Alan Pradel

Skull and brain of a 300-million-year-old chimaeroid fish revealed by synchrotron holotomography

Living cartilaginous fishes, or chondrichthyans, include numerous elasmobranch (sharks and rays) species but only few chimaeroid (ratfish) species. The early history of chimaeroids, or holocephalans, and the modalities of their divergence from elasmobranchs are much debated. During Carboniferous times, 358–300 million years (Myr) ago, they underwent a remarkable evolutionary radiation, with some odd and poorly understood forms, including the enigmatic iniopterygians that were known until now from poorly informative flattened impressions. Here, we report iniopterygian skulls found preserved in 3 dimensions in ≈300-Myr-old concretions from Oklahoma and Kansas. The study was performed by using conventional X-ray microtomography (μCT), as well as absorption-based synchrotron microtomography (SR-μCT) [Tafforeau P, et al. (2006) Applications of X-ray synchrotron microtomography for non-destructive 3D studies of paleontological specimens. Appl Phys A 83:95–202] and a new holotomographic approach [Guigay P, Langer M, Boistel R, Cloetens P (2007) Mixed transfer function and transport of intensity approach for phase retrieval in the Fresnel region. Opt Lett 32:1617–1619], which revealed their peculiar anatomy. Iniopterygians also share unique characters with living chimaeroids, suggesting that the key chimaeroid skull features were already established 300 Myr ago. Moreover, SR-μCT of an articulated skull revealed a strikingly brain-shaped structure inside the endocranial cavity, which seems to be an exceptional case of soft-tissue mineralization of the brain, presumably as a result of microbially induced postmortem phosphatization. This was imaged with exceptional accuracy by using holotomography, which demonstrates its great potential to image preserved soft parts in dense fossils.

A New Paleozoic Symmoriiformes (Chondrichthyes) from the Late Carboniferous of Kansas (USA) and Cladistic Analysis of Early Chondrichthyans

Background The relationships of cartilaginous fishes are discussed in the light of well preserved three-dimensional Paleozoic specimens. There is no consensus to date on the interrelationship of Paleozoic chondrichthyans, although three main phylogenetic hypotheses exist in the current literature: 1. the Paleozoic shark-like chondrichthyans, such as the Symmoriiformes, are grouped along with the modern sharks (neoselachians) into a clade which is sister group of holocephalans; 2. the Symmoriiformes are related to holocephalans, whereas the other Paleozoic shark-like chondrichthyans are related to neoselachians; 3. many Paleozoic shark-like chondrichthyans, such as the Symmoriiformes, are stem chondrichthyans, whereas stem and crown holocephalans are sister group to the stem and crown neoselachians in a crown-chondrichthyan clade. This third hypothesis was proposed recently, based mainly on dental characters. Methodology/Principal Findings On the basis of two well preserved chondrichthyan neurocrania from the Late Carboniferous of Kansas, USA, we describe here a new species of Symmoriiformes, Kawichthys moodiei gen. et sp. nov., which was investigated by means of computerized X-ray synchrotron microtomography. We present a new phylogenetic analysis based on neurocranial characters, which supports the third hypothesis and corroborates the hypothesis that crown-group chondrichthyans (Holocephali+Neoselachii) form a tightly-knit group within the chondrichthyan total group, by providing additional, non dental characters. Conclusions/Significance Our results highlight the importance of new well preserved Paleozoic fossils and new techniques of observation, and suggest that a new look at the synapomorphies of the crown-group chondrichthyans would be worthwhile in terms of understanding the adaptive significance of phylogenetically important characters.

The buccohypophyseal canal is an ancestral vertebrate trait maintained by modulation in sonic hedgehog signaling

BackgroundThe pituitary gland is formed by the juxtaposition of two tissues: neuroectoderm arising from the basal diencephalon, and oral epithelium, which invaginates towards the central nervous system from the roof of the mouth. The oral invagination that reaches the brain from the mouth is referred to as Rathke’s pouch, with the tip forming the adenohypophysis and the stalk disappearing after the earliest stages of development. In tetrapods, formation of the cranial base establishes a definitive barrier between the pituitary and oral cavity; however, numerous extinct and extant vertebrate species retain an open buccohypophyseal canal in adulthood, a vestige of the stalk of Rathke’s pouch. Little is currently known about the formation and function of this structure. Here we have investigated molecular mechanisms driving the formation of the buccohypophyseal canal and their evolutionary significance.ResultsWe show that Rathke’s pouch is located at a boundary region delineated by endoderm, neural crest-derived oral mesenchyme and the anterior limit of the notochord, using CD1, R26R-Sox17-Cre and R26R-Wnt1-Cre mouse lines. As revealed by synchrotron X-ray microtomography after iodine staining in mouse embryos, the pouch has a lobulated three-dimensional structure that embraces the descending diencephalon during pituitary formation. Polarisfl/fl; Wnt1-Cre, Ofd1-/- and Kif3a-/- primary cilia mouse mutants have abnormal sonic hedgehog (Shh) signaling and all present with malformations of the anterior pituitary gland and midline structures of the anterior cranial base. Changes in the expressions of Shh downstream genes are confirmed in Gas1-/- mice. From an evolutionary perspective, persistence of the buccohypophyseal canal is a basal character for all vertebrates and its maintenance in several groups is related to a specific morphology of the midline that can be related to modulation in Shh signaling.ConclusionThese results provide insight into a poorly understood ancestral vertebrate structure. It appears that the opening of the buccohypophyseal canal depends upon Shh signaling and that modulation in this pathway most probably accounts for its persistence in phylogeny.

A Palaeozoic shark with osteichthyan-like branchial arches

The evolution of serially arranged, jointed endoskeletal supports internal to the gills—the visceral branchial arches—represents one of the key events in early jawed vertebrate (gnathostome) history, because it provided the morphological basis for the subsequent evolution of jaws. However, until now little was known about visceral arches in early gnathostomes, and theories about gill arch evolution were driven by information gleaned mostly from both modern cartilaginous (chondrichthyan) and bony (osteichthyan) fishes. New fossil discoveries can profoundly affect our understanding of evolutionary history, by revealing hitherto unseen combinations of primitive and derived characters. Here we describe a 325 million year (Myr)-old Palaeozoic shark-like fossil that represents, to our knowledge, the earliest identified chondrichthyan in which the complete gill skeleton is three-dimensionally preserved in its natural position. Its visceral arch arrangement is remarkably osteichthyan-like, suggesting that this may represent the common ancestral condition for crown gnathostomes. Our findings thus reinterpret the polarity of some arch features of the crown jawed vertebrates and invert the classic hypothesis, in which modern sharks retain the ancestral condition. This study underscores the importance of early chondrichthyans in resolving the evolutionary history of jawed vertebrates.

Jaws for a spiral-tooth whorl: CT images reveal novel adaptation and phylogeny in fossil Helicoprion

New CT scans of the spiral-tooth fossil, Helicoprion, resolve a longstanding mystery concerning the form and phylogeny of this ancient cartilaginous fish. We present the first three-dimensional images that show the tooth whorl occupying the entire mandibular arch, and which is supported along the midline of the lower jaw. Several characters of the upper jaw show that it articulated with the neurocranium in two places and that the hyomandibula was not part of the jaw suspension. These features identify Helicoprion as a member of the stem holocephalan group Euchondrocephali. Our reconstruction illustrates novel adaptations, such as lateral cartilage to buttress the tooth whorl, which accommodated the unusual trait of continuous addition and retention of teeth in a predatory chondrichthyan. Helicoprion exemplifies the climax of stem holocephalan diversification and body size in Late Palaeozoic seas, a role dominated today by sharks and rays.

Holocephalan embryo provides new information on the evolution of the glossopharyngeal nerve, metotic fissure and parachordal plate in gnathostomes.

The phylogenetic relationships between the different groups of Paleozoic gnathostomes are still debated, mainly because of incomplete datasets on Paleozoic jawed vertebrate fossils and ontogeny of some modern taxa. This issue is illustrated by the condition of the glossopharyngeal nerve relative to the parachordal plate, the otic capsules and the metotic fissure in gnathostomes. Two main conditions are observed in elasmobranchs (shark and rays) and osteichthyans (bony fishes and tetrapods). The condition in the other chondrichthyan taxon, the holocephalans, is still poorly known, and without any information on this taxon, it remains difficult to polarize the condition in gnathostomes. Based on the anatomical study of an embryo of the holocephalan Callorhinchus milii by means of propagation X-Ray Synchrotron phase contrast microtomography using both holotomography and single distance phase retrieval process, we show that, contrary to what was previously inferred for holocephalans (i.e. an osteichthyan-like condition), the arrangement of the glossopharyngeal nerve relative to the surrounding structure in holocephalans is more similar to that of elasmobranchs. Furthermore, the holocephalan condition represents a combination of plesiomorphic characters for gnathostomes (e.g., the glossopharyngeal nerve leaves the braincase via the metotic fissure) and homoplastic characters. By contrast, the crown osteichthyans are probably derived in having the glossopharyngeal nerve that enters the saccular chamber and in having the glossopharyngeal foramen separated from the metotic fissure.

Pectoral Morphology in Doliodus: Bridging the ‘Acanthodian’-Chondrichthyan Divide

ABSTRACT Doliodus problematicus (NBMG 10127), from the Lower Devonian of New Brunswick, Canada (approx. 397–400 Mya) is the earliest sharklike jawed vertebrate (gnathostome) in which the pectoral girdle and fins are well preserved. Its pectoral endoskeleton included sharklike expanded paired coracoids, but Doliodus also possessed an “acanthodian-like” array of dermal spines, described here for the first time. Doliodus provides the strongest anatomical evidence to date that chondrichthyans arose from “acanthodian” fishes by exhibiting an anatomical mosaic of “acanthodian” and sharklike features.

Eating with a saw for a jaw: Functional morphology of the jaws and tooth-whorl in Helicoprion davisii

The recent reexamination of a tooth‐whorl fossil of Helicoprion containing intact jaws shows that the symphyseal tooth‐whorl occupies the entire length of Meckels cartilage. Here, we use the morphology of the jaws and tooth‐whorl to reconstruct the jaw musculature and develop a biomechanical model of the feeding mechanism in these early Permian predators. The jaw muscles may have generated large bite‐forces; however, the mechanics of the jaws and whorl suggest that Helicoprion was better equipped for feeding on soft‐bodied prey. Hard shelled prey would tend to slip anteriorly from the closing jaws due to the curvature of the tooth‐whorl, lack of cuspate teeth on the palatoquadrate (PQ), and resistance of the prey. When feeding on soft‐bodied prey, deformation of the prey traps prey tissue between the two halves of the PQ and the whorl. The curvature of the tooth‐whorl and position of the exposed teeth relative to the jaw joint results in multiple tooth functions from anterior to posterior tooth that aid in feeding on soft‐bodied prey. Posterior teeth cut and push prey deeper into the oral cavity, while middle teeth pierce and cut, and anterior teeth hook and drag more of the prey into the mouth. Furthermore, the anterior‐posterior edges of the teeth facilitate prey cutting with jaw closure and jaw depression. The paths traveled by each tooth during jaw depression are reminiscent of curved pathways used with slashing weaponry such as swords and knifes. Thus, the jaws and tooth‐whorl may have formed a multifunctional tool for capturing, processing, and transporting prey by cyclic opening and closing of the lower jaw in a sawing fashion. J. Morphol. 276:47–64, 2015.

1 - Elasmobranchs and Their Extinct Relatives: Diversity, Relationships, and Adaptations Through Time

1. Introduction 2. Systematic and Phylogenetic Framework of Chondrichthyan Diversity 2.1. Names, Taxa, and Characters 2.2. Chondrichthyan Diversity and Interrelationships 3. Environments and Adaptations 4. Conclusion Current views about chondrichthyan phylogeny and systematics are briefly reviewed, with particular reference to the living and fossil taxa that are, or have been, once referred to as “elasmobranchs.” Recent reviews of early fossil chondrichthyans suggest that the last common ancestor of the living elasmobranchs and holocephalans probably lived by the end of the Devonian period, about 370–380 Myr ago, but a number of Paleozoic, shark-like chondrichthyans are currently regarded as stem chondrichthyans that diverged before the last common ancestor of all living taxa. Stem holocephalans display an amazing morphological diversity that reflects adaptations to very diverse benthic habitats. By contrast, both stem elasmobranchs and stem chondrichthyans are generally shark-like and were probably adapted to a pelagic mode of life. The earliest evidence for tessellated prismatic calcified cartilage, the “signature” of euchondrichthyans (i.e., all chondrichthyans which possess tessellated calcified prismatic cartilage), is about 400 Myr old, but scales and teeth tentatively assigned to chondrichthyans have been recorded from earlier periods. The “acanthodians,” a paraphyletic ensemble of Paleozoic fishes known since about 445 Myr are currently regarded as possible stem chondrichthyans that diverged before the rise of euchondrichthyans.

First evidence of an intercalar bone in the braincase of “palaeonisciform” actinopterygians, with a virtual reconstruction of a new braincase of Lawrenciella Poplin, 1984 from the Carboniferous of Oklahoma

ABSTRACT n We describe here a new Lawrenciella Poplin, 1984 specimen from the Upper Carboniferous (Missourian, Pennsylvanian) from Oklahoma, USA. This specimen is three dimensionnally preserved in a phosphatic nodule. It was scanned by X-Ray microtomography. The neurocranium shows some morphological differences from Lawrenciella schaefferi Poplin, 1984, which might represent individual variability. The parasphenoid and a pair of intercalar bones are associated with the braincase. The presence of intercalars as an anterior extension covering the otico-occipital fissure have not been yet documented in “paleonisciforms” and may have a phylogenetic signal. A discussion about the evolutionary role of such intercalars in the closure of the otico-occipital fissure in modern actinopterygians is provided.