Biology subjects

Suzuki, D. G.

Publications and source records attributed to Suzuki, D. G..

5 recordsLinked to original sources

bioRxiv2025

Three-dimensional and molecular brain atlas of the hagfish reveals the evolutionary origin and early diversification of the vertebrate brain

Hagfish and lampreys form the clade cyclostomes, the earliest branching lineage of the vertebrates. Although hagfish are generally assumed to have experienced intense modifications, its brain development shows certain ancestral patterns that are secondarily lost in the lamprey. Therefore, hagfish provides key insights into the evolutionary origin and early diversification of the vertebrate brain. However, neuroanatomical information of the hagfish brain is substantially limited today due to its sources based on old-fashioned methodology alone. Here, we provide a detailed brain atlas of the adult hagfish, based on three-dimensional reconstruction and expression analysis of genetic markers for major neuronal transmitters. Through our analyses, we found the following key characteristics. First, the dopaminergic system appears to be distributed more broadly than previously thought in the hagfish brain, implying that dopamine is involved in various neural functions. Second, the previously suggested "primordial cerebellum" area in hagfish shows notable affinity to the cerebellum-like octavolateral structures of the jawed vertebrate hindbrain. Last, the gene expression profile suggests a hippocampus-equivalent brain region in hagfish, that is, the ventrolateral subnucleus of the central prosencephalic complex (NCvl). This study highlights conserved and diversified neuroarchitecture of the hagfish brain, providing a pivotal reference for further studies.

evolutionary biology↗

bioRxiv2025

Genome-wide and gene expression analyses of the hagfish olfactory receptors illuminate lineage-specific diversification of olfaction in basal vertebrates

Olfactory receptors (ORs) of vertebrates have undergone remarkable diversification, but the ancestral repertoire remains incompletely understood. Here, we present a comprehensive genome-wide survey and gene expression analyses of OR genes in hagfish, a cyclostome group that typically inhabits the deep sea with a well-developed olfactory system. We identified 48 main olfactory receptors (mORs), two vomeronasal type 1 receptors (V1Rs), 135 typical vomeronasal type 2 receptors (V2Rs), and no trace amine-associated receptors (TAARs) in the inshore hagfish (Eptatretus burgeri). Notably, V2Rs were highly clustered on a single scaffold, suggesting tandem gene duplications as the main mechanism of diversification. Transcriptome analysis confirmed that most of these OR genes are expressed predominantly in the olfactory organ. Using in situ hybridization, we further confirmed that at least some of these genes are expressed in olfactory receptor cells. These gene expression analyses support the role of these genes as functional ORs. Our findings challenge the prevailing view that typical olfactory V2Rs originated in gnathostomes and instead suggest that they were present in the common ancestor of all vertebrates but were lost in lampreys. The extensive diversification of V2Rs in hagfish likely reflects adaptations to life in low-light and chemically complex environments. This study highlights the evolution of vertebrate sensory systems in a mosaic manner, underscoring the importance of hagfish as a key animal for reconstructing the evolutionary history of early vertebrates. Graphical abstract O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=200 SRC="FIGDIR/small/666228v2_ufig1.gif" ALT="Figure 1"> View larger version (42K): org.highwire.dtl.DTLVardef@ba336borg.highwire.dtl.DTLVardef@85b62corg.highwire.dtl.DTLVardef@7b23ccorg.highwire.dtl.DTLVardef@6b2b74_HPS_FORMAT_FIGEXP M_FIG C_FIG Highlights- Genomic and expression analyses reveal hagfish olfactory receptor repertoire. - V2Rs are extensively diversified in hagfish. - The olfactory function of V2Rs is traced back to the common ancestor of vertebrates. - The olfactory receptor repertoires of basal vertebrates underwent mosaic evolution.

evolutionary biology↗

bioRxiv2025

Whole-mount acetylcholinesterase (AChE) staining reveals unique motor innervation of the lamprey oral region: with special reference to the evolutionary origin of the vertebrate jaw

The evolutionary change of the trigeminal nerve-innervation pattern is essential to reveal the mechanism underlying jaw acquisition. However, the homology of the branches between gnathostomes (jawed vertebrates) and cyclostomes (living jawless vertebrates) remains unclear. In this study, we focused on a sub-branch called the ramus subpharyngeus, which belongs to the second branch of the lamprey trigeminal nerve and projects to the lower lip, investigating whether it contains motor components. To visualize motor fibers, we performed acetylcholinesterase (AChE) staining, a histochemical method that visualizes intrinsic activities of the catabolic enzymes produced by motor neurons and muscle fibers. As a result, we found AChE staining signals that correspond to the innervation course of the ramus subpharyngeus. To confirm that the signals are not produced by the motoneuronal somata nor muscle fibers, we conducted gene expression analysis by in situ hybridization. The results support that the signals mark the motor fibers. Based on these results, we propose that the lamprey oral apparatus is chiefly controlled by the second (i.e., pre-mandibular) branch of the trigeminal nerve and further suggest that a drastic reorganization of the anterior craniofacial region occurred during the acquisition of the vertebrate jaw.

developmental biology↗

bioRxiv2023

Functional development of eye movements and visuomotor circuits in lampreys

Animals constantly redirect their gaze away or towards relevant targets and, besides these goal-oriented responses, stabilizing movements clamp the visual scene avoiding image blurring. The vestibulo-ocular (VOR) and the optokinetic reflexes are the main contributors to gaze stabilization, whereas the optic tectum integrates multisensory information and generates orienting/evasive gaze movements in all vertebrates. Lampreys show a unique stepwise development of the visual system whose understanding provides important insights into the evolution and development of vertebrate vision. Although the developmental emergence of the visual components, and the retinofugal pathways have been described, the functional development of the visual system and the development of the downstream pathways controlling gaze are still unknown. Here, we show that VOR followed by light-evoked eye movements are the first to appear already in larvae, despite their burrowed lifestyle. However, the circuits controlling goal-oriented responses emerge later, in larvae in nonparasitic lampreys but during late metamorphosis in parasitic lampreys. The appearance of stabilizing responses earlier than goal-oriented likely reflects their evolution, and its stepwise emergence offers a unique opportunity to isolate the functioning of their underlying circuits.

neuroscience↗

bioRxiv2022

Gross anatomy of the Pacific hagfish, Eptatretus burgeri, with special reference to the coelomic viscera

Hagfish (Myxinoidea) are a deep-sea taxon of cyclostomes, the extant jawless vertebrates. Many researchers have examined the anatomy and embryology of hagfish to shed light on the early evolution of vertebrates; however, the diversity within hagfish is often overlooked. Hagfish have two lineages, Myxininae and Eptatretinae. Usually, textbook illustrations of hagfish anatomy reflect the morphology of the former lineage, especially Myxine glutinosa, with its single pair of external branchial pores. Here, we instead report the gross anatomy of an Eptatretinae, Eptatretus burgeri, which has six pairs of branchial pores, especially focusing on the coelomic organs. Dissections were performed on fixed and unfixed specimens to provide a guide for those doing organ- or tissue-specific molecular experiments. Our dissections revealed that the ventral aorta is Y-branched in E. burgeri, which differs from the unbranched morphology of Myxine. Otherwise, there were no differences in the morphology of the lingual apparatus or heart in the pharyngeal domain. The thyroid follicles were scattered around the ventral aorta, as has been reported for adult lampreys. The hepatobiliary system more closely resembled those of jawed vertebrates than those of adult lampreys, with the liver having two lobes and a bile duct connecting the gallbladder to each lobe. Overall, the visceral morphology of E. burgeri does not differ significantly from that of the known Myxine at the level of gross anatomy, except for the number of branchial pores.

zoology↗