Musculoskeletal morphology of the pelvis and pelvic fins in the lungfishProtopterus annectens

Abstract

The West African lungfish (Protopterus annectens) performs benthic, pelvic fin-driven locomotion with gaits common to tetrapods, the sister group of the lungfishes. Features of P. annectens movement are similar to those of modern tetrapods and include use of the distal region of the pelvic fin as a “foot,” use of the fin to lift the body above the substrate and rotation of the fin around the joint with the pelvis. In contrast to these similarities in movement, the pelvic fins of P. annectens are long, slender structures that are superficially very different from tetrapod limbs. Here, we describe the musculoskeletal anatomy of the pelvis and pelvic fins of P. annectens with dissection, magnetic resonance imaging, histology and 3D-reconstruction methods. We found that the pelvis is embedded in the hypaxial muscle by a median rostral and two dorsolateral skeletal projections. The protractor and retractor muscles at the base of the pelvic fin are fan-shaped muscles that cup the femur. The skeletal elements of the fin are serially repeating cartilage cylinders. Along the length of the fin, repeating truncated cones of muscles, the musculus circumradialis pelvici, are separated by connective tissue sheets that connect the skeletal elements to the skin. The simplicity of the protractor and retractor muscles at the base of the fin is surprising, given the complex rotational movement those muscles generate. In contrast, the series of many repeating segmental muscles along the length of the fin is consistent with the dexterity of bending of the distal limb. P. annectens can provide a window into softtissue anatomy and sarcopterygian fish fin function that complements the fossil data from related taxa. This work, combined with previous behavioral examination of P. annectens, illustrates that fin morphologies that do not appear to be capable of walking can accomplish that function, and may inform the interpretation of fossil anatomical evidence.

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

“…VR, ventral retractor; DR, dorsal retractor; DP, dorsal protractor; VP, ventral protractor. 105262 of the rostral and caudal sides of the femur, respectively (King and Hale, 2014) (see Fig. 2 of the present study).…”

“…The goal of this study was to determine how African lungfish (P. annectens) produce complex movements of their pelvic fin about their hip joint (King et al, 2011), given their seemingly simple morphological system (King and Hale, 2014). Protopterus annectens has only two muscles, the protractor and retractor, spanning the hip joint.…”

“…First, we hypothesized that lungfish protractor and retractor muscles are functionally subdivided, allowing muscle regions to participate in different phases of the stride cycle. King and Hale have found broad origination and insertion of these muscles (King and Hale, 2014). This morphology suggests that regional activation in each muscle could generate force in a range of directions.…”

“…2). These fan-shaped muscles originate on the ventral and dorsal aspects of the pelvis and body wall and span the hip joint to insert on the rostral and caudal aspects of the femur, respectively (King and Hale, 2014) (see Fig. 2).…”

Characteristic tetrapod musculoskeletal limb phenotype emerged more than 400 MYA in basal lobe-finned fishes

“…Regarding the muscular anatomy of lobe-finned fishes, the major novel contributions of this work are 1) description of new muscles; 2) re-appraisal of evolutionary origin (e.g., from ventral/abductor vs. dorsal/adductor masses) and identity of previously described muscles; and 3) first comprehensive comparisons of pelvic and pectoral appendages (PELA, PECA) among these and other fish and in tetrapods, leading to proposal of new names, evolutionary origins and one-to-one homology hypotheses for all muscles of these taxa (see SI for more details, in particular between the differences between our work and previous studies). We discuss our results in the context of the anatomical, developmental, and paleontological literature, including recent papers on the soft tissues of adult dipnoans1920 and coelacanths14, of phylogenetically basal extant bony fishes such as Polypterus 21, and works on appendicular muscle development in most gnathostome clades111222232425262728293031323334.…”