Development and Evolution of the Muscles of the Pelvic Fin (original) (raw)

The pectoral fin muscles of the coelacanthLatimeria chalumnae: Functional and evolutionary implications for the fin-to-limb transition and subsequent evolution of tetrapods

The Anatomical Record, 2016

To investigate the morphology and evolutionary origin of muscles in vertebrate limbs, we conducted anatomical dissections, computed tomography and kinematic analyses on the pectoral fin of the African coelacanth, Latimeria chalumnae. We discovered nine antagonistic pairs of pronators and supinators that are anatomically and functionally distinct from the abductor and adductor superficiales and profundi. In particular, the first pronator and supinator pair represents mono-and bi-articular muscles; a portion of the muscle fibers is attached to ridges on the humerus and is separated into two mono-articular muscles, whereas, as a bi-articular muscle, the main body is inserted into the radius by crossing two joints from the shoulder girdle. This pair, consisting of a pronator and supinator, constitutes a muscle arrangement equivalent to two human antagonistic pairs of mono-articular muscles and one antagonistic pair of bi-articular muscles in the stylopod between the shoulder and elbow joints. Our recent kinesiological and biomechanical engineering studies on human limbs have demonstrated that two antagonistic pairs of mono-articular muscles and one antagonistic pair of bi-articular muscles in the stylopod (1) coordinately control output force and force direction at the wrist and ankle and (2) achieve a contact task to carry out weight-bearing motion and maintain stable posture. Therefore, along with dissections of the pectoral fins in two lungfish species, Neoceratodus forsteri and Protopterus aethiopicus, we discuss the functional and evolutionary implications for the fin-to-limb transition and subsequent evolution of tetrapods.

Shaping muscle bioarchitecture for the fin to limb transition

Bioarchitecture, 2012

Our recent paper examined how pelvic fins and their musculature form developmentally and how these mechanisms have evolved within the vertebrate lineage, a process fundamental to the tetrapod transition. The transition from the water onto the land is among one of the most well studied steps in the evolutionary history of vertebrates, yet the genetic basis of this evolutionary transition is little studied and ill-defined. The advent of these terrestrial species resulted in a shift in locomotor strategies from the rhythmic undulating muscles of the fish body to a reliance upon powerful weight bearing muscles of the limbs to generate movement. We demonstrated that the pelvic fin muscles of bony fish are generated by a mechanism that has features of both of limb/fin muscle formation in tetrapods and primitive cartilaginous fish. We hypothesize that the adoption of the fully derived mode of hindlimb muscle formation, was a further modification of the mode of development deployed to gener...

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

Previous accounts of the origin of tetrapod limbs have postulated a relatively sudden change, after the split between extant lobe-finned fish and tetrapods, from a very simple fin phenotype with only two muscles to the highly complex tetrapod condition. The evolutionary changes that led to the muscular anatomy of tetrapod limbs have therefore remained relatively unexplored. We performed dissections, histological sections, and MRI scans of the closest living relatives of tetrapods: coelacanths and lungfish. Combined with previous comparative, developmental and paleontological information, our findings suggest that the characteristic tetrapod musculoskeletal limb phenotype was already present in the Silurian last common ancestor of extant sarcopterygians, with the exception of the autopod (hand/foot) structures, which have no clear correspondence with fish structures. Remarkably, the two major steps in this long process – leading to the ancestral fin anatomy of extant sarcopterygians and limb anatomy of extant tetrapods, respectively – occurred at the same nodes as the two major similarity bottlenecks that led to the striking derived myological similarity between the pectoral and pelvic appendages within each taxon. Our identification of probable homologies between appendicular muscles of sarcopterygian fish and tetrapods will allow more detailed reconstructions of muscle anatomy in early tetrapods and their relatives. Most studies on the origin of limbs focus on fossil skeletal structures 1–5 , mainly because fossils usually do not preserve soft tissues, and because it is difficult to compare fish fins and tetrapod limbs as they are morphologically very different (e.g., in orientation of axes and number/configuration of muscles). Classic comparative anatomy works provided in-depth descriptions of the major rotation of the paired appendages that occurred during the early stages of the fins-limbs transition: the preaxial (radial/tibial) side, directed antero-dorsally in extant fishes such as Polypterus, Latimeria and living dipnoans, became directed antero-ventrally 6–11. However, these descriptions are not always taken into account in recent works, leading to errors and terminological problems (see below, and SI). Although numerous appendicular muscles have been described in the coelacanth Latimeria 12,13 , these descriptions are often excluded from recent discussions about the fins-limbs transition because dipnoans are phylogenetically closer to tetrapods than are coelacanths 14. Therefore, most authors consider that a transition occurred after the dipnoan-tetrapod divergence, from a very simple fin configuration with only two major muscle masses (adductor/abductor) to the highly complex tetrapod limbs that can have more than 50 muscles 15. Accordingly, Extant Phylogenetic Bracketing 16 , one of the most powerful tools for soft tissue reconstruction, has never been used to study this fins-limbs transition 17 , despite the fact that the relationships of extant sarcoptergians have long been well established 18. The original data obtained from extant taxa, combined with the comparisons, that are presented in this paper will be crucial in paving the way for the use of this method in muscle reconstructions of key tetrapod and non-tetrapod sarcopterygian extinct taxa. Specifically, for this work, we obtained new musculoskeletal data from dissections, MRI scans, 3D reconstructions, and histological sections of coelacanths (Latimeria) and dipnoans (Neoceratodus) (see SI, which includes Tables S1–S4 showing all muscle-bone attachments) and combined them

Unique pelvic fin in a tetrapod-like fossil fish, and the evolution of limb patterning

All living tetrapods have a one-to-two branching pattern in the embryonic proximal limb skeleton, with a single element at the base of the limb (the humerus or femur) that articulates distally with two parallel radials (the ulna and radius or the tibia and fibula). This pattern is also seen in the fossilized remains of stem-tetrapods, including the fishlike members of the group, in which despite the absence of digits, the proximal parts of the fin skeleton clearly resemble those of later tetrapods. However, little is known about the developmental mechanisms that establish and canalize this highly conserved pattern. We describe the well-preserved pelvic fin skeleton of Rhizodus hibberti, a Carboniferous sarcopterygian (lobe-finned) fish, and member of the tetrapod stem group. In this specimen, three parallel radials, each robust with a distinct morphology , articulate with the femur. We review this unexpected morphology in a phylogenetic and developmental context. It implies that the developmental patterning mechanisms seen in living tetrapods, now highly constrained, evolved from mechanisms flexible enough to accommodate variation in the zeugopod (even between pectoral and pelvic fins), while also allowing each element to have a unique morphology. zeugopod | pelvis | limb patterning | tetrapodomorph | rhizodontid

Evolution, Homology, and Development of Tetrapod Limb Muscles

Diversity, 2021

Since the early 1900s, researchers have attempted to unravel the origin and evolution of tetrapod limb muscles using a combination of comparative anatomy, phylogeny, and development. The methods for reconstructing soft tissues in extinct animals have been refined over time as our ability to determine muscle homology and phylogenetic relationships between tetrapods has improved. Since many muscles do not leave osteological correlates, muscle reconstruction in extinct animals is largely based on anatomy and development in extant animals. While muscle anatomy in extant tetrapods is quite conservative, the homologies of certain muscles between taxonomic groups are still uncertain. Comparative developmental studies can help to resolve these controversies, as well as revealing general patterns of muscle morphogenesis across tetrapod groups. We review the methods, results, and controversies in the muscle reconstructions of early members of the amniote, mammalian, and lissamphibian lineages...

Evidence that mechanisms of fin development evolved in the midline of early vertebrates

Nature, 2006

The origin of paired appendages was a major evolutionary innovation for vertebrates, marking the first step towards fin-(and later limb-) driven locomotion. The earliest vertebrate fossils lack paired fins but have well-developed median fins 1,2 , suggesting that the mechanisms of fin development were assembled first in the midline. Here we show that shark median fin development involves the same genetic programs that operate in paired appendages. Using molecular markers for different cell types, we show that median fins arise predominantly from somitic (paraxial) mesoderm, whereas paired appendages develop from lateral plate mesoderm. Expression of Hoxd and Tbx18 genes, which specify paired limb positions 3,4 , also delineates the positions of median fins. Proximodistal development of median fins occurs beneath an apical ectodermal ridge, the structure that controls outgrowth of paired appendages 5-7 . Each median fin bud then acquires an anteroposteriorly-nested pattern of Hoxd expression similar to that which establishes skeletal polarity in limbs 8,9 . Thus, despite their different embryonic origins, paired and median fins utilize a common suite of developmental mechanisms. We extended our analysis to lampreys, which diverged from the lineage leading to gnathostomes before the origin of paired appendages 2,10 , and show that their median fins also develop from somites and express orthologous Hox and Tbx genes. Together these results suggest that the molecular mechanisms for fin development originated in somitic mesoderm of early vertebrates, and that the origin of paired appendages was associated with re-deployment of these mechanisms to lateral plate mesoderm.

The evolutionary history of the development of the pelvic fin/hindlimb

Journal of Anatomy, 2013

The arms and legs of man are evolutionarily derived from the paired fins of primitive jawed fish. Few evolutionary changes have attracted as much attention as the origin of tetrapod limbs from the paired fins of ancestral fish. The hindlimbs of tetrapods are derived from the pelvic fins of ancestral fish. These evolutionary origins can be seen in the examination of shared gene and protein expression patterns during the development of pelvic fins and tetrapod hindlimbs. The pelvic fins of fish express key limb positioning, limb bud induction and limb outgrowth genes in a similar manner to that seen in hindlimb development of higher vertebrates. We are now at a point where many of the key players in the development of pelvic fins and vertebrate hindlimbs have been identified and we can now readily examine and compare mechanisms between species. This is yielding fascinating insights into how the developmental programme has altered during evolution and how that relates to anatomical change. The role of pelvic fins has also drastically changed over evolutionary history, from playing a minor role during swimming to developing into robust weight-bearing limbs. In addition, the pelvic fins/hindlimbs have been lost repeatedly in diverse species over evolutionary time. Here we review the evolution of pelvic fins and hindlimbs within the context of the changes in anatomical structure and the molecular mechanisms involved.

The Role of the Tail or Lack Thereof in the Evolution of Tetrapod Aquatic Propulsion

Integrative and Comparative Biology, 2021

Secondary aquatic vertebrates exhibit a diversity of swimming modes that use paired limbs and/or the tail. Various secondarily aquatic tetrapod clades, including amphibians, reptiles, and mammals use transverse undulations or oscillations of the tail for swimming. These movements have often been classified according to a kinematic gradient that was established for fishes but may not be appropriate to describe the swimming motions of tetrapods. To understand the evolution of movements and design of the tail in aquatic tetrapods, we categorize the types of tails used for swimming and examine swimming kinematics and hydrodynamics. From a foundation of a narrow, elongate ancestral tail, the tails used for swimming by aquatic tetrapods are classified as tapered, keeled, paddle, and lunate. Tail undulations are associated with tapered, keeled, and paddle tails for a diversity of taxa. Propulsive undulatory waves move down the tail with increasing amplitude toward the tail tip, while movin...