Morphology of the trigeminal nerve. a Total immunofluorescence for arctic lamprey (L. camtschaticum) prolarva at st. 27. Peripheral nerves are visualized by acetylated anti-tubulin antibody in green and cell nuclei are labeled DAPI in blue. b Schematic illustration of the cranial nerves. c Complete immunofluorescence for catshark (S. torazame) embryo in st. 27. Peripheral nerves are visualized by an acetylated anti-tubulin antibody in magenta and cell nuclei are marked by DAPI in blue. d Schematic illustration of the cranial nerves. Credit: Tamura et al. (Zoological Letters, 2023).
Jaws are bone or cartilage-based structures that hold teeth together in the mouths of most vertebrates (i.e., all animal species with a backbone or backbone ). Although these crucial structures have been the subject of numerous studies, their evolutionary origin and their development over the centuries and from one species to another still remain to be elucidated.
With their strong and highly efficient jaws, sharks are one of the most iconic animal species. Shark jaws are known to be partly flexible, allowing the animals, for example, to bite off parts of their prey when they are too large for them to swallow, via a pushing motion.
Researchers from Tsukuba University, Ehime University and other institutes in Japan and Europe recently conducted a study examining a crucial component of the vertebrate jaw, known as the trigeminal nerve. Their article, published in Zoological lettersidentifies unique patterns in the distribution of neuronal somata and expression of so-called Hmx genes in the lamprey (also known as vampire fish), which were not present in sharks.
“The trigeminal nerve is a key component in understanding jaw evolution, as it plays a crucial role as a sensorimotor interface for efficient manipulation of the jaw,” wrote Motoki Tamura, Ryota Ishikawa and colleagues in their article.
“This nerve is also found in the lamprey, an extant jawless vertebrate. The trigeminal nerve has three main branches in the lamprey and in jawed vertebrates. Although each of these branches has classically been considered homologous between these two taxa, this homology is now in doubt.”
The trigeminal nerve or fifth cranial nerve (V) is a key component of the vertebrate jaw, composed of both motor and sensory neurons. As its name suggests, this nerve is typically made up of three distinct branches, namely the ophthalmic, maxillary and mandibular nerves.
Interestingly, the lamprey, a blood-sucking, eel-like fish with sharp teeth but no clear jaw-like structure, also has a trigeminal nerve. The presence of this jawless nerve suggests that this fish species evolved differently from sharks, which are known to have a conventional vertebrate jaw.
In their paper, Tamura, Ishikawa and their colleagues sought to better understand the differences in the neuronal somata and gene expression patterns of lamprey and sharks. To do this, they examined the distribution of trigeminal sensory neurons in these two animals, as well as the expression patterns of Hmx genes, linked to the development of the nervous system and sensory organs.
Notably, previous studies in mice revealed that the Hmx1 gene was expressed in a specific segment of neurons, called rV.3 neuronal somata. The team attempted to determine whether these same gene expression patterns were also present in sharks and lampreys.
“We compared the expression profiles of Hmx, a candidate genetic marker of the mandibular nerve (rV3the third branch of the trigeminal nerve in jawed vertebrates), and the distribution of neuronal somata of the trigeminal nerve branches in the trigeminal ganglion in the lamprey and shark,” Tamura, Ishikawa and their colleagues wrote.
“We first confirmed the conserved expression pattern of Hmx1 in the shark rV3 neuronal somata, which are distributed in the caudal part of the trigeminal ganglion. In contrast, lamprey Hmx genes showed peculiar expression patterns, with expression in the ventrocaudal part of the trigeminal ganglion similar to Hmx1 expression in jawed vertebrates, which labeled the neuronal somata of the second branch.
Overall, the researchers found that while the Hmx expression patterns and distribution of trigeminal nerve neurons in sharks resembled those previously observed in mice, those in lampreys were markedly different. Based on these observations, they introduced two alternative hypotheses describing the possible evolutionary path of the branches of the trigeminal nerve.
The results collected in this study offer new insights into the evolutionary origins of the vertebrate jaw, which remain poorly understood. In the future, they could pave the way for further work exploring the differences between the trigeminal nerve of sharks and lampreys, potentially leading to important new discoveries.
More information:
Motoki Tamura et al, Comparative analysis of Hmx expression and neuronal somata distribution in the trigeminal ganglion in lamprey and shark: insights into the homology of trigeminal nerve branches and the evolutionary origin of the jaw vertebrates, Zoological letters (2023). DOI: 10.1186/s40851-023-00222-9.
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