Catherine A. Boisvert

The pectoral fin of Panderichthys and the origin of digits

One of the identifying characteristics of tetrapods (limbed vertebrates) is the presence of fingers and toes. Whereas the proximal part of the tetrapod limb skeleton can easily be homologized with the paired fin skeletons of sarcopterygian (lobe-finned) fish, there has been much debate about the origin of digits. Early hypotheses interpreted digits as derivatives of fin radials, but during the 1990s the idea gained acceptance that digits are evolutionary novelties without direct equivalents in fish fin skeletons. This was partly based on developmental genetic data, but also substantially on the pectoral fin skeleton of the elpistostegid (transitional fish/tetrapod) Panderichthys, which appeared to lack distal digit-like radials. Here we present a CT scan study of an undisturbed pectoral fin of Panderichthys demonstrating that the plate-like ‘ulnare’ of previous reconstructions is an artefact and that distal radials are in fact present. This distal portion is more tetrapod-like than that found in Tiktaalik and, in combination with new data about fin development in basal actinopterygians, sharks and lungfish, makes a strong case for fingers not being a novelty of tetrapods but derived from pre-existing distal radials present in all sarcopterygian fish.

The pelvic fin and girdle of Panderichthys and the origin of tetrapod locomotion

One of the most marked transformations in the vertebrate transition to land was that of fins to limbs. This transformation involved not only the generation of morphological novelties (digits, sacrum) but also a shift in locomotory dominance from the pectoral to the pelvic appendage. Despite its importance, the transformation from pelvic fin to hindlimb is the least studied and least well-documented part of this transformation, which is bracketed by the osteolepiform Eusthenopteron and the early tetrapods Ichthyostega and Acanthostega, but is not directly illuminated by any intermediate form. Panderichthys is the closest tetrapod relative currently represented by complete fossils, but its pelvic fin skeleton has not been described. Here, I present the only known articulated pelvic fin endoskeleton and associated partial pelvis of Panderichthys. The pelvic girdle is even less tetrapod-like than that of the osteolepiform Eusthenopteron, but the pelvic fin endoskeleton shares derived characteristics with basal tetrapods despite being more primitive than the pectoral fin of Panderichthys. The evolution of tetrapod locomotion appears to have passed through a stage of body-flexion propulsion, in which the pelvic fins played a relatively minor anchoring part, before the emergence of hindlimb-powered propulsion in the interval between Panderichthys and Acanthostega.

Development and Evolution of the Muscles of the Pelvic Fin

Locomotor strategies in terrestrial tetrapods have evolved from the utilisation of sinusoidal contractions of axial musculature, evident in ancestral fish species, to the reliance on powerful and complex limb muscles to provide propulsive force. Within tetrapods, a hindlimb-dominant locomotor strategy predominates, and its evolution is considered critical for the evident success of the tetrapod transition onto land. Here, we determine the developmental mechanisms of pelvic fin muscle formation in living fish species at critical points within the vertebrate phylogeny and reveal a stepwise modification from a primitive to a more derived mode of pelvic fin muscle formation. A distinct process generates pelvic fin muscle in bony fishes that incorporates both primitive and derived characteristics of vertebrate appendicular muscle formation. We propose that the adoption of the fully derived mode of hindlimb muscle formation from this bimodal character state is an evolutionary innovation that was critical to the success of the tetrapod transition.

Fossil musculature of the most primitive jawed vertebrates

From Jawless to Jawed The earliest vertebrates were jawless. Past reconstructions have assumed that the primitive jawed condition was much like that found in sharks. Trinajstic et al. (p. 160, published online 13 June; see the Perspective by Kuratani) describe fossil musculature from the early jawed placoderms (an extinct class of armored prehistoric fish) that show that the basal structure was distinct from that found in sharks, having a notable dermal joint between the skull and shoulder girdle. Fossilized muscles in an ancient armored fish reveal a distinctive neck musculature that differs from that of sharks. [Also see Perspective by Kuratani] The transition from jawless to jawed vertebrates (gnathostomes) resulted in the reconfiguration of the muscles and skeleton of the head, including the creation of a separate shoulder girdle with distinct neck muscles. We describe here the only known examples of preserved musculature from placoderms (extinct armored fishes), the phylogenetically most basal jawed vertebrates. Placoderms possess a regionalized muscular anatomy that differs radically from the musculature of extant sharks, which is often viewed as primitive for gnathostomes. The placoderm data suggest that neck musculature evolved together with a dermal joint between skull and shoulder girdle, not as part of a broadly flexible neck as in sharks, and that transverse abdominal muscles are an innovation of gnathostomes rather than of tetrapods.

Lohest's true and false ‘Devonian amphibians’: evidence for the rhynchodipterid lungfish Soederberghia in the Famennian of Belgium

Abstract Remains from the Upper Devonian (Famennian) of Belgium attributed to an early ‘amphibian’ during the nineteenth century are reviewed. This putative tetrapod material is identified here as a rhynchodipterid lungfish, possibly Soederberghia, a genus previously known from the Upper Devonian of East Greenland, Pennsylvania, and Australia. Newly discovered material from Belgium is also attributed to this large, cosmopolitan lungfish genus. Remains attributed to ?Jarvikia, another long-snouted dipnoan from East Greenland, have also been recovered from Famennian strata in Belgium. These occurrences provide additional evidence for paleobiogeographical links between Greenland and the central southern coast of the Euramerican continent during the Late Devonian.

Pelvic and reproductive structures in placoderms (stem gnathostomes)

Newly discovered pelvic and reproductive structures within placoderms, representing some of the most crownward members of the gnathostome stem group and the most basal jawed vertebrates, challenge established ideas on the origin of the pelvic girdle and reproductive complexity. Here we critically review previous descriptions of the pelvic structures in placoderms and reinterpret the morphology of the pelvic region within the arthrodires and ptyctodonts, in particular the position of the pelvic fin and the relationship of the male clasper to the pelvic girdle. Absence of clear articular surfaces on the clasper and girdle in the Arthrodira, along with evidence from the Ptyctodontida, suggest that these are separate structures along the body. We describe similarities between the pectoral and pelvic girdles and claspers, for example, all these have both dermal and perichondral (cartilaginous) components. Claspers in placoderms and chondrichthyans develop in very different ways; in sharks, claspers develop from the pelvic fin while the claspers in placoderms develop separately, suggesting that their independent development involved a posterior extension of the ‘competent stripes’ for fin development previously limited to the region between the paired pectoral and pelvic fins. Within this expanded zone, we suggest that clasper position relative to the pelvic fins was determined by genes responsible for limb position. Information on early gnathostome reproductive processes is preserved in both the Ptyctodontida and Arthrodira, including the presence of multiple embryos in pregnant females, embryos of differing sizes and of different sexes (e.g. male claspers preserved in some embyros). By comparison with chondrichthyans, these observations suggest more complex reproductive strategies in placoderms than previously appreciated.

Comparative pelvic development of the axolotl (Ambystoma mexicanum) and the Australian lungfish (Neoceratodus forsteri): conservation and innovation across the fish-tetrapod transition

BackgroundThe fish-tetrapod transition was one of the major events in vertebrate evolution and was enabled by many morphological changes. Although the transformation of paired fish fins into tetrapod limbs has been a major topic of study in recent years, both from paleontological and comparative developmental perspectives, the interest has focused almost exclusively on the distal part of the appendage and in particular the origin of digits. Relatively little attention has been paid to the transformation of the pelvic girdle from a small unipartite structure to a large tripartite weight-bearing structure, allowing tetrapods to rely mostly on their hindlimbs for locomotion. In order to understand how the ischium and the ilium evolved and how the acetabulum was reoriented during this transition, growth series of the Australian lungfish Neoceratodus forsteri and the Mexican axolotl Ambystoma mexicanum were cleared and stained for cartilage and bone and immunostained for skeletal muscles. In order to understand the myological developmental data, hypotheses about the homologies of pelvic muscles in adults of Latimeria, Neoceratodus and Necturus were formulated based on descriptions from the literature of the coelacanth (Latimeria), the Australian Lungfish (Neoceratodus) and a salamander (Necturus).ResultsIn the axolotl and the lungfish, the chondrification of the pelvic girdle starts at the acetabula and progresses anteriorly in the lungfish and anteriorly and posteriorly in the salamander. The ilium develops by extending dorsally to meet and connect to the sacral rib in the axolotl. Homologous muscles develop in the same order with the hypaxial musculature developing first, followed by the deep, then the superficial pelvic musculature.ConclusionsDevelopment of the pelvic endoskeleton and musculature is very similar in Neoceratodus and Ambystoma. If the acetabulum is seen as being a fixed landmark, the evolution of the ischium only required pubic pre-chondrogenic cells to migrate posteriorly. It is hypothesized that the iliac process or ridge present in most tetrapodomorph fish is the precursor to the tetrapod ilium and that its evolution mimicked its development in modern salamanders.

Vertebral development of modern salamanders provides insights into a unique event of their evolutionary history

The origin of salamanders and their interrelationships to the two other modern amphibian orders (frogs and caecilians) are problematic owing to an 80-100 million year gap in the fossil record between the Carboniferous to the Lower Jurassic. This is compounded by a scarcity of adult skeletal characters linking the early representatives of the modern orders to their stem-group in the Paleozoic. The use of ontogenetic characters can be of great use in the resolution of these questions. Growth series of all ten modern salamander families (a 120 cleared and stained larvae) were examined for pattern and timing of vertebral elements chondrification and ossification. The primitive pattern is that of the neural arches developing before the centra, while the reverse represents the derived condition. Both the primitive and derived conditions are observed within the family Hynobiidae, whereas only the derived condition is observed in all other salamanders. This provides support to the claims that Hynobiidae is both the most basal of modern families and potentially polyphyletic (with Ranodon and Hybobius forming the most basal clade and Salamandrella being a part of the most derived clade). This provides insight into a unique event in salamander evolutionary history and suggests that the developmental pattern switch occurred between the Triassic and the mid-Jurassic before the last major radiation.

The Ancient Origins of Neural Substrates for Land Walking

Walking is the predominant locomotor behavior expressed by land-dwelling vertebrates, but it is unknown when the neural circuits that are essential for limb control first appeared. Certain fish species display walking-like behaviors, raising the possibility that the underlying circuitry originated in primitive marine vertebrates. We show that the neural substrates of bipedalism are present in the little skate Leucoraja erinacea, whose common ancestor with tetrapods existed ∼420 million years ago. Leucoraja exhibits core features of tetrapod locomotor gaits, including left-right alternation and reciprocal extension-flexion of the pelvic fins. Leucoraja also deploys a remarkably conserved Hox transcription factor-dependent program that is essential for selective innervation of fin/limb muscle. This network encodes peripheral connectivity modules that are distinct from those used in axial muscle-based swimming and has apparently been diminished in most modern fish. These findings indicate that the circuits that are essential for walking evolved through adaptation of a genetic regulatory network shared by all vertebrates with paired appendages. VIDEO ABSTRACT.

Oldest pathology in a tetrapod bone illuminates the origin of terrestrial vertebrates.

The origin of terrestrial tetrapods was a key event in vertebrate evolution, yet how and when it occurred remains obscure, due to scarce fossil evidence. Here, we show that the study of palaeopathologies, such as broken and healed bones, can help elucidate poorly understood behavioural transitions such as this. Using high-resolution finite element analysis, we demonstrate that the oldest known broken tetrapod bone, a radius of the primitive stem tetrapod Ossinodus pueri from the mid-Viséan (333 million years ago) of Australia, fractured under a high-force, impact-type loading scenario. The nature of the fracture suggests that it most plausibly occurred during a fall on land. Augmenting this are new osteological observations, including a preferred directionality to the trabecular architecture of cancellous bone. Together, these results suggest that Ossinodus, one of the first large (>2m length) tetrapods, spent a significant proportion of its life on land. Our findings have important implications for understanding the temporal, biogeographical and physiological contexts under which terrestriality in vertebrates evolved. They push the date for the origin of terrestrial tetrapods further back into the Carboniferous by at least two million years. Moreover, they raise the possibility that terrestriality in vertebrates first evolved in large tetrapods in Gondwana rather than in small European forms, warranting a re-evaluation of this important evolutionary event.