On the peculiar morphology and development of the hypoglossal, glossopharyngeal and vagus nerves and hypobranchial muscles in the hagfish

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.