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On the Peculiar Morphology and Development of the Hypoglossal, Glossopharyngeal and Vagus Nerves and Hypobranchial Muscles in the Hagfish

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On the Peculiar Morphology and Development of the Hypoglossal, Glossopharyngeal and Vagus Nerves and Hypobranchial Muscles in the Hagfish

Yasuhiro Oisi et al. Zoological Lett.

Abstract

Introduction: The vertebrate body is characterized by its dual segmental organization: pharyngeal arches in the head and somites in the trunk. Muscular and nervous system morphologies are also organized following these metameric patterns, with distinct differences between head and trunk; branchiomeric nerves innervating pharyngeal arches are superficial to spinal nerves innervating somite derivatives. Hypobranchial muscles originate from rostral somites and occupy the "neck" at the head-trunk interface. Hypobranchial muscles, unlike ventral trunk muscles in the lateral body wall, develop from myocytes that migrate ventrally to occupy a space that is ventrolateral to the pharynx and unassociated with coelomic cavities. Occipitospinal nerves innervating these muscles also extend ventrally, thereby crossing the vagus nerve laterally.

Results: In hagfishes, the basic morphological pattern of vertebrates is obliterated by the extreme caudal shift of the posterior part of the pharynx. The vagus nerve is found unusually medially, and occipitospinal nerves remain unfasciculated, appearing as metameric spinal nerves as in the posterior trunk region. Moreover, the hagfish exhibits an undifferentiated body plan, with the hypobranchial muscles not well dissociated from the abaxial muscles in the trunk. Comparative embryological observation showed that this hagfish-specific morphology is established by secondary modification of the common vertebrate embryonic pattern, and the hypobranchial muscle homologue can be found in the rostral part of the oblique muscle with pars decussata.

Conclusion: The morphological pattern of the hagfish represents an extreme case of heterotopy that led to the formation of the typical hypoglossal nerve, and can be regarded as an autapomorphic trait of the hagfish lineage.

Keywords: Agnathans; Cranial nerves; Cyclostomes; Embryo; Evolution; Hagfish; Hypobranchial muscles.

Figures

Figure 1
Figure 1
Anatomical configuration of the putative “neck” region of the hagfish. (A) Left lateral view of an adult hagfish, Myxine garmani, originally drawn by Nishi (1938). (B) A schematized illustration showing the innervating pattern of a spinal nerve in a transverse section of a hagfish, Bdellostoma dombeyi. Redrawn from [22]. The arrow indicates the ventral branch that extends ventrally to innervate the oblique and rectus muscles. (C) Dorsal view of the oblique and rectus muscles together with the skin (sk) in M. glutinosa. (D) Dorsal view of a dissected head of M. glutinosa showing the morphological patterns of the nervous system (yellow). Note that the spinal nerves (sp1–3) are located dorsolateral to the branchiomeric nerve components: the glossopharyngeal (IX) and vagus (X) nerves. Light blue indicates cranial cartilage. (C) and (D) are redrawn from [15].
Figure 2
Figure 2
Mid- to late pharyngular-stage embryos of Eptatretus burgeri . (A–C) Left lateral views of 3D-reconstructed embryos at stages 45, 50, and 53. Pharyngeal endoderm is colored yellow and the arterial system is colored red. The light blue color beneath the brain primordia represents oronasal ectodermal derivatives (for details, see [10]). Note that the caudal half of the pharynx shifts caudally by the expansion of the pharyngeal arch 3 and 4 domain. (D–F) Reconstructions of embryos at stages 40, 50, and 53, with Tbx1/10A-positive mesodermal components (colored pink) as well as somites (sm). Note that somites initially arise caudal to the entire pharynx at stage 40, and later shift rostrally to reach the mid-otic level (F).
Figure 3
Figure 3
Mid to late pharyngular-stage embryos of Eptatretus burgeri . (A–C) Dorsal views of embryos at stages 45, 50, and 53, with the brain and notochord made transparent mainly to visualize the relative positions between pharynx (yellow), otic vesicle (ot) and somites. Dorsal root ganglia of spinal nerves (sp) are shown in orange, medial to the somites. (D–F) Development of the peripheral nerves in the same embryo as shown in A–C. Cranial nerves are shown by different colors. In this reconstruction, the glossopharyngeal and vagus nerves (green) are not always easy to distinguish from each other. Note that, as with the development of the somites, the spinal nerves first arise caudal to the pharynx and later shift rostrally to the mid-otic level at stage 53. (G, H) Reconstructions of the spinal nerves in the head (originally the right side) (G) and rostral part the body (head and pharynx; H) of a pre-hatching–stage E. atami embryo. Spinal nerves are colored orange. Note that in the head the rostral spinal nerves (putative occipitospinal nerves) pass superficial to the branchiomeric nerves, as does the hypoglossal nerve in other vertebrates.
Figure 4
Figure 4
Developmental changes in the morphology and topography of coelomic cavities. (A) 3D-reconstructed stage-50 embryo of Eptatretus burgeri showing the position of the coelomic cavity (dark pink). Light pink indicates Tbx1/10A-positive myoblasts in pharyngeal arches. The coelomic cavity consists of the pericardium and peritoneal cavity, which are well defined and separate from each other at the caudal end of the pharynx. This morphology represents the generalized configuration of the coelomic cavity in vertebrate embryos. (B, C) Left lateral (B) and left caudal (C) views of a stage-53 embryo. Note that the junction between the pericardium (pc) and peritoneal cavity (pnc) corresponds to the level of the 10th pharyngeal pouch (p10) or the caudal end of the posteriorly shifted pharynx. (D) Parasagittal section showing the pharyngeal-pericardial region. (E) The same section as C at higher magnification. Note that the pronephros (pneph) is constantly found in the rostral part of the peritoneal cavity, and caudal to the pharynx. (F, G) Two transverse sections cut at the levels shown in B, reconstructed from serial parasagittal sections of the stage-53 embryo showing the pericardium (pc in E) and peritoneal cavity (pnc in F). (H) Reconstruction of a stage-53 E. burgeri embryo showing the developmental pattern of the venous system (purple). (I, J) Parasagittal sections of a stage-53 E. burgeri embryo (I) and a pre-hatching–stage E. atami embryo (J) showing the peribranchial venous system. Note that the venous system expands to form a sinus surrounding the gill pouches of the pre-hatching stage, just like a peribranchial coelom.
Figure 5
Figure 5
Histological observations of hagfish muscle development. (A) Transverse section of a stage-53 Eptatretus burgeri embryo, cut at the posterior trunk level. Expression of MyHCA was detected by in situ hybridization. This gene was strongly expressed in the myotomal muscle plates (=precursor of the parietal muscles, m.par), and relatively weakly expressed in the abaxial muscles (m.dec + m.rect). (B) A transverse section adjacent to A, showing the expression of HandA, a marker of lateral plate-derived mesenchyme. HandA-expressing cells were predominantly located in the lateral body wall (arrowheads). (C) Reconstruction of a stage-53 embryo of E. burgeri showing the level of the section in D. (D) A transverse section cut at line D in C, showing the relationship between the parietal muscle anlage and the hypobranchial muscle anlage (m.obl + m.rect).
Figure 6
Figure 6
Development of hypobranchial muscles. Stage-53 (A–C) and stage-60 (D–F) embryos of Eptatretus burgeri reconstructed to show development of the putative hypobranchial (and abaxial) muscles in the hagfish; left lateral (A), right lateral (D), medial (B, E) and ventral (C, F) views. At stage 53 (A-C), the rostral part of the common anlage for oblique and rectus muscle (m.obl + m.rect) is arising from the ventrolateral edge of myotomes (anlage of parietal muscles, m.par) to grow ventrally into the superficial layer of the hagfish “neck”, appearing as the basal part of the hypoglossal cord in other vertebrate embryos. The epithelial cord (colored blue) indicates the anlage of the mucous gland (mg). At stage 60 (D-F), the parietal and hypobranchial muscles surround the entire pharyngeal basket laterally (E), and only the gill pores penetrate the muscle to the exterior (D). Mucous glands also develop external ducts that penetrate the hypobranchial muscle in a segmental pattern that does not correlate with that of myotomes (D).
Figure 7
Figure 7
Comparative morphology of the hagfish. A: Differences in anatomical patterns between the hagfish and other vertebrates. Generally in vertebrates, hypoglossal or occipitospinal nerves (XII) pass along the posterior edge of the pharynx, and when the accessory nerve (XI) is present, nerve XII passes medial to nerve XI and lateral to the vagus nerve (X) to innervate the hypobranchial muscles (hbm). Thus nerve XII does not pass within the lateral body wall. In the hagfishes, putative hypobranchial muscle is assumed to arise in the rostral part of the ventral muscle that continues posteriorly into the rectus muscle in the trunk. Here, nerve XII does not form a single nerve trunk, but segmental occipitospinal nerves are shifted rostrally and no longer circumvent the pharynx caudally. However, this nerve still lies in the neck lateral to nerve X, as seen in the lampreys and gnathostomes. This peculiar morphology in the hagfish is thought to be due to a secondary modification of embryonic development, which is regarded as an autapomorphy for the hagfish. B: Homology of the hypobranchial muscle in the hagfish. The ventral somitic muscles of the hagfish can be seen as ventrally overgrown Lbx1-positive somitic muscles (dark green) in the larval lamprey. In the hagfish scheme, the pars decussata on the contralateral side is flipped back to the original (left) side of the body, and suspended ventrally. On the basis of this similarity, the homologue of the hypobranchial muscle is identified in the rostral oblique muscle with pars decussata in the hagfish.

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