The evolutionary origins and diversity of the neuromuscular system of paired appendages in batoids

Appendage patterning and evolution have been active areas of inquiry for the past two centuries. While most work has centred on the skeleton, particularly that of amniotes, the evolutionary origins and molecular underpinnings of the neuromuscular diversity of fish appendages have remained enigmatic. The fundamental pattern of segmentation in amniotes, for example, is that all muscle precursors and spinal nerves enter either the paired appendages or body wall at the same spinal level. The condition in finned vertebrates is not understood. To address this gap in knowledge, we investigated the development of muscles and nerves in unpaired and paired fins of skates and compared them to those of chain catsharks. During skate and shark embryogenesis, cell populations of muscle precursors and associated spinal nerves at the same axial level contribute to both appendages and body wall, perhaps representing an ancestral condition of gnathostome appendicular neuromuscular systems. Remarkably in skates, this neuromuscular bifurcation as well as colinear Hox expression extend posteriorly to pattern a broad paired fin domain. In addition, we identified migratory muscle precursors (MMPs), which are known to develop into paired appendage muscles with Pax3 and Lbx1 gene expression, in the dorsal fins of skates. Our results suggest that muscles of paired fins have evolved via redeployment of the genetic programme of MMPs that were already involved in dorsal fin development. Appendicular neuromuscular systems most likely have emerged as side branches of body wall neuromusculature and have been modified to adapt to distinct aquatic and terrestrial habitats.

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The evolutionary origins and diversity of the neuromuscular system of paired appendages in batoids

10.1101/644062 ◽

2019 ◽

Author(s):

Natalie Turner ◽

Deimante Mikalauskaite ◽

Krista Barone ◽

Kathleen Flaherty ◽

Gayani Senevirathne ◽

...

Keyword(s):

Body Wall ◽

Spinal Nerves ◽

The Past ◽

Evolutionary Origins ◽

Neuromuscular Systems ◽

Terrestrial Habitats ◽

Fundamental Pattern ◽

Migratory Muscle Precursors ◽

Fin Development ◽

Appendage Patterning

AbstractAppendage patterning and evolution have been active areas of inquiry for the past two centuries. While most work has centered on the skeleton, particularly that of amniotes, the evolutionary origins and molecular underpinnings of the neuromuscular diversity of fish appendages have remained enigmatic. The fundamental pattern of segmentation in amniotes, for example, is that all muscle precursors and spinal nerves enter either the paired appendages or body wall at the same spinal level. The condition in finned vertebrates is not understood. To address this gap in knowledge, we investigated the development of muscles and nerves in unpaired and paired fins of skates and compared them to those of chain catsharks. During skate and shark embryogenesis, cell populations of muscle precursors and associated spinal nerves at the same axial level contribute to both appendages and body wall, perhaps representing an ancestral condition of gnathostome appendicular neuromuscular systems. Remarkably in skates, this neuromuscular bifurcation as well as colinear Hox expression extend posteriorly to pattern a broad paired fin domain. In addition, we identified migratory muscle precursors (MMPs), which are known to develop into paired appendage muscles with Pax3 and Lbx1 gene expression, in the dorsal fins of skates. Our results suggest that muscles of paired fins have evolved via redeployment of the genetic program of MMPs that were already involved in dorsal fin development. Appendicular neuromuscular systems most likely have emerged as side branches of body wall neuromusculature and have been modified to adapt to distinct aquatic and terrestrial habitats.

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Acupuncture Points of the Typical Spinal Nerves

The American Journal of Chinese Medicine ◽

10.1142/s0192415x85000083 ◽

1985 ◽

Vol 13 (01n04) ◽

pp. 39-47 ◽

Cited By ~ 8

Author(s):

H.C. Dung

Keyword(s):

Body Wall ◽

Acupuncture Point ◽

The Body ◽

Acupuncture Points ◽

Spinal Nerves ◽

Thoracic And Abdominal

Typical spinal nerves have six cutaneous branches which reach to the skin of the body wall in the thorax and abdomen. Each of these six cutaneous branches correlates to an acupuncture point. This communication describes acupuncture points found in the thoracic and abdominal walls using anatomic nomenclature relating to cutaneous branches of the spinal nerves.

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Acupuncture Points of the Lumbar Plexus

The American Journal of Chinese Medicine ◽

10.1142/s0192415x85000186 ◽

1985 ◽

Vol 13 (01n04) ◽

pp. 133-143 ◽

Cited By ~ 6

Author(s):

H.C. Dung

Keyword(s):

Body Wall ◽

Lumbar Plexus ◽

Acupuncture Points ◽

Lumbar Region ◽

Lower Abdomen ◽

Spinal Nerves ◽

Medial Surface ◽

Anatomic Basis ◽

Lumbar Spinal

This communication is the fifth in a series of six publications describing acupuncture points by anatomic nomenclature. This article describes acunpuncture points in the lumbar region of the posterior body wall, the inguinal and pelvic regins of the lower abdomen, and the medial surface of the thigh and leg. Acunpuncture points in these regions are generally established by anatomic features of the lumbar spinal nerves. Nerve branches of the posterior primary rami of the lumbar spinal nerves and the lumbar plexus provide the anatomic basis for acunpuncture points in these regions and are used to name the points accordingly.

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The Spinal Nerves of the Dogfish (Scyliorhinus)

Journal of the Marine Biological Association of the United Kingdom ◽

10.1017/s0025315400046415 ◽

1969 ◽

Vol 49 (1) ◽

pp. 51-75 ◽

Cited By ~ 23

Author(s):

B. L. Roberts

Keyword(s):

Body Wall ◽

Subcutaneous Tissue ◽

Muscle Spindles ◽

Motor Innervation ◽

Spinal Nerves ◽

Nerve Bundles ◽

Spinal Roots ◽

Tendon Organs ◽

Physiological Isolation ◽

Sensory Endings

The locomotory musculature of dogfish is innervated by the segmental spinal nerves. The sensory and motor innervation of the abdominal musculature was studied in a preparation consisting of a strip of the abdominal body wall innervated by the ventral rami of the spinal nerves.Each ventral ramus consists of two separate nerve bundles which were found to be peripheral extensions of the dorsal and ventral spinal roots. Recordings from the sensory bundles showed that there are few sensory endings in the musculature and body wall of the dogfish. It was possible to differentiate between ephemeral responses produced by cutaneous free-nerve endings and prolonged discharges which were generated by more specialized sensory endings. In some details these endings were found to be unlike either muscle spindles or tendon organs. Further, skinning experiments suggested that these mechanoreceptors lay in the skin or the very outer layers of the myotome.Histological searching, together with physiological isolation of units, suggested that these receptors were the corpuscular endings distributed sparsely amongst subcutaneous tissue. These endings are apparently the same as those described by Wunderer (1908) in the fins of elasmobranchs.

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Neuromuscular physiology of Hymenolepis diminuta and H. microstoma (Cestoda)

Parasitology ◽

10.1017/s0031182000056766 ◽

1984 ◽

Vol 89 (3) ◽

pp. 567-578 ◽

Cited By ~ 20

Author(s):

C. S. Thompson ◽

D. F. Mettrick

Keyword(s):

Muscle Contraction ◽

Body Wall ◽

Neck Region ◽

Hymenolepis Diminuta ◽

Bathing Solution ◽

Inhibitory Mechanisms ◽

Neuromuscular Systems ◽

Ionic Changes ◽

Chloride Salts

SUMMARYThe physiology of the neuromuscular systems in Hymenolepis diminuta and H. microstoma was studied in vitro using intact, adult worm and strips of worm body wall. Intact worms were insensitive to ionic changes in the in vitro buffering system. However, strips of body wall containing longitudinal muscles were extremely sensitive to ionic manipulation. In intact worms tension generated in the strobila had two components; small brief tension peaks up to 500 mg amplitude are superimposed on larger, longer peaks of up to 1200 mg amplitude. Removal of the scolex and neck region either failed to show significant changes in tension, or showed a reduction in amplitude but not of frequency. Muscle contraction of both H. diminuta and H. microsoma were qualitatively similar. In split-worm preparations the concentration of Ca2+ in the bathing solution significantly affected both spontaneous and evoked contractions in H. diminuta and H. microstoma; the addition of CaCl2 greatly reduced the amplitude and frequency of the contractions. The chloride salts of cobalt, barium, cadmium and manganese elicited prolonged contractions of the longitudinal musculature of both H. diminuta and H. microstoma. While CoCl2 was the most effective in stimulating muscle contraction, the magnitude of the response varied with the concentration of Ca2+ in the bath. The results indicate that peripheral inhibition is extremely important in cestode motor control and that extracellular calcium ions may regulate the peripheral inhibitory mechanisms.

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Adipose fin development and its relation to the evolutionary origins of median fins

10.1101/283432 ◽

2018 ◽

Author(s):

Thomas A. Stewart ◽

Robert K. Ho ◽

Melina E. Hale

Keyword(s):

Spinal Cord ◽

Facial Nerve ◽

Sensory Innervation ◽

Evolutionary Origins ◽

Evolution And Development ◽

Dorsal Rami ◽

Adipose Fin ◽

Median Fins ◽

Fin Development

AbstractThe dorsal, anal and caudal fins of vertebrates are proposed to have originated by the partitioning and transformation of the continuous median fin fold that is plesiomorphic to chordates. Evaluating this hypothesis has been challenging, because it is unclear how the median fin fold relates to the adult median fins of vertebrates. To understand how new median fins originate, here we study the development and diversity of adipose fins. Phylogenetic mapping shows that in all lineages except Characoidei (Characiformes) adipose fins develop from a domain of the larval median fin fold. To inform how the larva’s median fin fold contributes to the adipose fin, we study Corydoras aeneus (Siluriformes). As the fin fold reduces around the prospective site of the adipose fin, a fin spine develops in the fold, growing both proximally and distally, and sensory innervation, which appears to originate from the recurrent ramus of the facial nerve and from dorsal rami of the spinal cord, develops in the adipose fin membrane. Collectively, these data show how a plesiomorphic median fin fold can serve as scaffolding for the evolution and development of novel, individuated median fins, consistent with the median fin fold hypothesis.

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Development of the Pectoral Lobed Fin in the Australian Lungfish Neoceratodus forsteri

Frontiers in Ecology and Evolution ◽

10.3389/fevo.2021.679633 ◽

2021 ◽

Vol 9 ◽

Author(s):

Tatsuya Hirasawa ◽

Camila Cupello ◽

Paulo M. Brito ◽

Yoshitaka Yabumoto ◽

Sumio Isogai ◽

...

Keyword(s):

Brachial Plexus ◽

Body Wall ◽

Developmental Changes ◽

Evolutionary Novelty ◽

Evolutionary Transition ◽

Surface Ectoderm ◽

Spinal Nerves ◽

X Ray ◽

Girdle Muscle ◽

Australian Lungfish

The evolutionary transition from paired fins to limbs involved the establishment of a set of limb muscles as an evolutionary novelty. In parallel, there was a change in the topography of the spinal nerves innervating appendicular muscles, so that distinct plexuses were formed at the bases of limbs. However, the key developmental changes that brought about this evolutionary novelty have remained elusive due to a lack of data on the development of lobed fins in sarcopterygian fishes. Here, we observed the development of the pectoral fin in the Australian lungfish Neoceratodus forsteri (Sarcopterygii) through synchrotron radiation X-ray microtomography. Neoceratodus forsteri is a key taxon for understanding the fin-to-limb transition due to its close phylogenetic relationships to tetrapods and well-developed lobed fins. At the onset of the fin bud in N. forsteri, there is no mesenchyme at the junction between the axial body wall and the fin bud, which corresponds to the embryonic position of the brachial plexus formed in the mesenchyme in tetrapods. Later, concurrent with the cartilage formation in the fin skeleton, the fin adductor and abductor muscles become differentiated within the surface ectoderm of the fin bud. Subsequently, the girdle muscle, which is homologous to the tetrapod serratus muscle, newly develops at the junction between the axial body wall and the fin. Our study suggests that the acquisition of embryonic mesenchyme at the junction between the axial body wall and the appendicular bud opened the door to the formation of the brachial plexus and the specialization of individual muscles in the lineage that gave rise to tetrapods.

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