One of the main vertebrate novelties was the elaboration of the vertebrate head, with an array of sense organs and features involved in an active predatory lifestyle. These structures are derived from two embryonic cell populations, cranial placodes and the neural crest, which arose near the base of the vertebrate lineage. Both of these pluripotent cell types undergo epithelial to mesenchymal transitions and have the capacity to migrate extensively within the body to form a variety of structures and cell types, including sensory neurons, the facial skeleton, connective tissue in the head and neck, peripheral neurons and glia, and melanocytes. The appearance of neural crest cells and cranial placodes and the resultant accumulation of special sense organs in the vertebrate head appears to have facilitated the evolution and radiation of the vertebrates. The subsequent invention of jaws enhanced the evolutionary success of the vertebrates, allowing a new mode of feeding.
Cranial placodes are discrete regions of thickened ectoderm that form in characteristic positions in the head of vertebrate embryos and contribute to specialized head structures. They make important contributions to the paired sense organs (nose, eyes, ears, and lateral line) and to cranial sensory ganglia, and are required for the formation of the sensory nervous system in the vertebrate head (Fig. 6.8a). Several lines of evidence suggest that at least some types of placodes are not unique to vertebrates but can also be found in basal chordates. Potential homologs of the olfactory placode have been identified in Amphioxus (corpuscles of Quatrefages) and in the colonial ascidian Botryllus schlosseri (neurohypophyseal duct). These specialized cell types form at the anterior end of the embryo, undergo morphogenetic movements, and express some of the same markers as vertebrate olfactory placodes. Another ascidian, Halocynthia roretzi, possesses structures (atrial primordia) that develop in a similar manner to, and express homologs of genes found in, the vertebrate otic placode. While placodes are apparently not unique to the vertebrates, they were, however, elaborated extensively during early vertebrate evolution and became indispensable for the formation of the vertebrate head.
The neural crest is derived from cells found at the interface of the lateral neural plate and epidermis along the dorsal side of the body (Fig. 6.8b,c). Basal vertebrate lineages such as hagfish and lampreys, as well as early fossil vertebrates, appear to possess most neural crest
I I DiencaphaNc and anterior mescnc&phaiic NC ^ Posterior mesgnwpnalic NO □ MIC
I I DiencaphaNc and anterior mescnc&phaiic NC ^ Posterior mesgnwpnalic NO □ MIC
Developmental origin of cranial placodes and neural crest
(a) In the chick embryo, cranial placodes (eight-somite stage fate map shown on right side) and neural crest contribute sensory neurons to the ganglia of cranial nerves (shown on left side). (b) Hox gene expression in the chick embryo at day 3 when the branchial arches (BA) are being colonized by neural crest cells originating from the posterior half of the midbrain (mesencephalon) and the rhombomeres (rl —r8). The arrows indicate the origin of the neural crest cells migrating to each BA. Expression of Hox genes is also indicated in the superficial ectoderm, the endoderm, and mesoderm. (c) Color-coded migration map of cephalic neural crest cells in the avian embryo. Posterior midbrain neural crest cells contribute to the anterodistal part of branchial arch 1 (BA1). The complementary portion of BA1 derives from r1/r2 together with a small contribution from r3. Other branchial arches (BA2-4) are populated by neural crest cells from more caudal rhombomeres.
Source: Part a from Baker CV, Bronner-Fraser M. Dev Biol 2001; 232: 1-61; copyright (2001), reprinted with permission from Elsevier. Parts b,c from Couly G, Creuzet S, et al. Development 2002; 129: 1061-1073.
derivatives, indicating that these cell populations arose early in the vertebrate lineage. Other chordates, such as amphioxus and ascidians, do not have homologous cell types. Nevertheless, comparisons of gene expression have suggested that members of the regulatory circuits that are required for neural crest induction in vertebrates are deployed in the neural tube in more basal chordates. Vertebrate neural crest cells express a suite of developmental regulatory genes, including transcription factors of the Dlx, Msx, slug/snail, Pax2/5/8, and Pax3/7 families. Homologs of these genes are expressed in comparable positions in both amphioxus and ascidians. Thus, the spatial expression domains of these genes appear to have been established before neural crest cells evolved at the base of the vertebrate lineage. Conspicuously, other markers of neural crest cells are not expressed at the lateral edge of the neural plate in amphioxus, but can be found in neural crest cells in lampreys. The elaboration of the neural crest in the vertebrate lineage, with its diverse neuronal and non-neuronal cell types, may have its roots in a small ancestral population of cells in or near the chordate lateral neural plate. The changes must have occurred "rapidly" at the base of the vertebrate lineage.
The earliest vertebrates (agnathans) lacked jaws but jawed vertebrates (gnathostomes) appeared ~400 million years ago and subsequently radiated to occupy varied terrestrial and aquatic niches. During gnathostome development, both the upper and lower jaws are formed from the first set of branchial/pharyngeal arches, paired structures located ventrally in the cranial region of the embryo. The upper jaw will develop from the proximal portion of the arch while the lower jaw develops from the distal region. Neural crest cells from the midbrain and hindbrain migrate into the branchial arches (Fig. 6.8b,c) and differentiate into (among other things) the cartilage and bone of the craniofacial skeleton, including the jaws. In lampreys (agnathans), the early development of the neural crest and arches, including gene expression patterns, is similar to that of gnathostomes, except for the presence of lamprey Hox gene expression in the first arch. In vertebrates, Hox gene expression in the first arch represses jaw formation. The absence of Hox expression in the first arch of vertebrates may have allowed the formation of extra cartilage, which acted as a substrate for jaw formation
While shifts in Hox gene expression may have been permissive for jaw development and evolution, other patterning genes were recruited for the subsequent sculpting of jaw architecture. In mammals, the Dlx genes are expressed in nested domains along the proximodis-tal axis of the arches (Fig. 6.9a). Dxl3/7 are expressed at the distal tips of the arches while Dlx5/6 are expressed in a broad distal domain and Dlx1/2 are expressed and required throughout the arches. By contrast, lampreys do not show restricted expression of any Dlx genes along the proximodistal axes of the arches. The combinatorial expression of the Dlx genes acts to specify different domains along the proximodistal axis of the arches and regulates the identity of jaw elements (Fig. 6.9b). This regionalization of the first arch was likely a crucial step in elaboration of the upper and lower jaws in the gnathostome lineage.
The increased complexity of vertebrate cranial development, including the elaboration of placodes, the appearance of a neural crest cell population, and formation of jaws may be correlated with expansion of the vertebrate genome through large-scale duplication events (see Chapter 4). The additional developmental regulatory genes that were created by gene duplication evolved novel roles in controlling the differentiation of new cell types and the more complex organization of the vertebrate central and peripheral nervous systems. In vertebrates, gene duplication and divergence appears to have provided the potential for more complex morphologies.
Caudal branchial arches BA2 BA1
Was this article helpful?