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.