Integrative and Comparative Biology Advance Access originally published online on June 28, 2008
Integrative and Comparative Biology 2008 48(5):611-619; doi:10.1093/icb/icn065
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Historical hypotheses regarding segmentation of the vertebrate head
Neurobiology Unit, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0201, USA; Department of Neurosciences, School of Medicine, University of California, San Diego, La Jolla, CA 92093-0201, USA
Correspondence: 1E-mail: rgnorthcutt{at}ucsd.edu
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The morphology of the vertebrate head is extremely complex and comprises numerous iterative structures that arise from each of the embryonic germ layers. The search for a fundamental plan uniting all of these serial structures spans
200 years. The earliest attempt to identify a common plan was J. W. Goethe's vertebral theory of skull organization, in which the skull was interpreted as being formed by a series of trunk vertebrae. This theory was rejected by T. H. Huxley in the 1858
Croonian Lecture and was replaced by the segmented mesodermal model of Francis Balfour, which was elaborated subsequently by A. Marshall, Gavin de Beer, and Edwin Goodrich. This model assumes that the head of the earliest vertebrates consisted of eight segments. It further assumes that each segment contained dorsal muscles arising from the somitic mesoderm, and ventral muscles arising from lateral plate mesoderm, except for the first segment, which lacked ventral muscles derived from the lateral plate mesoderm. The muscles of each head segment were believed to be innervated by two pairs of cranial nerves, homologous to the dorsal and ventral spinal nerves of lampreys. The validity of this theory, known as the Goodrich model, came into question, however, after the discovery that the branchiomeric muscles associated with each pharyngeal arch do not arise from lateral plate mesoderm, as initially proposed by Marshall and subsequently accepted by Goodrich and de Beer, but, rather, arise from paraxial mesoderm. Furthermore, segmentation of the brain into some 14 neuromeres cannot be accommodated by any model involving eight segments. Finally, there is also clear evidence that at least one, if not two, additional series of placodally derived sensory nerves occurs in the head and has no counterpart in the trunk. At present, there is no theory of segmentation that can account for all cephalic iterative structures. |
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Our current view of the organization of the vertebrate head is the result of a number of research agendas that primarily span the period of 1790–1940. During this period, a number of developmental topics were studied intensively for the first time. They include (1) formation of germ layers, (2) mesodermal differentiation, (3) cranial nerve development, (4) brain morphogenesis, (5) neural crest differentiation, and (6) placodal development. Much of this research was driven by two major questions: (1) What is the nature of the vertebrate body plan? and (2) Is the vertebrate head segmented? The data that resulted from these studies led to a number of major hypotheses, including the vertebral hypothesis, the mesodermal segmental hypotheses, and the neuroepithelial hypotheses. The history of these hypotheses has been touched on in a number of brief reviews, including those by de Beer (1937
), Hall and Hanken (1985), Northcutt (1990, 1993), and Holland (2000), but the hypotheses have not been re-evaluated in the context of much of the developmental data generated in the past 10 years. The present essay attempts to correct this situation by re-visiting the 200-year-old question of whether or not the vertebrate head is segmented.
A review of the literature on head segmentation clearly indicates that there is no agreement on the meaning of this term. In some cases, it implies that the vertebrate head arose ancestrally from a series of complete head segments (metameres), such as those seen in annelids (Dohrn's theory 1875) or arthropods (Gaskell's theory 1908). In other cases, however, segmentation in vertebrates has been viewed as the more restricted division of one or more embryonic tissues, such as the paraxial mesoderm (Balfour 1878), neurectoderm (Neal 1898), or endoderm (Kingsbury 1926; Romer 1972), into a series of iterative structures in the anterior to posterior axis. In this review, the vertebrate head is viewed as segmented if there is developmental evidence that its structures arise from each of the three germ layers and form a series of repeated elements, in registry, in the anterior–posterior axis.
The vertebral hypothesis
According to de Beer (1937), Johann Wolfgang Goethe, the German naturphilosopher best known as the author of Faust, was the first person to hit upon the idea that the vertebrate skull consisted of fused vertebrae when his servant called his attention to a partially disarticulated sheep's skull in a Jewish cemetery in Venice in 1790. However, Goethe did not publish his idea until 1820 by which time the idea had also occurred to a number of other people including Oken (1807) and Geoffroy St.-Hillaire (1818). During much of the 19th century, the vertebral hypothesis, in various forms, was widely accepted and was most dramatically illustrated by Owen (1848) in his publication On the Archetype and Homologies of the Vertebrate Skeleton. Initially, Owen viewed an archetype as a fundamental pattern on which a natural group of animals or an organ system has been constructed, but later he appears to have believed that it represented a Platonic ideal. Various political and social reasons have been suggested for this shift (Desmond 1982; Rupke 1994). In any case, Owen described the head of the vertebrate archetype as consisting of four segments, with the skull being formed by the modification of four vertebrae, which he identified rostrocaudally as the nasal, frontal, parietal, and occipital vertebrae (Fig. 1). In his view, an ideal vertebra consisted of a dorsal neural arch, a centrally located centrum, and a ventral hemal arch (Fig. 1). The neural arch was believed to be formed by a pair of neurapophyses, capped by a neural spine, whereas the hemal arch was believed to be formed by a pair of dorsal pleurapophyses and a pair of ventral hemapophyses, capped by a hemal spine. Owen believed that the fused centra formed the floor of the neurocranium, whereas the enlarged neurapophyses and neural spines formed the walls and roof of the neurocranium, respectively. Finally, he interpreted the first and second hemal arches of the head as forming the upper and lower jaws, respectively, with the third and fourth hemal arches forming the branchial skeleton. Thus, Owen was able to account for all bones of the vertebrate "endocranium" as modified elements of four vertebrae.
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In 1858, Huxley dealt the death blow to all vertebral hypotheses in his now famous Croonian Lecture before the Royal Society. The paper (Huxley 1858
) based on his lecture is a masterpiece of scientific reasoning and still well worth reading. Huxley realized that two questions had to be answered in order to test these hypotheses. The two questions were: (1) Are all vertebrate skulls constructed on the same plan? and (2) If such a plan exists, is it identical to that of the vertebral column? He also realized that only two methods could be used to answer these questions: comparative adult anatomical studies and comparative developmental studies. In the first case, Huxley considered it necessary to examine an extensive series of skulls and vertebral columns and in the second case he believed it was necessary to compare the embryonic development of skulls and vertebral columns. He stated that comparative developmental evidence was the stronger of the two, but did not list the reasons on which he based this conclusion. It is possible that Huxley believed that if two adult structures arise from the same embryonic source and pass through the same developmental stages, they must be homologous. It is also possible, however, that he emphasized development because Owen lacked expertise in this area (Rupke 1994). For whatever reasons, Huxley concluded that all vertebrate skulls do exhibit a common plan, but that skulls and vertebrae arise from different embryonic sources and develop through very different stages. Huxley noted that only the caudalmost portion of the skull includes the notochord, one of the main embryonic sources of vertebral formation; the notochord is totally absent from the rostral two-thirds of the skull, which arises from trabecular mesenchyme, a tissue unique to the skull.
In an elegant conclusion, Huxley stated:
"I confess I do not perceive how it is possible, fairly and consistently to reconcile these facts with any existing theory of the vertebrate composition of the skull, except by drawing ad libitum upon the Deus ex machina of the speculator, - imaginary "confluences", "connations", "irrelative repetitions", and shiftings of position – by whose skilful application it would not be difficult to devise half a dozen very pretty vertebral theories, all equally true, in the course of a summer's day."
Although different vertebral hypotheses continued to appear in some anatomical texts for a few years after Huxley's lecture, comparative studies shifted heavily to a developmental paradigm.
Mesodermal segmental hypotheses
In 1878, Balfour published the first detailed description of the development of the shark Scyllium (Scyliorhinus). Balfour claimed that the mesodermally derived muscle plates of the trunk, now recognized as somites, continued into the head as a series of hollow epithelial sacs that he termed head cavities. He recognized eight of these (Fig. 2) and suggested that they were evidence that the head consisted of eight segments, which he termed, rostrocaudally, the preoral or premandibular, the mandibular, the hyoid, and the first through the fifth branchial segments. Shortly afterwards, Marshall (1881) confirmed Balfour's observations and suggested that the lateral plate mesoderm, which forms smooth muscle in the trunk, also continues into the head, where it is divided into branchiomeres by the developing pharyngeal pouches. In contrast to the trunk, however, the lateral plate mesoderm was believed to form striated muscle. In 1891, Julia Platt looked at head development in the spiny dogfish, Squalus acanthias, and described an additional head cavity rostral to the premandibular head cavity described by Balfour and Marshall. The discovery of this additional head cavity, which is known as Platt's vesicle (Figs. 2 and 3), raised the possibility that there was a total of nine head somites and thus nine segments, which would have included two premandibular segments.
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Additional studies on Scyllium and other elasmobranches (van Wijhe 1882
; Dohrn 1890; Froriep 1894) indicated a variable number of head somites ranging from 12 to 15. In an attempt to resolve these differences, Goodrich (1918) re-examined head development in Scyllium. He recognized the premandibular, mandibular, and hyoid head cavities of Balfour, but he was also able to trace the head mesoderm rostral to the premandibular head cavity, where it ended rostral to the foregut as a sheet of cells that is presently recognized as the prechordal plate. It is within this plate in Squalus, that Platt described the development of her vesicle. In Scyllium, however, Goodrich claimed that the prechordal plate disappears without ever forming a vesicle. In Squalus, however, Platt (1891) and Lamb (1902) believed that her vesicle formed myoblasts before degenerating. In any case, Goodrich (1918) concluded that Platt's vesicle had no phylogenetic significance and that only three preotic head cavities or somites existed in the earliest vertebrates.
Goodrich also attempted to resolve another problem with head somites. In contrast to Balfour (1878) and Marshall (1881), both of whom recognized eight head somites, van Wijhe (1882) attributed nine segments to the head, but believed that the pharyngeal slit and branchiomere associated with the fourth head somite had been lost so that the "facial" nerve innervated two somites. In re-examining head development in Scyllium, Goodrich saw no evidence for the loss of a pharyngeal slit and associated branchiomere, but he did see evidence for the loss of at least one, if not two, head somites. As the otic capsule develops in Scyllium, it comes to lie over the caudal portion of the third somite and most of the fourth somite (Fig. 2). Goodrich believed that the expansion of the otic capsule destroyed the caudal portion of the third somite and all of the fourth somite, so that no distinct myotome forms in this region. He also believed that the fifth head somite was affected by the otic capsule, so that only the most caudal portion of the fifth somite formed myoblasts, and he was unable to identify a nerve innervating these myoblasts. Therefore, he concluded that head somites four and five failed to form somatic muscle. Similar conclusions were reached regarding the fourth and fifth head somite in Squalus by de Beer (1922), 4 years later.
In his 1918 paper, Goodrich published what may have become the single most important morphological illustration of the 20th Century (Fig. 4), in which he indicated the fate of myotomes and branchiomeres, as well as their innervation in each of the eight segments that he believed constituted the primitive head of jawed vertebrates. He reprinted this figure in his magnus opus (Goodrich 1930), as did de Beer (1937) in his treatise on the vertebrate skull. Goodrich's model of the organization of the vertebrate head has been widely adopted and has been reproduced in almost all American textbooks of comparative anatomy.
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Many European textbooks of comparative anatomy, however, have adopted another segmental mesodermal model based primarily on the morphological studies of Bjerring (1970
, 1972, 1977, 1984) and Jarvik (1980). These authors believed that Platt's vesicle gives rise to the inferior oblique muscle, which was claimed by Holmgren (1940) to be evidence that the head of the first jawed vertebrates consisted of two premandibular segments, in addition to the remaining seven segments of Goodrich's model. Although they accepted van Wijhe's claim (1882) that a pair of dorsal and ventral nerves characterizes each head segment; they suggested that the terminal nerve is the dorsal nerve of the first premandibular segment; they divided the oculomotor nerve into two nerves for the first and second premandibular segments; and they claimed that they had discovered an additional nerve, nervus tenuis, said to supply their last preotic somite, which, unlike Goodrich, they believed forms a posterior basiotic muscle (Bjerring 1970).
A number of criticisms can be raised regarding the models of Goodrich and Jarvik-Bjerring (Kingsbury 1926; Romer 1972; Northcutt 1990, 1993). Although Kingsbury's and Romer's criticisms predate the publication of the Jarvik-Bjerring model, their criticisms nonetheless apply to it as well as to Goodrich's model. Kingsbury (1926) emphasized that in order for the vertebrate head to be segmented, each head segment should contain a number of iterative structures, such as a neuromere, a pair of dorsal and ventral cranial nerves, and a mesodermal somite. Kingsbury accepted the earlier claims that both the head somites and pharyngeal arches form iterative series but believed there was no evidence that they were in topographical registry. He noted that segmentation of the paraxial mesoderm in the head developmentally precedes formation of the pharyngeal pouch, and he concluded that segmentation of the paraxial mesoderm (mesomerism) and lateral plate mesoderm (branchiomerism) had occurred independently.
Similar concerns were raised by Romer (1972), who believed that the head of vertebrates consisted of somatic and visceral units, which arose phylogenetically at different times. He argued that the head of the earliest deuterostomes essentially consisted of a visceral branchial basket used for feeding and that a somatic series of head muscles was added later as part of a locomotive apparatus. Thus, he concluded:
"It may happen by chance that during development some one gill bar and its musculature may lie below some one specific myotome and its derived musculature. But there is no a priori reason to think that the two segmental systems – one basically mesodermal and related to the "somatic" animal, the other basically endodermal, "visceral" in origin – have any necessary relationship to one another."
The authors of all mesodermal segmental models, as well as the earlier critics of these models (Kingsbury 1926; Romer 1972), accepted Marshall's initial claim (1881) that branchiomeric muscles arise from lateral plate mesoderm. If this were true, however, branchiomeric muscles should consist of smooth muscle fibers, not striated muscle fibers, and these muscles should be innervated in the same manner as gut muscle, by first and second order visceral motor neurons. Only Romer (1972) addressed the discrepancy of muscle type by arguing that branchiomeric muscles were striated due to "the functional need for more efficient musculature in the mouth and pharynx region." Amazingly, the differences in the innervation patterns of smooth and striated muscle were already known (Gaskell 1886; Langley 1893) at the time that Goodrich formulated his head segmentation model in 1918, but no attempt was ever made by any of the authors of the mesodermal segmental models to account for this discrepancy in innervation.
Fortunately, the discrepancy in muscle type was resolved experimentally in 1983 when Noden transplanted segments of paraxial head mesoderm between quail and chick embryos and demonstrated that branchiomeric muscles arise from paraxial mesoderm, not lateral plate mesoderm. This seminal observation not only substantially altered all mesodermal segmental models but also negated Romer's "dual animal" model and blunted much of Kingsbury's arguments concerning the independent segmentation of paraxial and lateral plate mesoderm. Although Noden's experiments also explain the way in which branchiomeric muscles are innervated, they do not address the issue raised by Kingsbury (1926) and Northcutt (1993) of the claimed alignment of cranial nerves and paraxial mesoderm. This issue will be considered in the next section on neuroepithelial segmental hypotheses.
Neuroepithelial segmental hypotheses
The cephalic neural tube in vertebrate embryos exhibits a series of transitory transverse ridges, termed neuromeres, which are separated by furrows. These neural segments have been interpreted as additional evidence of head segmentation (Locy 1895; Neal 1898, 1918; Vaage 1969). After their initial discovery, and a brief period in which neuromeres were extensively described in many vertebrates, they were generally afforded less significance and were believed to be artifacts, due to histological fixation, or localized swellings of the neural tube, due to stress points where nerve roots enter or exit the brain, or a reflection of localized neuronal migration. The lack of agreement on their number, reported to be between 4 and 15 (Neal 1898), further reinforced the notion that they were neural artifacts. Thus, Goodrich (1930) and Bjerring (1984) did not even mention neuromeres, and Jarvik (1980) dismissed them as having no significance for the understanding of head organization.
It was not until Lumsden and Keynes (1989) revived Neal's earlier (1898, 1918) claim that most cranial motor nuclei arise from adjacent pairs of neuromeres, and experimentally confirmed this claim, and the discovery that hindbrain neuromeres, termed rhombomeres, are determined by the Hox genes (reviewed by Wilkinson and Krumlauf 1990), that neuromeres came to be regarded as critical elements in the development of the brain and thus important to our understanding of the organization of the head (Noden 1991; Gilland and Baker 1993; Northcutt 1993). In addition, the discovery that the expression patterns of an extensive series of developmental genes allow recognition of midbrain and forebrain segments (reviewed by Puelles and Rubenstein 1993, 2003) has allowed a resolution of most of the discrepancies regarding the number and extent of the more rostral neuromeres.
At present, the most widely accepted neuromeric model (Puelles and Rubenstein 2003) recognizes that the hindbrain consists of an isthmus (r0), seven distinct additional rhombomeres, and two or three pseudorhombomeres, which have many of the cellular and histochemical patterns of the more rostral rhombomeres but are not delineated by distinct sulci (Fig. 5). The midbrain appears to consist of a single neuromere, termed the mesomere (Fig. 5). The forebrain consists of four segments: a pretectum (p1), a dorsal thalamus (p2), a ventral thalamus or prethalamus (p3), and a prechordal segment, the secondary prosencephalon, which consists of the hypothalamus, the optic vesicle, and the telencephalon (Fig. 5).
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The neuromeric origin of the motor neurons of the cranial nerves has been experimentally determined in a number of species (Lumsden and Keynes 1989
; Gilland 1992; Gilland and Baker 1993), and the segmental locations of these efferent neurons are generally conserved. The oculomotor and trochlear motor neurons arise in the mesomere and the isthmic rhombomere (r0), respectively (Fig. 5). The origin of the abducent motor neurons is varied, as these neurons may arise only in rhombomere 5 (mammals), only in rhombomere 6 (elasmobranchs), or in both rhombomeres 5 and 6 (teleosts and birds). In contrast, the motor neurons of the hypoglossal cranial nerve appear to arise within pseudorhombomere 8 in all vertebrates that have been examined. The motor neurons of the branchiomeric cranial nerves generally have been described as arising from neuromeric pairs. Thus, the motor neurons of the trigeminal and facial cranial nerves arise from rhombomeres 2 and 3, and 4 and 5, respectively in most vertebrates that have been examined. Similarly, the motor neurons of the glossopharyngeal cranial nerve arise from rhombomeres 6 and 7 (Fig. 5). In mammals, however, both the trigeminal and facial motor nuclei each arise from three neuromeres (Gilland and Baker 1993). The trigeminal motor neurons arise from caudal rhombomere 1, as well as rhombomeres 2 and 3, and the facial motor nucleus arises from rhombomeres 4 and 5, as well as rhombomere 6. There is also variation in the neuromeric origin of vagal motor neurons. These neurons arise from rhombomeres 7 and 8 in most vertebrates, but in Squalus they appear to arise only from rhombomere 8.
Clearly, both the cephalic neural tube and the cephalic paraxial mesoderm form iterative units, but are the two series aligned? Neal (1918) concluded that they were, and he believed there was embryological evidence that both the brain and the paraxial mesoderm were divided into seven segments, which were aligned. He believed that the forebrain arose from the first neuromere and was aligned with the premandibular somite (head cavity). The midbrain was believed to arise from the second neuromere and to be aligned with the mandibular somite (head cavity). Neal's third neuromere was subdivided to form rhombomeres 1 and 2, which were aligned with the hyoid somite (head cavity). Finally, neuromeres 4 through 7 (rhombomeres 3 through 6) were aligned with his somites 4 through 7. Neal's model is not supported, however, by the neuromeric model of Puelles and Rubinstein (2003), which is based heavily on the expression of a number of developmental genes for recognition of individual neuromeres and their boundaries. This new model suggests that the brain is divided into at least 14 neuromeres, which can not be aligned with the recognized paraxial mesodermal subdivisions (Fig. 5) or with Goodrich's model of eight head segments (Fig. 4). In fact, in amniotic embryos the paraxial mesoderm is not divided at all. Whereas the cephalic paraxial mesoderm in many anamniotic embryos is clearly divided into a series of epithelial head cavities, the cephalic paraxial mesoderm in amniotic embryos is only partially constructed, at best, into units that have been termed somitomeres (see Jacobson 1993, for an extensive review). Those researchers who have recognized somitomeres have reported them in varying numbers in different vertebrate groups. What is notable is that somitomeres, if they exist at all, do not exist in sufficient number to be in registry with 14 neuromeres.
Furthermore, the origin and distribution of the cranial nerves do not support van Wijhe's (1882) contention that these nerves correspond to the dorsal and ventral spinal nerves of lampreys, a position that was also adopted in Goodrich's model (1918, 1930). In 1882, van Wijhe examined the development of the spinal and cranial nerves of Scyliorhinus and concluded that the spinal nerves, as well as most of the cranial nerves, initially develop as separate dorsal and ventral nerves. Subsequently, the spinal nerves were said to fuse, except in lampreys, where separate dorsal and ventral spinal nerves were said to be retained. Based on these observations, van Wijhe concluded that most of the cranial nerves constitute pairs of dorsal and ventral nerves that do not fuse, and he argued that all cranial nerves can be grouped into three series: (1) special sensory nerves of the paired sense organs; (2) a dorsal series of nerves (profundal, trigeminal, facial, glossopharyngeal, and vagal); and (3) a ventral series of nerves (oculomotor, trochlear, abducent, and hypoglossal). Over the next 40 years, the distribution of the sensory and motor components of these nerves was established (Strong 1895; Cole 1896; Allis 1897; Herrick 1899; Norris and Hughes 1920), and it was noted that many, if not all, of the dorsal cranial nerves contain sensory fibers that innervate lateral line and gustatory organs. These fibers were interpreted as specialized somatic components (innervating the lateral line organs) and specialized visceral components (innervating the gustatory organs), which were retained in the dorsal cranial nerves but lost in the dorsal spinal nerves (Strong 1895). Although this view became predominant (Goodrich 1930; Romer 1970; Jarvik 1980), at least two researchers (Pollard 1892 and Cole 1896) noted that lateral line organs are innervated by sensory fibers whose cell bodies form ganglia distinctly separate from those of the dorsal cranial nerves and proposed that the cranial nerves innervating lateral line organs should be considered a separate series of nerves. Furthermore, comparative embryological studies (Landacre and Conger 1913; Stone 1922; Northcutt and Brändle 1995; O’Neill et al. 2007) have demonstrated that these nerves and their organs arise from a series of cephalic dorsolateral placodes. Today, there is substantial evidence that six pairs of lateral line nerves are derived from these placodes (Song and Northcutt 1991; Northcutt and Bemis 1993; Northcutt and Brändle 1995) and form an additional series of cranial nerves.
The sensory ganglia of spinal nerves arise only from the neural crest, whereas many sensory ganglia of the "dorsal" cranial nerves arise from epibranchial placodes as well as the neural crest. The epibranchial placodes are a series of ectodermal thickenings located dorsally adjacent to the pharyngeal slits, which are induced by the pharyngeal endoderm (Begbie et al. 1999; Matz and Northcutt 1999) and are believed to innervate taste buds (Gross et al. 2003). Sensory neurons that arise from these placodes contribute to the geniculate ganglion of the facial cranial nerve and form the separate distal sensory ganglia of the glossopharyngeal and vagal nerves. While the glossopharyngeal nerve exhibits only a single distal, epibranchially derived sensory ganglion, the vagal nerve is frequently characterized by four distal, epibranchially derived sensory ganglia. It is possible that these gustatory sensory ganglia, like the sensory ganglia of the lateral line nerves, are evidence that vertebrates originally possessed a separate series of six gustatory cranial nerves that have secondarily become associated with the neural crest derived sensory ganglia of the "dorsal" cranial nerves (Northcutt 1990; Butler and Hodos 1996). If so, most anamniotic vertebrates actually possess 25 pairs of cranial nerves, (the terminal nerve, the 12 traditionally recognized cranial nerves, 6 lateral line nerves, and 6 gustatory nerves) a number that cannot be accommodated by any single existing segmental model of the vertebrate head.
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Research over the past 200 years has resulted in a wealth of information on the organization of the vertebrate body plan. Many of the evolutionary steps leading to the emergence of this body plan—which is impacted by the neural crest, neurogenic placodes, and the muscularization of lateral plate mesoderm—have been elucidated, and during the past 20 years, there has been remarkable progress in understanding the genetic framework for the developmental basis of this body plan. Unfortunately, all segmental hypotheses for explaining this plan have proven inadequate so far. There is no question that the vertebrate head consists of a large number of iterative structures, involving the brain, neurogenic placodes, and paraxial mesoderm, but there is no obvious alignment of these cephalic serial structures. Such alignment must exist for there to be any possibility that the vertebrate head is segmented (i.e., metameric). Even if an alignment were discovered, this would not necessarily demonstrate segmentation. Such demonstration would also require the discovery of genetic mechanisms that underlie and conserve the registration of neuromeres, paraxial subdivisions, pharyngeal pouches, and neurogenic placodes. To paraphrase Huxley (1858
), no existing theory, and perhaps no future theory, will, even after many summer days, demonstrate head segmentation in vertebrates. |
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I thank Shigeru Kuratani and Thomas Schilling for inviting me to participate in their symposium on vertebrate head segmentation. I also thank Jo Griffith for assistance with the illustrations, Susan Commerford for literature retrieval and word processing, and Mary Sue Northcutt for assistance with numerous phases of the research and preparation of the manuscript. This research was supported, in part, by the National Science Foundation (IBN-0236018).
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From the symposium "Vertebrate Head Segmentation in a Modern Evo-Devo Context" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 2–6, 2008, at San Antonio, Texas.
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