New, puzzling insights from comparative myological studies on the old and unsolved forelimb/hindlimb enigma

Abstract

Most textbooks and research reports state that the structures of the tetrapod forelimbs and hindlimbs are serial homologues. From this view, the main challenge of evolutionary biologists is not to explain the similarity between tetrapod limbs, but instead to explain why and how they have diverged. However, these statements seem to be related to a confusion between the serial homology of the vertebrate pelvic and pectoral appendages as a whole, and the serial homology of the specific soft- and hard-tissue structures of the tetrapod forelimbs and hindlimbs, leading to an even more crucial and puzzling question being overlooked: why are the skeletal and particularly the muscle structures of the forelimb and hindlimb actually so strikingly similar to each other? Herein we provide an updated discussion of these questions and test two main hypotheses: (i) that the similarity of the limb muscles is due to serial homology; and (ii) that tetrapods that use hindlimbs for a largely exclusive function (e.g. bipedalism in humans) exhibit fewer cases of similarity between forelimbs and hindlimbs than do quadrupedal species. Our review shows that of the 23 arm, forearm and hand muscles/muscle groups of salamanders, 18 (78%) have clear 'topological equivalents' in the hindlimb; in lizards, 14/24 (58%); in rats, 14/35 (40%); and in modern humans, 19/37 (51%). These numbers seem to support the idea that there is a plesiomorphic similarity and subsequent evolutionary divergence, but this tendency actually only applies to the three former quadrupedal taxa. Moreover, if one takes into account the total number of 'correspondences', one comes to a surprising and puzzling conclusion: in modern humans the number of forelimb muscles/muscle groups with clear 'equivalents' in the hindlimb (19) is substantially higher than in quadrupedal mammals such as rats (14), lizards (14) and even salamanders (18). These data contradict the hypothesis that divergent functions lead to divergent morphological structures. Furthermore, as we show that at least five of the 19 modern human adult forelimb elements that have a clear hindlimb 'equivalent' derive from embryonic anlages that are very different from the ones giving rise to their adult hindlimb 'equivalents', they also contradict the hypothesis that the similarity in muscle structures between the forelimb and hindlimb of tetrapods such as modern humans are due to their origin as serial homologues. This similarity is instead the result of phylogenetically independent evolutionary changes leading to a parallelism/convergence due to: (i) developmental constraints, i.e. similar molecular mechanisms are involved (particularly in the formation of the neomorphic hand), but this does not necessarily mean that similar anlages are used to form the similar adult structures; (ii) functional constraints, related to similar adaptations; (iii) topological constraints, i.e. limited physical possibilities; and even (iv) phylogenetic constraints, which tend to prevent/decrease the occurrence of new homoplasic similar...

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

“…In contrast, the co-option of various similar genes in the development of the more distal, and phylogenetically more recent, stylopod/zeugopod and particularly autopod regions of the PECA and PELA of tetrapods led to a marked derived anatomical and developmental similarity between these structures in both appendages (i.e., a ‘similarity bottleneck’ sensu Diogo et al 46, Diogo and Molnar48, and sensu the present work). These more distal limb regions, principally the autopodia, display developmental patterns that are quite different from those of the fins of plesiomorphic gnathostomes41, and of more proximal limb regions in tetrapods.…”

“…A recent compilation of comparative anatomical, paleontological and developmental data strongly suggests that the PECA and PELA were markedly different from each other anatomically in the earliest fishes that had both, and that their most proximal regions (i.e., pelvic vs. pectoral girdles) have remained anatomically, developmentally and genetically quite different454647. In contrast, the co-option of various similar genes in the development of the more distal, and phylogenetically more recent, stylopod/zeugopod and particularly autopod regions of the PECA and PELA of tetrapods led to a marked derived anatomical and developmental similarity between these structures in both appendages (i.e., a ‘similarity bottleneck’ sensu Diogo et al 46, Diogo and Molnar48, and sensu the present work).…”

“…Such schemes have previously been attempted, mostly in the 19 th /early 20 th centuries, but they were strongly biased by the old Romantic ‘archetypal’, idealistic view of evolution46. As seen in Table S7, the topological correspondences inferred here between the girdle/stylopod muscles of the PECA and PELA are, in both salamanders and humans, mainly between groups of muscles, without clear one-to-one equivalences, while those between the zeugopod/autopod muscles are mainly one-to-one.…”

Muscle development in the shark Scyliorhinus canicula: implications for the evolution of the gnathostome head and paired appendage musculature

“…In adult chondrichthyans the pectoral abductor and adductor and the pelvic adductor have superficial and deep bundles, but the pelvic abductor has instead proximal and distal bundles, demonstrating that the significant anatomical differences between the pectoral and pelvic appendages of sharks concern not only hard tissues, but also soft tissues such as muscles [22, 49, 58]. Our results demonstrate that during early developmental stages the muscles of the pectoral and pelvic fins are more similar to each other than in adulthood.…”

“…However, dismissed from these theories are additional components essential for fin/limb function and which probably reinforced their adaptive rate, such as muscles, nerves, or blood vessels. Comparative myogenic studies performed by Diogo and colleagues, integrated with data from other authors and fields, suggest that the musculature of pectoral (fore-) and pelvic (hind-) appendages are particularly different in the proximal (girdle) region of these appendages [22, 49, 50]. These data question the existence of a common serial homologue musculature in pectoral and pelvic appendages, and indicate that what makes the pectoral and pelvic appendages so unique, and so remarkably similar in derived gnathostomes such as tetrapods, might in fact be the result of derived co-option [51].…”