Functional subdivision of fin protractor and retractor muscles underlies pelvic fin walking in the African lungfish Protopterus annectens

Abstract

African lungfish Protopterus annectens can produce rotational movements around the joint between the pelvis and the pelvic fin, allowing these animals to walk across benthic substrates. In tetrapods, limb rotation at the hip joint is a common feature of substrate-based locomotion. For sprawling tetrapods, rotation can involve nine or more muscles, which are often robust and span multiple joints. In contrast, P. annectens uses a modest morphology of two fan-shaped muscles, the pelvic fin protractor and retractor, to accomplish this movement. We hypothesized that functional subdivision, coupled with their broad insertions on the femur, allows each of these muscles to pull on the limb from multiple directions and provides a mechanism for fin rotation. To test this hypothesis, we examined the muscle activity at three locations in both the protractor and the retractor muscles during walking. Electromyograms show differences in the timing of muscle activation between dorsal and ventral regions of each muscle, suggesting that each muscle is functionally subdivided once. The subdivisions demonstrate sequential onsets of muscle activity and overlap of activity between regions, which are also features of limb control in tetrapods. These data indicate that subdivisions of protractor and retractor muscles impart functional complexity to a morphologically simple system, and suggest a mechanism that allows lungfish to produce a tetrapod-like walking gait with only two muscles. As one of few extant sarcopterygian fishes, P. annectens may provide important functional data to inform interpretation of limb movement of fossil relatives.