Pelvic Appendages Research Articles

Reconstruction of the pelvic girdle and hindlimb musculature of the early tetanurans Piatnitzkysauridae (Theropoda, Megalosauroidea).

Piatnitzkysauridae were Jurassic theropods that represented the earliest diverging branch of Megalosauroidea, being one of the earliest lineages to have evolved moderate body size. This clade's typical body size and some unusual anatomical features raise questions about locomotor function and specializations to aid in body support; and other palaeobiological issues. Biomechanical models and simulations can illuminate how extinct animals may have moved, but require anatomical data as inputs. With a phylogenetic context, osteological evidence, and neontological data on anatomy, it is possible to infer the musculature of extinct taxa. Here, we reconstructed the hindlimb musculature of Piatnitzkysauridae (Condorraptor, Marshosaurus, and Piatnitzkysaurus). We chose this clade for future usage in biomechanics, for comparisons with myological reconstructions of other theropods, and for the resulting evolutionary implications of our reconstructions; differential preservation affects these inferences, so we discuss these issues as well. We considered 32 muscles in total: for Piatnitzkysaurus, the attachments of 29 muscles could be inferred based on the osteological correlates; meanwhile, in Condorraptor and Marshosaurus, we respectively inferred 21 and 12 muscles. We found great anatomical similarity within Piatnitzkysauridae, but differences such as the origin of M. ambiens and size of M. caudofemoralis brevis are present. Similarities were evident with Aves, such as the division of the M. iliofemoralis externus and M. iliotrochantericus caudalis and a broad depression for the M. gastrocnemius pars medialis origin on the cnemial crest. Nevertheless, we infer plesiomorphic features such as the origins of M. puboischiofemoralis internus 1 around the "cuppedicus" fossa and M. ischiotrochantericus medially on the ischium. As the first attempt to reconstruct muscles in early tetanurans, our study allows a more complete understanding of myological evolution in theropod pelvic appendages.

Developmental Genetic Basis of Hoxd9 Homeobox Domain Deletion in Pampus argenteus Pelvic Fin Deficiency.

Pampus argenteus is important for commercial fishery catch species and is an emerging target for aquaculture production. Notably, P. argenteus has a bizarre morphology and lacks pelvic fins. However, the reason for the lack of pelvic fins remains unclear, ultimately leading to frequent upside-down floating of P. argenteus during breeding and marked consumption of physical energy. Some lineages, including whales, fugu, snakes, and seahorse, independently lost the pelvic appendages over evolutionary time. Do different taxa employ the same molecular genetic pathways when they independently evolve similar developmental morphologies? Through analysis of the gene responsible for appendage localization, Hoxd9, it was discovered that the Hox domain was absent in the Hoxd9 gene of P. argenteus, and the Hoxd9b gene lacked the Hox9 activation region, a feature not observed in the Hoxd9 gene of other fish species. Interestingly, those distinctive characteristics are not observed in the Hoxd9 gene of other fish species. To determine the association between the Hoxd9 gene characteristics and the pelvic fin deletion in P. argenteus, the full-length cDNA of the Hoxd9a gene was cloned, and morphological observations of the species' juveniles were performed using stereomicroscopy and scanning electron microscopy. Thereafter, the tissue localization of Hoxd9a in the species was analyzed at the gene and protein levels. Based on the results, deletion of the Hoxd9a structural domain possibly leads to disruptions in the protein translation and the pelvic fin localization in P. argenteus during its early ontogenetic developmental stage, resulting in the absence of pelvic fins.

Galeaspid anatomy and the origin of vertebrate paired appendages.

Paired fins are a major innovation1,2 that evolved in the jawed vertebrate lineage after divergence from living jawless vertebrates3. Extinct jawless armoured stem gnathostomes show a diversity of paired body-wall extensions, ranging from skeletal processes to simple flaps4. By contrast, osteostracans (a sister group to jawed vertebrates) are interpreted to have the first true paired appendages in a pectoral position, with pelvic appendages evolving later in association with jaws5. Here we show, on the basis of articulated remains of Tujiaaspis vividus from the Silurian period of China, that galeaspids (a sister group to both osteostracans and jawed vertebrates) possessed three unpaired dorsal fins, an approximately symmetrical hypochordal tail and a pair of continuous, branchial-to-caudal ventrolateral fins. The ventrolateral fins are similar to paired fin flaps in other stem gnathostomes, and specifically to the ventrolateral ridges of cephalaspid osteostracans that also possess differentiated pectoral fins. The ventrolateral fins are compatible with aspects of the fin-fold hypothesis for the origin of vertebrate paired appendages6-10. Galeaspids have a precursor condition to osteostracans and jawed vertebrates in which paired fins arose initially as continuous pectoral-pelvic lateral fins that our computed fluid-dynamics experiments show passively generated lift. Only later in the stem lineage to osteostracans and jawed vertebrates did pectoral fins differentiate anteriorly. This later differentiation was followed by restriction of the remaining field of fin competence to a pelvic position, facilitating active propulsion and steering.

Cranial or postcranial-Dual origin of the pectoral appendage of vertebrates combining the fin-fold and gill-arch theories?

Two main theories have been used to explain the origin of pectoral and pelvic appendages. The "fin-fold theory" proposes that they evolved from a trunk bilateral fin fold, while Gegenbaur's theory assumes they derived from the head branchial arches. However, none of these theories has been fully supported. The "fin-fold" theory is mainly often accepted due to some existing developmental data, but recent developmental studies have revived Gegenbaur's theory by revealing common mechanisms underlying the patterning of branchial arches and paired appendages. Here I review developmental data and many others lines of evidence, which lead to a crucial question: might the apparent contradictions between the two theories be explained by a dual origin of the pectoral appendage, that is, the pectoral girdle and fin/limb being mainly related to the head and trunk, respectively? If this is so then (a) the pectoral and pelvic girdles would not be serial homologues; (b) the term "developmental serial homologues" could only potentially be applied to the pectoral and pelvic fins/limbs. Fascinatingly, in a way this would be similar to what Owen had already suggested, more than 170 years ago: that the pectoral and pelvic girdles are mainly related to the head and trunk, respectively.

Evolutionary parallelisms of pectoral and pelvic network-anatomy from fins to limbs

Lobe-fins transformed into limbs during the Devonian period, facilitating the water-to-land transition in tetrapods. We traced the evolution of well-articulated skeletons across the fins-to-limbs transition, using a network-based approach to quantify and compare topological features of fins and limbs. We show that the topological arrangement of bones in pectoral and pelvic appendages evolved in parallel during the fins-to-limbs transition, occupying overlapping regions of the morphospace, following a directional trend, and decreasing their disparity over time. We identify the presence of digits as the morphological novelty triggering topological changes that discriminated limbs from fins. The origin of digits caused an evolutionary shift toward appendages that were less densely and heterogeneously connected, but more assortative and modular. Disparity likewise decreased for both appendages, more markedly until a time concomitant with the earliest-known tetrapod tracks. Last, we rejected the presence of a pectoral-pelvic similarity bottleneck at the origin of tetrapods.

A novel enhancer near the Pitx1 gene influences development and evolution of pelvic appendages in vertebrates

Vertebrate pelvic reduction is a classic example of repeated evolution. Recurrent loss of pelvic appendages in sticklebacks has previously been linked to natural mutations in a pelvic enhancer that maps upstream of Pitx1. The sequence of this upstream PelA enhancer is not conserved to mammals, so we have surveyed a large region surrounding the mouse Pitx1 gene for other possible hind limb control sequences. Here we identify a new pelvic enhancer, PelB, that maps downstream rather than upstream of Pitx1. PelB drives expression in the posterior portion of the developing hind limb, and deleting the sequence from mice alters the size of several hind limb structures. PelB sequences are broadly conserved from fish to mammals. A wild stickleback population lacking the pelvis has an insertion/deletion mutation that disrupts the structure and function of PelB, suggesting that changes in this ancient enhancer contribute to evolutionary modification of pelvic appendages in nature.

Evolution of Hindlimb Muscle Anatomy Across the Tetrapod Water-to-Land Transition, Including Comparisons With Forelimb Anatomy.

Tetrapod limbs are a key innovation implicated in the evolutionary success of the clade. Although musculoskeletal evolution of the pectoral appendage across the fins-to-limbs transition is fairly well documented, that of the pelvic appendage is much less so. The skeletal elements of the pelvic appendage in some tetrapodomorph fish and the earliest tetrapods are relatively smaller and/or qualitatively less similar to those of crown tetrapods than those of the pectoral appendage. However, comparative and developmental works have suggested that the musculature of the tetrapod forelimb and hindlimb was initially very similar, constituting a "similarity bottleneck" at the fins-to-limbs transition. Here, we used extant phylogenetic bracketing and phylogenetic character optimization to reconstruct pelvic appendicular muscle anatomy in several key taxa spanning the fins-to-limbs and water-to-land transitions. Our results support the hypothesis that transformation of the pelvic appendages from fin-like to limb-like lagged behind that of the pectoral appendages. Compared to similar reconstructions of the pectoral appendages, the pelvic appendages of the earliest tetrapods had fewer muscles, particularly in the distal limb (shank). In addition, our results suggest that the first tetrapods had a greater number of muscle-muscle topological correspondences between the pectoral and pelvic appendages than tetrapodomorph fish had. However, ancestral crown-group tetrapods appear to have had an even greater number of similar muscles (both in terms of number and as a percentage of the total number of muscles), indicating that the main topological similarity bottleneck between the paired appendages may have occurred at the origin of the tetrapod crown group. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 303:218-234, 2020. © 2018 American Association for Anatomy.

Loss in the making: absence of pelvic fins and presence of paedomorphic pelvic girdles in a Late Devonian antiarch placoderm (jawed stem-gnathostome).

Within jawed vertebrates, pelvic appendages have been modified or lost repeatedly, including in the most phylogenetically basal, extinct, antiarch placoderms. One Early Devonian basal antiarch, Parayunnanolepis, possessed pelvic girdles, suggesting the presence of pelvic appendages at the origin of jawed vertebrates; their absence in more derived antiarchs implies a secondary loss. Recently, paired female genital plates were identified in the Late Devonian antiarch, Bothriolepis canadensis, in the position of pelvic girdles in other placoderms. We studied these putative genital plates along an ontogenetic series of B. canadensis; ontogenetic changes in their morphology, histology and elemental composition suggest they represent endoskeletal pelvic girdles composed of perichondral and endochondral bone. We suggest that pelvic fins of derived antiarchs were lost, while pelvic girdles were retained, but reduced, relative to Parayunnanolepis This indicates developmental plasticity and evolutionary lability in pelvic appendages, shortly after these elements evolved at the origin of jawed vertebrates.

Comparative anatomy and development of zebrafish fin muscles: basis for functional, developmental, and macroevolutionary studies

Dario rerio is a model organism extensively used in numerous evo‐devo studies devoted to the fin skeletal anatomy and fin‐limb transition. While the skeleton of the paired and median fins of the zebrafish have been described in great detail, little is known about the anatomy and development of the appendicular musculature of this fish. In order to provide a basis for myological, comparative and evolutionary studies, we described for the first time the development, identity, overall configuration, and attachments of all appendicular muscles of D. rerio. We show that the muscle pattern of the caudal fin differs from patterns seen in other zebrafish fins but it is very similar among teleosts in general. This finding supports the idea that developmentally and evolutionary this fin is very peculiar. We describe for the first time interhypural muscles present in the caudal fin of young fishes and absent in adults. The musculature of the adult zebrafish pectoral and pelvic fins is very similar in general, but we note marked differences concerning the development of these muscles. We therefore discuss whether the pectoral appendage might be evolutionary closer to the head than to the pelvic appendage. We provide the anatomical and developmental description of the dorsal and anal fin muscles in zebrafish and describe homologies between the appendicular structures of zebrafish and other fish taxa. We discuss evolutionary trends within these clades to investigate whether the zebrafish is a good model for teleosts in particular and actinopterygians in general. Lastly, we discuss examples of phylo‐devo parallelism that links evolution and development. Our data on the adult phenotype and myogenesis in the zebrafish provide a basis for more integrative developmental, functional, evolutionary, and pathological studies.Support or Funding InformationThis work was supported by Russian Foundation for Basic Research, project nos. 14‐04‐00590 and 17‐04‐01617. The research was done using equipment of the Core Centrum of Insitute of Developmental Biology RAS.This abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Anatomical network analysis of the musculoskeletal system reveals integration loss and parcellation boost during the fins-to-limbs transition.

Tetrapods evolved from within the lobe-finned fishes around 370 Ma. The evolution of limbs from lobe-fins entailed a major reorganization of the skeletal and muscular anatomy of appendages in early tetrapods. Concurrently, a degree of similarity between pectoral and pelvic appendages also evolved. Here, we compared the anatomy of appendages in extant lobe-finned fishes (Latimeria and Neoceratodus) and anatomically plesiomorphic amphibians (Ambystoma, Salamandra) and amniotes (Sphenodon) to trace and reconstruct the musculoskeletal changes that took place during the fins-to-limbs transition. We quantified the anatomy of appendages using network analysis. First, we built network models-in which nodes represent bones and muscles, and links represent their anatomical connections-and then we measured network parameters related to their anatomical integration, heterogeneity, and modularity. Our results reveal an evolutionary transition toward less integrated, more modular appendages. We interpret this transition as a diversification of muscle functions in tetrapods compared to lobe-finned fishes. Limbs and lobe-fins show also a greater similarity between their pectoral and pelvic appendages than ray-fins do. These findings on extant species provide a basis for future quantitative and comprehensive reconstructions of the anatomy of limbs in early tetrapod fossils, and a way to better understand the fins-to-limbs transition.

Comparative anatomy of zebrafish paired and median fin muscles: basis for functional, developmental, and macroevolutionary studies.

In the last decades, Danio rerio became one of the most used model organisms in various evo-devo studies devoted to the fin skeletal anatomy and fin-limb transition. Surprisingly, there is not even a single paper about the detailed anatomy of the adult muscles of the five fin types of this species. To facilitate more integrative developmental, functional, genetic, and evolutionary studies of the appendicular musculoskeletal system of the zebrafish and to provide a basis for further comparisons with other fishes and tetrapods, we describe here the identity, overall configuration, and attachments of appendicular muscles in a way that can be easily understood and implemented by non-anatomist researchers. We show that the muscle pattern of the caudal fin is very different from patterns seen in other fins but is very consistent within teleosts. Our observations support the idea of the developmental and evolutionary distinction of the caudal fin and point out that the musculature of the adult zebrafish pectoral and pelvic fins is in general very similar. Both paired fins have superficial and deep layers of abductors and adductors going to all/most rays plus the dorsal and ventral arrectors going only to the first ray. Nevertheless, we noted three major differences between the pelvic and pectoral fins of adult zebrafishes: (i) the pectoral girdle lacks a retractor muscle, which is present in the pelvic girdle - the retractor ischii; (ii) the protractor of the pelvic girdle is an appendicular/trunk muscle, while that of the pectoral girdle is a branchiomeric muscle; (iii) the first ray of the pectoral fin is moved by an additional arrector-3. The anal and dorsal fins consist of serially repeated units, each of which comprises one half-ray and three appendicular muscles (one erector, depressor, and inclinator) on each side of the body. The outermost rays are attachment points for the longitudinal protractor and retractor. Based on our results, we discuss whether the pectoral appendage might evolutionarily be closer to the head than to the pelvic appendage and whether the pelvic appendage might have been derived from the trunk/median fins. We discuss a hypothesis of paired fin origin that is a hybrid of the fin-fold and Gegenbaur's theories. Lastly, our data indicate that D.rerio is indeed an appropriate model organism for the appendicular musculature of teleosts in particular and, at least in the case of the paired fins, also of actinopterygians as a whole.

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

BackgroundThe origin of jawed vertebrates was marked by profound reconfigurations of the skeleton and muscles of the head and by the acquisition of two sets of paired appendages. Extant cartilaginous fish retained numerous plesiomorphic characters of jawed vertebrates, which include several aspects of their musculature. Therefore, myogenic studies on sharks are essential in yielding clues on the developmental processes involved in the origin of the muscular anatomy.ResultsHere we provide a detailed description of the development of specific muscular units integrating the cephalic and appendicular musculature of the shark model, Scyliorhinus canicula. In addition, we analyze the muscle development across gnathostomes by comparing the developmental onset of muscle groups in distinct taxa. Our data reveal that appendicular myogenesis occurs earlier in the pectoral than in the pelvic appendages. Additionally, the pectoral musculature includes muscles that have their primordial developmental origin in the head. This culminates in a tight muscular connection between the pectoral girdle and the cranium, which founds no parallel in the pelvic fins. Moreover, we identified a lateral to ventral pattern of formation of the cephalic muscles, that has been equally documented in osteichthyans but, in contrast with these gnathostomes, the hyoid muscles develop earlier than mandibular muscle in S. canicula.ConclusionOur analyses reveal considerable differences in the formation of the pectoral and pelvic musculatures in S. canicula, reinforcing the idea that head tissues have contributed to the formation of the pectoral appendages in the common ancestor of extant gnathostomes. In addition, temporal differences in the formation of some cranial muscles between chondrichthyans and osteichthyans might support the hypothesis that the similarity between the musculature of the mandibular arch and of the other pharyngeal arches represents a derived feature of jawed vertebrates.

A major paradigm shift in fish, tetrapod and limb evolution: 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 has 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 exception to 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.Support or Funding InformationAm. Assoc. Anat. postdoctoral grant to JLM, and European Union's Horizon 2020 Marie Skłodowska‐Curie grant No 654155 to BE‐A.

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.

Evolution of Serial Patterns in the Vertebrate Pharyngeal Apparatus and Paired Appendages via Assimilation of Dissimilar Units

Evolution of serially similar structures has attracted interest since the infancy of comparative morphology and embryology. A long-standing assumption is that the serial patterning reflects ancestral metamerism, which persists in preconceived character polarity from a primitive state of polyisomerism (a series of identical or similar units) to a derived state of anisomerism (a series of differentially specialized parts). We test this assumption against an alternative character polarity — from anisomeric to polyisomeric — in the vertebrate pharyngeal apparatus and paired appendages. We show that, contrary to what is usually assumed, serial similarity represents a derived state in both pharyngeal apparatus and paired appendages: the distinctly patterned structures secondarily assimilated each other. Acquisitions of serial similarity in the pharyngeal apparatus and paired appendages straddle major evolutionary events such as the origin of the jaw and fish-tetrapod transitions. We suggest that: (a) the origin of the jaw coincided with extension of the serial pharyngeal patterning onto the mandibular region; and (b) the pectoral and pelvic appendages have independent origins and their distal portions acquired serial similarities later during the fin-limb transitions.

On the serial homology of the pectoral and pelvic girdles of tetrapods.

While fore- and hindlimbs are commonly assumed to be serially homologous, the serial homology of the pectoral and pelvic girdles is more ambiguous. We investigate the degree to which a common history, developmental program, and gene network are shared between the girdles relative to the rest of the appendicular skeleton. Paleontological data indicate that pectoral appendages arose millions of years before pelvic appendages. Recent embryological and genetic data suggest that the anatomical similarity between the fore- and hindlimbs arose through the sequential, derived deployment of similar developmental programs and gene networks, and is therefore not due to ancestral serial homology. Much less developmental work has however been published about the girdles. Here, we provide the first detailed review of the developmental programs and gene networks of the pectoral and pelvic girdles. Our review shows that, with respect to these programs and networks, there are fewer similarities between pelvic and pectoral girdles than there are between the limbs. The available data therefore support recent hypotheses that the anatomical similarities between the fore- and hindlimbs arose during the fin-to-limb transition through the derived co-option of similar developmental mechanisms, while the phylogenetically older pectoral and pelvic girdles have remained more distinct since their evolutionary origin.

Pelvic girdle and fin ofTiktaalik roseae

A major challenge in understanding the origin of terrestrial vertebrates has been knowledge of the pelvis and hind appendage of their closest fish relatives. The pelvic girdle and appendage of tetrapods is dramatically larger and more robust than that of fish and contains a number of structures that provide greater musculoskeletal support for posture and locomotion. The discovery of pelvic material of the finned elpistostegalian, Tiktaalik roseae, bridges some of these differences. Multiple isolated pelves have been recovered, each of which has been prepared in three dimensions. Likewise, a complete pelvis and partial pelvic fin have been recovered in association with the type specimen. The pelves of Tiktaalik are paired and have broad iliac processes, flat and elongate pubes, and acetabulae that form a deep socket rimmed by a robust lip of bone. The pelvis is greatly enlarged relative to other finned tetrapodomorphs. Despite the enlargement and robusticity of the pelvis of Tiktaalik, it retains primitive features such as the lack of both an attachment for the sacral rib and an ischium. The pelvic fin of Tiktaalik (NUFV 108) is represented by fin rays and three endochondral elements: other elements are not preserved. The mosaic of primitive and derived features in Tiktaalik reveals that the enhancement of the pelvic appendage of tetrapods and, indeed, a trend toward hind limb-based propulsion have antecedents in the fins of their closest relatives.

Propulsive Forces of Mudskipper Fins and Salamander Limbs during Terrestrial Locomotion: Implications for the Invasion of Land

The invasion of land was a pivotal event in vertebrate evolution that was associated with major appendicular modifications. Although fossils indicate that the evolution of fundamentally limb-like appendages likely occurred in aquatic environments, the functional consequences of using early digited limbs, rather than fins, for terrestrial propulsion have had little empirical investigation. Paleontological and experimental analyses both have led to the proposal of an early origin of "hind limb-driven" locomotion among tetrapods or their ancestors. However, the retention of a pectoral appendage that had already developed terrestrial adaptations has been proposed for some taxa, and few data are available from extant functional models that can provide a foundation for evaluating the relative contributions of pectoral and pelvic appendages to terrestrial support among early stem tetrapods. To examine these aspects of vertebrate locomotor evolution during the invasion of land, we measured three-dimensional ground reaction forces (GRFs) produced by isolated pectoral fins of mudskipper fishes (Periophthalmus barbarus) during terrestrial crutching, and compared these to isolated walking footfalls by the forelimbs and hind limbs of tiger salamanders (Ambystoma tigrinum), a species with subequally-sized limbs that facilitate comparisons to early tetrapods. Pectoral appendages of salamanders and mudskippers exhibited numerous differences in GRFs. Compared with salamander forelimbs, isolated fins of mudskippers bear lower vertical magnitudes of GRFs (as a proportion of body weight), and had GRFs that were oriented more medially. Comparing the salamanders' forelimbs and hind limbs, although the peak net GRF occurs later in stance for the forelimb, both limbs experience nearly identical mediolateral and vertical components of GRF, suggesting comparable contributions to support. Thus, forelimbs could also have played a significant locomotor role among basal tetrapods that had limbs of sub-equal size. However, the salamander hind limb and mudskipper pectoral fin had a greater acceleratory role than did the salamander forelimb. Together, data from these extant taxa help to clarify how structural change may have influenced locomotor function through the evolutionary invasion of land by vertebrates.

Descriptive Anatomy of the Pelvic Appendage Myology of the Endemic Chinese Grouse (Tetrastes sewerzowi)

The musculature of the pelvic appendage of the Chinese Grouse (Tetrastes sewerzowi) is described in detail. T. sewerzowi exhibits the same features as other tetraonids in the absence of M. adductor digiti II, and the relatively weak development of other intrinsic foot muscles, which are thought to be an adaptation to the extreme cold climate of the habitat of grouse. Myological modifications include weak development of the vincula between the flexor tendons to the digits (M. flexor perforans digiti III and M. flexor perforans et perforatus digiti III, M. flexor digitorum longus, and M. flexor hallus longus), the proximolateral insertion of M. flexor perforans digiti II, the well-developed middle head of M. flexor perforans digiti IV, and the ossification of the insertion tendon of M. extensor brevis digiti IV. These features are suggested to be associated with the requirement of finer control over the individual digits while moving on the tree, especially a thin branch.

Behavioral evidence for the evolution of walking and bounding before terrestriality in sarcopterygian fishes

Tetrapods evolved from sarcopterygian fishes in the Devonian and were the first vertebrates to colonize land. The locomotor component of this transition can be divided into four major events: terrestriality, the origins of digited limbs, solid substrate-based locomotion, and alternating gaits that use pelvic appendages as major propulsors. As the sister group to tetrapods, lungfish are a morphologically and phylogenetically relevant sarcopterygian taxon for understanding the order in which these events occurred. We found that a species of African lungfish (Protopterus annectens) uses a range of pelvic fin-driven, tetrapod-like gaits, including walking and bounding, in an aquatic environment, despite having a derived limb endoskeleton and primitively small, muscularly supported pelvis. Surprisingly, given these morphological traits, P. annectens also lifts its body clear of the substrate using its pelvic fins, an ability thought to be a tetrapod innovation. Our findings suggest that some fundamental features of tetrapod locomotion, including pelvic limb gait patterns and substrate association, probably arose in sarcopterygians before the origin of digited limbs or terrestriality. It follows that the attribution of some of the nondigited Devonian fossil trackways to limbed tetrapods may need to be revisited.