Musculoskeletal anatomical changes that accompany limb reduction in lizards

Abstract

Muscles, bones, and tendons in the adult tetrapod limb are intimately integrated, both spatially and functionally. However, muscle and bone evolution do not always occur hand in hand. We asked, how does the loss of limb bones affect limb muscle anatomy, and do these effects vary among different lineages? To answer these questions, we compared limb muscular and skeletal anatomy among gymnophthalmid lizards, which exhibit a remarkable variation in limb morphology and different grades of digit and limb reduction. We mapped the characters onto a phylogeny of the group to assess the likelihood that they were acquired independently. Our results reveal patterns of reduction of muscle and bone elements that did not always coincide and examples of both, convergent and lineage-specific non-pentadactyl musculoskeletal morphologies. Among lineages in which non-pentadactyly evolved independently, the degree of convergence seems to depend on the number of digits still present. Most tetradactyl and tridactyl limbs exhibited profound differences in pattern and degree of muscle loss/reduction, and recognizable morphological convergence occurred only in extremely reduced morphologies (e.g., spike-like appendix). We also found examples of muscles that persisted although the bones to which they plesiomorphically attach had been lost, and examples of muscles that had been lost although their normal bony attachments persisted. Our results demonstrate that muscle anatomy in reduced limbs cannot be predicted from bone anatomy alone, meaning that filling the gap between osteological and myological data is an important step toward understanding this recurrent phenomenon in the evolution of tetrapods.

Coordinated development of the limb musculoskeletal system: Tendon and muscle patterning and integration with the skeleton

“…Unlike the skeleton, the evolution of soft tissues is challenging to study due to the paucity of significant fossil records. However, comparative anatomy studies across species show a considerable degree of variation in the number of limb muscles and tendons and their pattern, suggesting that adaptability of musculoskeletal units may confer some functional benefits (Abdala et al, 2015; Diogo et al, 2009; Diogo et al, 2015). Clinical observations in humans also demonstrate a wide range in normal variation; for example, the palmaris longus muscle of the forelimb is missing in up to a quarter of the population and the fourth superficial flexor tendon in the digits is missing in over 10% of humans studied (Martinoli et al, 2010; Townley et al, 2010).…”

Myology of the forelimb of Majungasaurus crenatissimus (Theropoda, Abelisauridae) and the morphological consequences of extreme limb reduction

“…An attachment to the distal ulna for Flexor carpi ulnaris has also been described in teiid lizards with reduced forelimb (Abdala et al. ). This insertion of Flexor carpi ulnaris would have resulted in the loss of its action on the carpus and the anterior projection of the distal ulna would have made this muscle a strong flexor of the antebrachium.…”

“…Muscles that typically attach to the carpals are either lost or their attachments shift to a nearby bone when their attachment sites become cartilaginous, as has been described in lepidosaurs (Berger‐Dell'mour, ; Abdala et al. ). It is most common for distal attachments of muscles inserting on the carpals to shift to the proximal metacarpals (these attachments will be discussed below), but Flexor carpi ulnaris may have taken a more proximal insertion in Majungasaurus (Fig.…”

“…) and teiid lizards with reduced forelimbs (Abdala et al. ). The substantial rugosity on the distal radius does not obviously correspond to any other antebrachial muscle and may represent the fusion and common insertion of these two muscles in abelisaurids, where it would serve primarily as an extensor of the forearm.…”

“…Although the manus of Majungasaurus is very reduced, this muscle is often retained in extant taxa with reduced manus (McGowan, ; Berger‐Dell'mour, ; Abdala et al. ), so it is here reconstructed as present. The tendon of this muscle would have reached the manus via a shallow groove in the flaring distal margin of the radius, between the ulnar articular facet and the posterior projection of the radial distal articular surface.…”