The musculature of Peripatus and its innervation

Abstract

The musculature of the Onychophoran Peripatus dominicae , its ultrastructure and details of innervation are described. Significant differences were noted between its gross anatomy and that reported in previous accounts, notably in the presence of inner circular body wall muscle and a prominent, functionally significant, levator of the leg. The former is important in regard to the evolutionary position of the Onychophora while the latter helps us to understand the control of walking in a lobopodial leg, and therefore the evolution of arthropod locomotion, which was the focus of our interest. Individual muscle fibres are either directly or indirectly attached to the body wall by collagen. There is a small degree of branching of fibres, with or without anastomosis, near their insertions, but most are as long as the muscle of which they are part, and are unbranched except for an occasional thin arm, emerging at an angle, that becomes invaded by collagen fibres and inserts in the skin. Diameters of muscle fibres vary from 1 to 45 pm. They are invaginated by two separate systems of unique wide (0.3 pm) tubules, longitudinal and radial. These are lined with similar material to that forming the basement material of the sarcolemma, and also contain fine strands with collagen-type cross-banding that connect to collagen bundles outside the fibres. In addition there are narrow tubules of ordinary T-tubule diameter. Both wide and narrow tubules make contacts with sarcoplasmic reticulum cysternae. Dense Z bodies are attached to both kinds of wide tubule, to the inside of the sarcolemma, and are scattered, without any obvious array, in the sarcoplasm. Thin myofilaments emerge from the Z bodies parallel to the fibre axis. Thick filaments occur in clusters with a loosely hexagonal array, but without any regular relation to thin ones: relatively few orbits of thin around thick filaments were seen in many muscle fibres regardless of fibre length and conditions during fixation. A unique innervation pattern was found, consisting of a combination of muscle arm to nerve contacts, which appear to be the commonest, and nerve on muscle fibre synapses. At least 13 motor axons were found to supply each small muscle or cluster of muscle fibres in a large muscle. Each muscle arm simultaneously makes synaptic contact with 3 to 7 axons. Nerve on muscle junctions contain from 1 to 8 axons, each making synaptic contacts. The details of the postsynaptic endplate-specializations resemble those seen in mammalian endplates and are markedly different from both arthropod and annelidan neuromuscular synapses.

Common and special features of the nervous system of Onychophora: A comparison with Arthropoda, Annelida and some other invertebrates

“…In fact, the innervation of the muscle system and the leg is so different from insects and other land form arthropods in so many aspects that it has been set apart entirely (Hoyle and del Castillo, 1979;Hoyle and Williams, 1980). Hoyle and Williams considered the simply organized lobopodium as a living model for the formation of an arthropod appendage and emphasized the unparalleled structrue of muscle and nerve muscle junctions.…”

“…One substantial difference between the onychophorans and the leeches is the mode of locomotion (walking). We suggest that the high number of neurons in the former, representing augmentation of channels, might account for the unique elaborate muscle and lobopode locomotion apparatus (Hoyle and Williams, 1980), a neuronal attribute invented for organizing locomotion.…”

“…Nerve-muscle junctions occur in two forms: nerve contacting muscle and, more commonly distributed, muscle arms connected to nerves (Hoyle and Williams, 1980). Synaptic contacts resemble annelid-type junctions (Schiirmann, 1978b).…”

“…The multiple onychophoran neuro-muscular synapse (Fig. 2) is considered to be unique (Hoyle and Williams, 1980).…”

Onychophoran-like musculature in a phosphatized Cambrian lobopodian

“…Nevertheless, the derivation of three-layered musculature from the presumably ancestral twin layers observed in priapulids [23] is not straightforward. In priapulids and extant onychophorans, the outermost muscles are circular and the innermost longitudinal, with onychophorans incorporating an intermediate layer of interwoven oblique muscles [24,25]. Tritonychus phanerosarkus exhibits equivalent layers-though their order is reversed, leaving the homology of each layer with those in other panarthropods unclear, and revealing an unexpected diversity of muscle arrangement in early panarthropods.…”