Reconstructing pectoral appendicular muscle anatomy in fossil fish and tetrapods over the fins‐to‐limbs transition

The question of how tetrapod limbs evolved from fins is one of the great puzzles of evolutionary biology. While palaeontologists, developmental biologists, and geneticists have made great strides in explaining the origin and early evolution of limb skeletal structures, that of the muscles remains largely unknown. The main reason is the lack of consensus about appendicular muscle homology between the closest living relatives of early tetrapods: lobe‐finned fish and crown tetrapods. In the light of a recent study of these homologies, we re‐examined osteological correlates of muscle attachment in the pectoral girdle, humerus, radius, and ulna of early tetrapods and their close relatives. Twenty‐nine extinct and six extant sarcopterygians were included in a meta‐analysis using information from the literature and from original specimens, when possible. We analysed these osteological correlates using parsimony‐based character optimization in order to reconstruct muscle anatomy in ancestral lobe‐finned fish, tetrapodomorph fish, stem tetrapods, and crown tetrapods. Our synthesis revealed that many tetrapod shoulder muscles probably were already present in tetrapodomorph fish, while most of the more‐distal appendicular muscles either arose later from largely undifferentiated dorsal and ventral muscle masses or did not leave clear correlates of attachment in these taxa. Based on this review and meta‐analysis, we postulate a stepwise sequence of specific appendicular muscle acquisitions, splits, and fusions that led from the ancestral sarcopterygian pectoral fin to the ancestral tetrapod forelimb. This sequence largely agrees with previous hypotheses based on palaeontological and comparative work, but it is much more comprehensive in terms of both muscles and taxa. Combined with existing information about the skeletal system, our new synthesis helps to illuminate the genetic, developmental, morphological, functional, and ecological changes that were key components of the fins‐to‐limbs transition.     

Computed tomography and magnetic resonance imaging studies of Latimeria chalumnae

Synopsis Recent radiologic imaging techniques (CT[Computed Tomography] and MRI[Magnetic Resonance Imaging]) were used to investigate the cranial anatomy of the coelacanth Latimeria chalumnae. The non-invasive CT and MRI techniques were performed successfully on a 1.45 m female specimen. This specimen had been frozen a year earlier for future research; the CT was conducted on the frozen animal, whereas the MRI method was performed immediately after thawing. The CT technique provides information about differential density of the organism (especially informative with respect to hard tissues, bone and cartilage), whereas three different types of MRI (proton resonance T₁, T₂ and flash) distinguish cartilage, muscles, and different connective tissues. A total of 381 CT cross sections (2 mm thick with 1 mm of overlap) through the head region were used in a computerized three-dimensional reconstruction program to address questions concerning cranial morphology. The results obtained from these radiologic imaging techniques confirmed most of the basic anatomy known from traditional dissections. However, the morphology of complex structures. such as the cartilaginous processes of the neurocranium, and the integration of the branchial arches and palate can only now be described more accurately.     

The oldest sarcopterygian fish

The study of basal sarcopterygians is crucial to an understanding of the relationships and interrelationships of sarcopterygians, including their relationship to tetrapods. The new material from Qujing, Yunnan, southwestern China, represents the oldest known sarcopterygian fish and extends the record of sarcopterygians to the Late Silurian, or about 410 Ma. The new form is close to Youngolepis and Powichthys at the base of the Crossopterygii. Similarities among the lower jaws of onychodonts, porolepiforms, Youngolepis, Powichthys and the new form support a position of onychodonts within the Crossopterygii. Four characters in the character matrix of Cloutier & Ahlberg (1996, in Stiassny et al: Interrelationships of Fishes , Academic Press) are reviewed, and sarcopterygian interrelationships are studied on the basis of their data with minor modifications. The new scheme of sarcopterygian interrelationships differs markedly from Cloutier & Ahlberg's scheme. Neither actinistians nor onychodonts are situated at the base of Sarcopterygii, but within the Crossopterygii. Youngolepis and Powichthys are at the base of the Crossopterygii, instead of being the sister group of dipnoans plus Diabolepis.     

LATE DEVONIAN (FAMENNIAN) LUNGFISHES FROM THE CATSKILL FORMATION OF PENNSYLVANIA, USA

Abstract:  Occurrences of fossil lungfishes (Dipnoi: Sarcopterygii) in the Famennian Catskill Formation of Pennsylvania are reviewed. A nearly complete dermal skull roof is assigned to a new genus and species, Apatorhynchus opistheretmus . Other recently discovered lungfish specimens include an incomplete postcranium similar to that of the Frasnian genus Fleurantia , a small parasphenoid of uncertain affinities, and isolated toothplates. Previously described dipnoan remains from the Catskill Formation include a partial skull roof of Soederberghia groenlandica , toothplates assigned to several species of Dipterus , a putative rostral or symphysial region placed in the problematic form taxon Ganorhynchus , and sedimentary structures interpreted as burrows. The toothplates attributed to Dipterus are indeterminate and are placed in open nomenclature, while the specimen identified as Ganorhynchus is not convincingly dipnoan. The status of the burrows remains uncertain pending the discovery of lungfish remains within these or similar structures in Catskill deposits. The distinct ichthyofaunas within the Catskill Formation and their lungfish components are briefly reviewed. Lungfishes are found in the Holoptychius - and Bothriolepis -dominated faunas common in the Catskill succession, as well as in the compositionally distinctive Red Hill assemblage. Many of the Devonian continental faunas that contain tetrapods also include long-snouted, denticle-bearing lungfishes ('rhynchodipterids', fleurantiids, or both). The composition of Late Devonian ichthyofaunas may have predictive qualities that will allow researchers to identify localities likely to produce the remains of early tetrapods.     

The Upper Devonian tetrapodomorph Gogonasus andrewsae from Western Australia: Reconstruction of the shoulder girdle and opercular series using X-ray Micro-Computed Tomography

The tetrapodomorph fish, Gogonasus andrewsae is a three dimensionally well-preserved sarcopterygian from the Gogo Formation (Frasnian, early Upper Devonian, ∼380 million years ago) in Western Australia. High-resolution X-ray Micro-Computed Tomography and 3D printouts were used to obtain a digital reconstruction of its shoulder girdle and opercular series. Our new findings show the opercular series in a close fit against the upper bones of the shoulder girdle only if the anocleithrum, supracleithrum and post-temporal are aligned more horizontally than in previous reconstructions. The lowermost subopercular bone also differs, in partly covering the clavicle of the shoulder girdle. The ascending process of the clavicle, and the ventral process of the anocleithrum, do not fit closely inside the cleithrum, and perhaps functioned for ligamentous attachment. A rugose area on the anocleithral process is in a similar relative position to the attachment of a muscle ligament on the shoulder girdle of various living actinopterygians. Our manipulation of 3D printouts permits testing of the morphological fit of extremely fragile acid-etched bones, and indicates a new way to investigate the constructional morphology of one or more mechanical units of the vertebrate skeleton. It is suggested that Micro-CT imaging, reconstruction, visualisation and 3D printing techniques will provide a rigorous new test leading to modification of previous reconstructions of extinct vertebrates that were based on graphical methods and 2D imaging.     

The ear region of Latimeria chalumnae: functional and evolutionary implications

The anatomy of Latimeria chalumnae has figured prominently in discussions about tetrapod origins. While the gross anatomy of Latimeria is well documented, relatively little is known about its otic anatomy and ontogeny. To examine the inner ear and the otoccipital part of the cranium, a serial-sectioned juvenile coelacanth was studied in detail and a three-dimensional reconstruction was made. The ear of Latimeria shows a derived condition compared to other basal sarcopterygians in having a connection between left and right labyrinths. This canalis communicans is perilymphatic in nature and originates at the transition point of the saccule and the lagena deep in the inner ear, where a peculiar sense end organ can be found. In most gnathostomes the inner ears are clearly separated from each other. A connection occurs in some fishes, e.g. within the Ostariophysi. In the sarcopterygian lineage no connections between the inner ears are known except in the Actinistia. Some fossil actinistians show a posteriorly directed duct lying between the foramen magnum and the notochordal canal, similar to the condition in the ear of Latimeria, so this derived character complex probably developed early in actinistian history. Because some features of the inner ear of Latimeria have been described as having tetrapod affinities, the problem of hearing and the anatomy of the otical complex in the living coelacanth has been closely connected to the question of early tetrapod evolution. It was assumed in the past that the structure found in Latimeria could exemplify a transitional stage in otic evolution between the fishlike sarcopterygians and the first tetrapods in a functional or even phylogenetic way. Here the possibility is considered that the canalis communicans does not possess any auditory function but rather is involved in sensing pressure changes during movements involving the intracranial joint. Earlier hypotheses of a putative tympanic ear are refuted.     

Comparative anatomy, homologies and evolution of the pectoral muscles of bony fish and tetrapods: a new insight

The Osteichthyes, including bony fishes and tetrapods, is a highly speciose group of vertebrates, comprising more than 42,000 living species. The anatomy of osteichthyans has been the subject of numerous comparative studies, but most of these studies concern osteological structures; much less attention has been paid to muscles. The most detailed comparative analyses of osteichthyan pectoral muscles that were actually based on a direct observation of representatives of various major actinopterygian and sarcopterygian groups were provided several decades ago by authors such as Howell and Romer. Despite the quality of their work, these authors did not have access to much information that is now available. In the present work, an updated discussion on the homologies and evolution of the osteichthyan pectoral muscles is provided, based on the authors' own analyses and on a survey of the literature, both old and recent. It is stressed that much caution should be taken when the results obtained in molecular and developmental studies concerning the pectoral muscles of model actinopterygians such as the teleostean zebrafish are discussed and compared with the results obtained in studies concerning model sarcopterygians from clades such as the Amphibia and/or the Amniota. This is because, as shown here, as a result of the different evolutionary routes followed within the actinopterygian and the sarcopterygian clades none of the individual muscles found, for example, in derived actinopterygians such as teleosts is found in derived sarcopterygians such as tetrapods. It is hoped that the information provided in the present work may help in paving the way for future analyses of the pectoral muscles in taxa from different osteichthyan groups and for a proper comparison between these muscles in those taxa.     

The hyomandibulae of rhizodontids (Sarcopterygii, stem-tetrapoda)

Despite its important role in the study of the evolution of tetrapods, the hyomandibular bone (the homologue of the stapes in crown-group tetrapods) is known for only a few of the fish-like members of the tetrapod stem-group. The best-known example, that of the tristichopterid Eusthenopteron, has been used as an exemplar of fish-like stem-tetrapod hyomandibula morphology, but in truth the conditions at the base of the tetrapod radiation remain obscure. We report, here, four hyomandibulae, from three separate localities, which are referable to the Rhizodontida, the most basal clade of stem-tetrapods. These specimens share a number of characteristics, and are appreciably different from the small number of hyomandibulae reported for other fish-like stem-tetrapods. While it is unclear if these characteristics represent synapomorphies or symplesiomorphies, they highlight the morphological diversity of hyomandibulae within the early evolution of the tetrapod total-group. Well-preserved muscle scarring on some of these hyomandibulae permit more robust inferences of hyoid arch musculature in stem-tetrapods.     

The Sensory Canal Systems of the Living Coelacanth, Latimeria Chalumnae: A New Instalment

Entire sensory canal systems of the coelacanth, Latimeria chalumnae, are described: not only the course of principal canals with their primary and secondary collaterals, but also the course and branches of the pit-line and reticular canals. The number of pores on the left side of the head were found to be 296 in an early (yolksac) embryo, 321 in a late term fetus, 485 in a juvenile, and 2974 in adults. This means that in latimeria most of the lateral-line canal system develop after parturition. Pit lines of the living coelacanth are not rows of superficial neuromasts but canals covered by a thin epidermis like in other sensory canals of the lateral line. These pit-line canals, however, have a very specific structure and branching pattern: the medial dorsal pit-line canal is connected by fine branches on top of the head. The infra-dentary pit-line canal connects via these branches with canals deep inside the bones. Several fine and richly branched canaliculi of unknown function radiate from each quadratojugal pit-line canal. The gular plate pit-line canal has superficially branching arms as well as connections to numerous deeper canals inside the bone. These canals consist of fine branches that in turn lead to and open on the ventral surface of the gular plates as small pores. The system is reminiscent of the reticular (pore) canal system known only from some fossil agnathans and fishes. Thus latimeria combines the reticular system of ancient vertebrates with the lateral-line system of modern fishes. The significance of this gular (possibly electro-sensory) system for feeding by the coelacanth will be discussed.