates. Amphioxus has a putative ho- genes, including members of the Msx, (Fig. 2) is inferred by the presence of a mologue of the olfactory placode in the slug͞snail, Zic, Pax-3͞7, and Distalless complex branchial skeleton (12). Interest- corpuscles of de Quatrefages, a specialized gene families. Lateral neural plate cells ingly, no evidence of trunk neural crest group of anterior ectoderm cells. These cells also express these genes in vertebrate em- derivatives is seen in these fossils (al- bryos, suggesting some continuity of char- though this is not strong evidence for send axonal projections to the central ner- acter between these two cell populations. absence because preservation of such vous system along the most anterior nerve Homologues of several putative neural structures may be poor). Second, neural and are marked by expression of the ho- crest cell inducers and markers have been crest cells at one axial level may them- meobox gene AmphiMsx (7). This putative cloned from amphioxus and͞or tunicates, selves be a diverse population, with cells homology to olfactory placodes could be and their expression patterns have been that migrate at different times having dif- compared with vertebrates. These studies ferent developmental properties and pos- ͞ *To whom reprint requests should be addressed. E-mail: have revealed that the single BMP-2 4 sibly distinct evolutionary origins. For [email protected] and p.w.h.holland@reading. gene is expressed in non-neural ectoderm example, the zebrafish mutant narrow- ac.uk. PNAS ͉ April 25, 2000 ͉ vol. 97 ͉ no. 9 ͉ 4449–4452 Downloaded by guest on September 30, 2021 novelty, therefore, but the concentration of neurogenesis to discrete focal regions of ectoderm. Experiments show that the chick trigeminal placode is induced by signals from the neural plate (18) whereas pharyngeal endoderm is the source of the inductive signal (Bmp-7) for epibranchial placodes (16). In both cases, competence to respond to the inductive signal is wide- spread in cranial ectoderm, but absent from trunk ectoderm (16, 19). These data suggest that the focused neurogenesis of vertebrate epibranchial and dorsolateral placodes is achieved by a combination of localized inductive signals and restricted ectodermal competence. In summary, the collective term ‘‘pla- codes’’ refers to some rather different structures, probably with different evolu- tionary origins. Some sensory placodes (at least the otic and olfactory) may have homologues in basal chordates. Even if this is so, it is apparent that they were elaborated considerably during early ver- tebrate evolution. Epibranchial and dor- solateral placodes appear to be new; we infer that their origin depended on the evolution of specific inductive signals. Elaboration of the Vertebrate Brain. A com- plex brain with specialized fore-, mid-, and hindbrain regions is characteristic of all ver- Fig. 1. What is a vertebrate? Phylogeny showing the relationship between living members of the Phylum tebrates. Other chordates also possess a Chordata (in bold, at top), plus the Cambrian fossils Myllokunmingia (12) (a craniate) and Haikouella (30) distinct structure at the rostral end of the (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 rela- neural tube, called the cerebral vesicle (am- tionships are less clear. Systematics reserves the taxon Vertebrata for those animals possessing vertebrae: phioxus) or sensory vesicle (ascidian larvae). that is, lampreys and jawed vertebrates, with hagfish excluded as a sister group. These three taxa are The extent of homology between these united by the term Craniata. Some molecular analyses, however, support monophyly of lampreys and structures has long been controversial, but is hagfish (comprising the Cyclostomata) (33), which would make the Vertebrata paraphyletic. Here we central to discerning which aspects of brain depict the node at the base of hagfish, lampreys, and jawed vertebrates as unresolved to reflect this organization are vertebrate innovations. conflict between molecular and morphological data. We view
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