Placoderm fishes,pharyngeal denticles,and the vertebrate dentition

The correlation of the origin of teeth with jaws in vertebrate history has recently been challenged with an alternative to the canonical view of teeth deriving from separate skin denticles. This alternative proposes that organized denticle whorls on the pharyngeal (gill) arches in the fossil jawless fish Loganellia are precursors to tooth families developing from a dental lamina along the jaw, such as those occurring in sharks, acanthodians, and bony fishes. This not only indicates that homologs of tooth families were present, but also illustrates that they possessed the relevant developmental controls, prior to the evolution of jaws. However, in the Placodermi, a phylogenetically basal group of jawed fishes, the state of pharyngeal denticles is poorly known, tooth whorls are absent, and the presence of teeth homologous to those in extant jawed fishes (Chondrichthyes + Osteichthyes) is controversial. Thus, placoderms would seem to provide little evidence for the early evolution of dentitions, or of denticle whorls, or tooth families, at the base of the clade of jawed fishes. However, organized denticles do occur at the rear of the placoderm gill chamber, but are associated with the postbranchial lamina of the anterior trunkshield, assumed to be part of the dermal cover. Significantly, these denticles have a different organization and morphology relative to the external dermal trunkshield tubercles. We propose that they represent a denticulate part of the visceral skeleton, under the influence of pharyngeal patterning controls comparable to those for pharyngeal denticles in other jawed vertebrates and Loganellia.     

Origin and evolution of gnathostome dentitions: a question of teeth and pharyngeal denticles in placoderms

The fossil group Placodermi is the most phylogenetically basal of the clade of jawed vertebrates but lacks a marginal dentition comparable to that of the dentate Chondrichthyes, Acanthodii and Osteichthyes (crown-group Gnathostomata). The teeth of crown-group gnathostomes are part of an ordered dentition replaced from, and patterned by, a dental lamina, exemplified by the elasmobranch model. A dentition recognised by these criteria has been previously judged absent in placoderms, based on structural evidence such as absence of tooth whorls and typical vertebrate dentine. However, evidence for regulated tooth addition in a precise spatiotemporal order can be observed in placoderms, but significantly, only within the group Arthrodira. In these fossils, as in other jawed vertebrates with statodont, non-replacing dentitions, new teeth are added at the ends of rows below the bite, but in line with biting edges of the dentition. The pattern is different on each gnathal bone and probably arises from single odontogenic primordia on each, but tooth rows are arranged in a distinctive placoderm pattern. New teeth are made of regular dentine comparable to that of crown-gnathostomes, formed from a pulp cavity. This differs from semidentine previously described for placoderm gnathalia, a type present in the external dermal tubercles. The Arthrodira is a derived taxon within the Placodermi, hence origin of teeth in placoderms occurs late in the phylogeny and teeth are convergently derived, relative to those of other jawed vertebrates. More basal placoderm taxa adopted other strategies for providing biting surfaces and these vary substantially, but include addition of denticles to the growing gnathal plates, at the margins of pre-existing denticle patches. These alternative strategies and apparent absence of regular dentine have led to previous interpretations that teeth were entirely absent from the placoderm dentition. A consensus view emerged that a dentition, as developed within a dental lamina, is a synapomorphy characterising the clade of crown-group gnathostomes. Recent comparisons between sets of denticle whorls in the pharyngeal region of the jawless fish Loganellia scotica (Thelodonti) and those in sharks suggest homology of these denticle sets on gill arches. Although the placoderm pharyngeal region appears to lack denticles (placoderm gill arches are poorly known), the posterior wall of the pharyngeal cavity, formed by a bony flange termed the postbranchial lamina, is covered in rows of patterned denticle arrays. These arrays differ significantly, both in morphology and arrangement, from those of the denticles located externally on the head and trunkshield plates. Denticles in these arrays are homologous to denticles associated with the gill arches in other crown-gnathostomes, with pattern similarities for order and position of pharyngeal denticles. From their location in the pharynx these are inferred to be under the influence of a cell lineage from endoderm, rather than ectoderm. Tooth sets and tooth whorls in crown-group gnathostomes are suggested to derive from the pharyngeal denticle whorls, at least in sharks, with the patterning mechanisms co-opted to the oral cavity. A comparable co-option is suggested for the Placodermi.     

The scapulocoracoid of the Queensland lungfish Neoceratodus forsteri (Dipnoi: Sarcopterygii): morphology, development and evolutionary implications for bony fishes (Osteichthyes)

Among bony fishes, the ontogenetic sequence by which the actinopterygian scapulocoracoid develops has been well described, but that of the sarcopterygian scapulocoracoid is poorly known, as the majority of taxa are only known from fossils. To rectify this, the cartilaginous scapulocoracoid of the extant lungfish Neoceratodus forsteri is examined. In initial stages of its development, the scapulocoracoid of Neoceratodus has a simple rounded shape, and supports the glenoid fossa. It appears nearly contemporaneously with the proximal endochondral element (humerus) of the pectoral fin. Pectoral fin elements develop by segmentation from a continuous field of cartilaginous precursor cells extending distally from the glenoid region of the scapulocoracoid. Subsequent scapulocoracoid development produces a ventromedial process, which is not associated with this field of precursor cells. A dorsal process also develops outside this field. Thus, the scapulocoracoid of Neoceratodus may consist of at least two developmentally distinct regions; (1) the ventromedial being homologous with the coracoid of actinopterygians, tetrapods and other jawed vertebrates and (2) a smaller dorsal process, homologous to the scapular region. The two, together with the glenoid region, give an overall triangular shape. The scapulocoracoids of fossil lungfish and other sarcopterygian fishes are also triangular and are composed of scapular and coracoid regions, rather than the 'buttresses' associated with scapulocoracoids of the Actinopterygii and Tetrapoda.     

Number and arrangement of extraocular muscles in primitive gnathostomes: evidence from extinct placoderm fishes

Exceptional braincase preservation in some Devonian placoderm fishes permits interpretation of muscles and cranial nerves controlling eye movement. Placoderms are the only jawed vertebrates with anterior/posterior obliques as in the jawless lamprey, but with the same function as the superior/inferior obliques of other gnathostomes. Evidence of up to seven extraocular muscles suggests that this may be the primitive number for jawed vertebrates. Two muscles innervated by cranial nerve 6 suggest homologies with lampreys and tetrapods. If the extra muscle acquired by gnathostomes was the internal rectus, Devonian fossils show that it had a similar insertion above and behind the eyestalk in both placoderms and basal osteichthyans.     

Development of the paired fins in the paddlefish, Polyodon spathula

In Polyodon spathula, the pectoral fin radials, with the exception of the metapterygium, are derived from the decomposition of a single continuous cartilage fin plate that is continuous with the scapulocoracoid. This cartilage sheet develops two interior splits to form three precursor pieces, and these decompose in a predictable way to generate the propterygium and radials. The metapterygium is an extension of the scapulocoracoid that segments off of it during early development. To our knowledge, this has not been reported for acipenserids or other basal actinopterygians. In teleosts, the proximal radials also develop from the "break up" of an initially continuous paddle-like sheet of cartilage along the posterior edge of the scapulocoracoid, and in Polypterus and sharks a similar pattern holds. Thus, the pattern observed in Polyodon may represent the basal developmental condition for the gnathostome pectoral fin. The process underlying development of the superficially similar cartilages of the pelvic and pectoral fins is different. In the pectoral fin, the metapterygium is segmented off of the scapulocoracoid and other radials form from the decomposition of the cartilage plate. In contrast, individual rod-like basipterygial elements form in a close one-to-one correspondence with the middle radials of the pelvic fin, but later fuse to form an anterior element that is branched in appearance. To evaluate further claims of similarity among the pectoral and pelvic fin elements of various fishes, the course of the development of these structures must be observed. The pectoral fin and girdle in Polyodon ossifies in a different sequence than that proposed as ancestral (and highly conserved) for actinopterygians: the supracleithrum ossifies significantly before the cleithrum. The later ossification of the cleithrum in Polyodon may be related to the primary use of the caudal fin vs. the pectoral fins in their locomotion.     

Discriminating signal from noise in the fossil record of early vertebrates reveals cryptic evolutionary history

The fossil record of early vertebrates has been influential in elucidating the evolutionary assembly of the gnathostome bodyplan. Understanding of the timing and tempo of vertebrate innovations remains, however, mired in a literal reading of the fossil record. Early jawless vertebrates (ostracoderms) exhibit restriction to shallow-water environments. The distribution of their stratigraphic occurrences therefore reflects not only flux in diversity, but also secular variation in facies representation of the rock record. Using stratigraphic, phylogenetic and palaeoenvironmental data, we assessed the veracity of the fossil records of the jawless relatives of jawed vertebrates (Osteostraci, Galeaspida, Thelodonti, Heterostraci). Non-random models of fossil recovery potential using Palaeozoic sea-level changes were used to calculate confidence intervals of clade origins. These intervals extend the timescale for possible origins into the Upper Ordovician; these estimates ameliorate the long ghost lineages inferred for Osteostraci, Galeaspida and Heterostraci, given their known stratigraphic occurrences and stem–gnathostome phylogeny. Diversity changes through the Silurian and Devonian were found to lie within the expected limits predicted from estimates of fossil record quality indicating that it is geological, rather than biological factors, that are responsible for shifts in diversity. Environmental restriction also appears to belie ostracoderm extinction and demise rather than competition with jawed vertebrates.     

Ecomorphological correlates in ten species of subtropical seagrass fishes: diet and microhabitat utilization

Synopsis Ecomorphological correlates were sought among ten species of distantly related subtropical seagrass fishes. Morphometric data associated with feeding and microhabitat utilization were compared by principal components analysis, cluster analysis, and canonical correspondence analysis to dietary data. Morphology was generally a poor predictor of diet except for a group of mid-water planktotrophic filter feeders. Separation of the species along morphological axes appears to be related more to microhabitat utilization resulting in three major groups: (1) a group of planktotrophic, mid-water fishes specialized for cruising and seeking out evasive prey characterized by a compressed fusiform body, forked caudal fin, long, closely spaced gill rakers, short to intermediate! length pectoral fin, pointed pectoral fin, large lateral eye, short head, and a terminal or subterminal mouth; (2) slow swimming, less maneuverable epibenthic fishes that pick or suck their prey off the substrate. They are united by more rounded caudal and pectoral fins, and short or no gill rakers; and (3) a group of more mobile and maneuverable epibenthic foragers characterized by a more compressed, sub-gibbose body, long, pointed pectoral fins, forked caudal fins, large lateral eyes, subterminal mouth, and greater jaw protrusibility. Cases of convergence in trophic and microhabitat utilization characters were apparent in some of the groups.     

Bone vascularization and growth in placoderms (Vertebrata): The example of the premedian plate of Romundina stellina Ørvig, 1975

The Placodermi (armored jawed fishes), which appeared during the Lower Silurian and disappeared without leading any descendants at the end of the Famennian (Latest Devonian), have the highest diversity of known Devonian vertebrate groups. As phylogenetically basal gnathostomes (jawed vertebrates), they are potentially informative about primitive jawed vertebrate anatomy and origins. Until recently, the study of their internal or histological structures has required destructive methods such as sectioning or serial grinding. Recent advances in tomography and imaging technologies, especially through the increasing use of synchrotron phase contrast imaging for the study of fossils, allow us to reveal the inner structures of the fossil nondestructively and with unprecedented three-dimensional level of detail. Here, we present for the first time the prerostral anatomy of the small acanthothoracid Romundina stellina, one of the earliest and most basal placoderms. Phase contrast imaging allows us to reconstruct the vascularization and nerve canals of the premedian plate and adjacent parts of the skeleton three-dimensionally in great detail, providing important clues to the growth modes and biology of the animal.     

Paired fin skeletons and relationships of the fossil group Porolepiformes (Osteichthyes: Sardcopterygii)

The endoskeletal girdles, anocleithrum and paired fin supports of the porolepiform fish Glyptolepis (Osteichthyes: Sarcopterygii: Porolepiformes) are figured and described. The pectoral fin skeleton is known from the proximal part only and the pelvic fin skeleton is fragmentary, but the scapulocoracoid, anocleithrum and pelvic girdle can be reconstructed in their entirety. The anocleithrum is entirely subdermal. The pectoral fin skeleton in shown to be biserial, with a large number of axial mesomeres, whereas the pelvic fin contains fewer mesomeres and is strongly asymmetrical with very few postaxial radials. The scapulocoracoid is essentially similar to a reconstruction figured by Jarvik (1980), but has a more elongate glenoid; this has functional implications. The pelvic girdle consists of two separate halves as in Eusthenopteron, but differs from that genus in lacking dorsolateral rami. A brief survey of the evidence of paired fin structure in other porolepiform genera is carried out to establish whether the structures seen in Glyptolepis are likely to be representative for the Porolepiformes. A study of the morphology and muscle attachments of the paired fin skeletons indicates that the pattern of fin movement was significantly different from that in Neoceratodus. The fin supports and girdles of Glyptolepis are compared with those of other sarcopterygian groups as well as with actinopterygians, placoderms and sharks, in order to establish evolutionary polarities. Glyptolepis is shown to display a number of derived characters. The information gained from the comparison is used to construct a maximum parsimony cladogram, which places coelacanths as the sister group of porolepiforms + lungfishes, with the rhizodonts + tetrapods and osteolepiforms as successive sister groups of this clade. Characters of uncertain polarity are considered in the light of this cladogram. A comparison with recently published cladograms shows that none are completely compatible with the results from this study.     

Fossil fishes from china provide first evidence of dermal pelvic girdles in osteichthyans

Background

The pectoral and pelvic girdles support paired fins and limbs, and have transformed significantly in the diversification of gnathostomes or jawed vertebrates (including osteichthyans, chondrichthyans, acanthodians and placoderms). For instance, changes in the pectoral and pelvic girdles accompanied the transition of fins to limbs as some osteichthyans (a clade that contains the vast majority of vertebrates – bony fishes and tetrapods) ventured from aquatic to terrestrial environments. The fossil record shows that the pectoral girdles of early osteichthyans (e.g., Lophosteus, Andreolepis, Psarolepis and Guiyu) retained part of the primitive gnathostome pectoral girdle condition with spines and/or other dermal components. However, very little is known about the condition of the pelvic girdle in the earliest osteichthyans. Living osteichthyans, like chondrichthyans (cartilaginous fishes), have exclusively endoskeletal pelvic girdles, while dermal pelvic girdle components (plates and/or spines) have so far been found only in some extinct placoderms and acanthodians. Consequently, whether the pectoral and pelvic girdles are primitively similar in osteichthyans cannot be adequately evaluated, and phylogeny-based inferences regarding the primitive pelvic girdle condition in osteichthyans cannot be tested against available fossil evidence.

Methodology/Principal Findings

Here we report the first discovery of spine-bearing dermal pelvic girdles in early osteichthyans, based on a new articulated specimen of Guiyu oneiros from the Late Ludlow (Silurian) Kuanti Formation, Yunnan, as well as a re-examination of the previously described holotype. We also describe disarticulated pelvic girdles of Psarolepis romeri from the Lochkovian (Early Devonian) Xitun Formation, Yunnan, which resemble the previously reported pectoral girdles in having integrated dermal and endoskeletal components with polybasal fin articulation.

Conclusions/Significance

The new findings reveal hitherto unknown similarity in pectoral and pelvic girdles among early osteichthyans, and provide critical information for studying the evolution of pelvic girdles in osteichthyans and other gnathostomes.     

Early Evolution of the Vertebrate Eye—Fossil Evidence

Evidence of detailed brain morphology is illustrated and described for 400-million-year-old fossil skulls and braincases of early vertebrates (placoderm fishes). Their significance is summarized in the context of the historical development of knowledge of vertebrate anatomy, both before and since the time of Charles Darwin. These ancient extinct fishes show a unique type of preservation of the cartilaginous braincase and demonstrate a combination of characters unknown in other vertebrate species, living or extinct. The structure of the oldest detailed fossil evidence for the vertebrate eye and brain indicates a legacy from an ancestral segmented animal, in which the braincase is still partly subdivided, and the arrangement of nerves and muscles controlling eye movement was intermediate between the living jawless and jawed vertebrate groups. With their unique structure, these placoderms fill a gap in vertebrate morphology and also in the vertebrate fossil record. Like many other vertebrate fossils elucidated since Darwin’s time, they are key examples of the transitional forms that he predicted, showing combinations of characters that have never been observed together in living species.     

Endemicity and palaeobiogeography of the Osteostraci and Galeaspida: a test of scenarios of gnathostome evolution

Abstract: Armoured stem‐gnathostomes (jawless vertebrates previously termed ‘ostracoderms’) have long been assumed to exhibit strong endemicity. This assumption has underpinned their utility in many palaeobiogeographic studies as well as scenarios regarding the evolution and dominance of jawed vertebrates over their jawless relatives. The hypothesis of endemicity in stem‐gnathostomes is investigated for the first time in the light of the phylogeny of the closest relatives of jawed vertebrates – Osteostraci and Galeaspida. Palaeobiogeography of each is reconstructed using Fitch optimization and modified Brooks Parsimony Analysis. Palaeobiogeographic distributions corroborate phylogeny. Results, along with consideration of the Heterostraci, enable identification of similar patterns across groups (broad ancestral range, Early Devonian expansion, endemic and pandemic clades within each, and Middle Devonian radiation events) and inferences to the palaeogeographic relationship between major terranes (i.e. Laurentia, Baltica, Avalonia, Kara, Altaids, South China, Tarim). Comparison of basin and terrane level analyses identifies the different palaeogeographic processes responsible for the distributions of each group: sea‐level changes in the case of the Osteostraci and rifting in the case of the Galeaspida. The general endemic nature of the Osteostraci and Galeaspida is confirmed, and thus the hypothesis that the demise and extinction of stem‐gnathostomes was because of their limited dispersal capacity is supported.     

The characters of Palaeozoic jawed vertebrates

Newly discovered fossils from the Silurian and Devonian periods are beginning to challenge embedded perceptions about the origin and early diversification of jawed vertebrates (gnathostomes). Nevertheless, an explicit cladistic framework for the relationships of these fossils relative to the principal crown lineages of the jawed vertebrates (osteichthyans: bony fishes and tetrapods; chondrichthyans: sharks, batoids, and chimaeras) remains elusive. We critically review the systematics and character distributions of early gnathostomes and provide a clearly stated hierarchy of synapomorphies covering the jaw‐bearing stem gnathostomes and osteichthyan and chondrichthyan stem groups. We show that character lists, designed to support the monophyly of putative groups, tend to overstate their strength and lack cladistic corroboration. By contrast, synapomorphic hierarchies are more open to refutation and must explicitly confront conflicting evidence. Our proposed synapomorphy scheme is used to evaluate the status of the problematic fossil groups Acanthodii and Placodermi, and suggest profitable avenues for future research. We interpret placoderms as a paraphyletic array of stem‐group gnathostomes, and suggest what we regard as two equally plausible placements of acanthodians: exclusively on the chondrichthyan stem, or distributed on both the chondrichthyan and osteichthyan stems. © 2014 The Authors. Zoological Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of The Linnean Society of London     

Observations on Ctenurella (Ptyctodontida) and the classification of placoderm fishes

The structure of the hyoid arch of the ptyctodont Ctenurella is described and discussed with reference to theories of jaw suspension in placoderm fishes. It is concluded that primitive placoderms had a modified hyoid arch but that the hyomandibular took no direct role in supporting the jaws. The relationships of ptyctodonts are discussed and it is concluded that they are placoderm fishes. Several different classifications of placoderm fishes are evaluated and are shown to be weakly based, chiefly because of lack of precise knowledge of character distribution. An attempt is made to produce a classification by using a simple cladistic computer analysis. The result highlights homoplasy in character distribution amongst traditionally recognized placoderm groups.     

First Shark from the Late Devonian (Frasnian) Gogo Formation,Western Australia Sheds New Light on the Development of Tessellated Calcified Cartilage

BackgroundLiving gnathostomes (jawed vertebrates) comprise two divisions, Chondrichthyes (cartilaginous fishes, including euchondrichthyans with prismatic calcified cartilage, and extinct stem chondrichthyans) and Osteichthyes (bony fishes including tetrapods). Most of the early chondrichthyan (‘shark’) record is based upon isolated teeth, spines, and scales, with the oldest articulated sharks that exhibit major diagnostic characters of the group—prismatic calcified cartilage and pelvic claspers in males—being from the latest Devonian, c. 360 Mya. This paucity of information about early chondrichthyan anatomy is mainly due to their lack of endoskeletal bone and consequent low preservation potential.Conclusions/SignificanceThe Meckel’s cartilages show a jaw articulation surface dominated by an expansive cotylus, and a small mandibular knob, an unusual condition for chondrichthyans. The scapulocoracoid of the new specimen shows evidence of two pectoral fin basal articulation facets, differing from the standard condition for early gnathostomes which have either one or three articulations. The tooth structure is intermediate between the ‘primitive’ ctenacanthiform and symmoriiform condition, and more derived forms with a euselachian-type base. Of special interest is the highly distinctive type of calcified cartilage forming the endoskeleton, comprising multiple layers of nonprismatic subpolygonal tesserae separated by a cellular matrix, interpreted as a transitional step toward the tessellated prismatic calcified cartilage that is recognized as the main diagnostic character of the chondrichthyans.     

Evolution and development of the synarcual in early vertebrates

The synarcual is a structure incorporating the anterior vertebrae of the axial skeleton and occurs in vertebrate taxa such as the fossil group Placodermi and the Chondrichthyes (Holocephali, Batoidea). Although the synarcual varies morphologically in these groups, it represents the first indication, phylogenetically, of a differentiation of the vertebral column into separate regions. Among the placoderms, the synarcual of Cowralepis mclachlani Ritchie, 2005 (Arthrodira) shows substantial changes during ontogeny to produce an elongate, spool-shaped structure with a well-developed dorsal keel. Because the placoderm synarcual is covered in perichondral bone, the ontogenetic history of this Cowralepis specimen is preserved as it developed anteroposteriorly, dorsally and ventrally. As well, in the placoderm Materpiscis attenboroughi Long et al., 2008 (Ptyctodontida), incomplete fusion at the posterior synarcual margin indicates that both neural and haemal arch vertebral elements are added to the synarcual. A survey of placoderm synarcuals shows that taxa such as Materpiscis and Cowralepis are particularly informative because perichondral ossification occurs prior to synarcual fusion such that individual vertebral elements can be identified. In other placoderm synarcuals (e.g. Nefudina qalibahensis Lelièvre et al., 1995; Rhenanida), cartilaginous vertebral elements fuse prior to perichondral ossification so that individual elements are more difficult to recognize. This ontogenetic development in placoderms can be compared to synarcual development in Recent chondrichthyans; the incorporation of neural and haemal elements is more similar to the holocephalans, but differs from the batoid chondrichthyans.