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.     

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.     

Histology of “placoderm” dermal skeletons: Implications for the nature of the ancestral gnathostome

The vertebrate dermal skeleton has long been interpreted to have evolved from a primitive condition exemplified by chondrichthyans. However, chondrichthyans and osteichthyans evolved from an ancestral gnathostome stem‐lineage in which the dermal skeleton was more extensively developed. To elucidate the histology and skeletal structure of the gnathostome crown‐ancestor we conducted a histological survey of the diversity of the dermal skeleton among the placoderms, a diverse clade or grade of early jawed vertebrates. The dermal skeleton of all placoderms is composed largely of a cancellar architecture of cellular dermal bone, surmounted by dermal tubercles in the most ancestral clades, including antiarchs. Acanthothoracids retain an ancestral condition for the dermal skeleton, and we record its secondary reduction in antiarchs. We also find that mechanisms for remodeling bone and facilitating different growth rates between adjoining plates are widespread throughout the placoderms. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

Romundina and the evolutionary origin of teeth

Theories on the origin of vertebrate teeth have long focused on chondrichthyans as reflecting a primitive condition—but this is better informed by the extinct placoderms, which constitute a sister clade or grade to the living gnathostomes. Here, we show that ‘supragnathal’ toothplates from the acanthothoracid placoderm Romundina stellina comprise multi-cuspid teeth, each composed of an enameloid cap and core of dentine. These were added sequentially, approximately circumferentially, about a pioneer tooth. Teeth are bound to a bony plate that grew with the addition of marginal teeth. Homologous toothplates in arthrodire placoderms exhibit a more ordered arrangement of teeth that lack enameloid, but their organization into a gnathal, bound by layers of cellular bone associated with the addition of each successional tooth, is the same. The presence of enameloid in the teeth of Romundina suggests that it has been lost in other placoderms. Its covariation in the teeth and dermal skeleton of placoderms suggests a lack of independence early in the evolution of jawed vertebrates. It also appears that the dentition—manifest as discrete gnathal ossifications—was developmentally discrete from the jaws during this formative episode of vertebrate evolution.     

Histological structure of the cancellous bone layer in Bothriolepis canadensis (Antiarchi, Placodermi)

The Placodermi are extinct basal gnathostomes which had extensive dermal and perichondral bone, but which lacked the endochondral bone which characterizes the more derived bony fishes. Thin sections of bone from a specimen of the antiarch placoderm Bothriolepis canadensis, from the Escuminac Formation (Frasnian, Upper Devonian), Québec, Canada, reveal that part of the cancellous layer in its dermal and endoskeletal bone formed from perichondral bone trabeculae growing around cartilage spheres. The resultant structure mimics that of osteichthyan endochondral bone. The layout and dimensions of this polygonal mosaic patterning of the bone trabeculae and flattened cartilage spheres resemble those of the prismatic layers of calcified cartilage in chondrichthyans. If the lack of endoskeletal bone in chondrichthyans is a derived character, then the structure identified in B. canadensis could represent a 'template' for the formation of prismatic calcified cartilage in the absence of bone.     

The phyllolepid placoderm Cowralepis mclachlani: Insights into the evolution of feeding mechanisms in jawed vertebrates

Remarkably preserved specimens of Cowralepis mclachlani Ritchie, 2005 (Proc Linn Soc NSW 126:215–259) (Phyllolepida, Placodermi) represent a unique ontogenetic sequence adding to our understanding of anatomy, function, and phylogeny among basal jawed vertebrates (gnathostomes). A systematic review demonstrates that the Phyllolepida are a subgroup of the Arthrodira. Consideration of visceral and neurocranial characters supports the hypothesis that placoderms are the sister group to remaining gnathostomes. Placoderms possess, as adult plesiomorphic features, a number of characters that are only seen in the development of extant gnathostomes—a peramorphic shift relative to placoderms. Developmental evidence in vertebrates leads to a revised polarity of character transitions. These include 1) hyomandibula‐neurocranium and ventral parachordal‐palatoquadrate articulations (vertebrate synapomorphies); 2) jointed pharynx, paired basibranchials, anterior ethmoidal‐palatoquadrate articulation, short trabeculae cranii, and anterior and posterior neurocranial fissures (gnathostome synapomorphies); and 3) fused basibranchials, dorsal palatoquadrate‐neurocranium articulation, loss of the anterior neurocranial fissure, elongated trabeculae cranii, and transfer of the ventral parachordal‐palatoquadrate articulation to the trabeculae (crown group gnathostomes). The level of preservation in C. mclachlani provides the basis for a reinterpretation of phyllolepid anatomy and function. Cowralepis mclachlani possesses paired basibranchials allowing the reinterpretation of the visceral skeleton in other placoderms. Mandible depression in C. mclachlani follows an osteichthyan pattern and the ventral visceral skeleton acts as a functional unit. Evidence for hypobranchial musculature demonstrates the neural crest origin of the basibranchials and that Cowralepis was a suction feeder. Finally, the position of the visceral skeleton relative to the neurocranium in placoderms parallels the condition in selachians and osteichthyans, but differs in the elongation of the occiput. The cucullaris fossa of placoderms (interpreted as a site of muscle attachment) is shown to represent, in part, the parabranchial chamber. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

Exceptional preservation of nerve and muscle tissues in Late Devonian placoderm fish and their evolutionary implications

In this paper, we show exceptional three-dimensionally preserved fossilized muscle tissues in 380–384Myr old placoderm fish (Late Devonian), offering new morphological evidence supporting the hypothesis that placoderms are the sister group to all other gnathostomes. We describe the oldest soft tissue discovered in gnathostomes, which includes striated muscle fibres, circulatory and nerve tissues, preserved as phosphatized structures precipitated by microbial infilling of small, protected areas under the headshield of the arthrodire, Eastmanosteus calliaspis. Muscle impressions have also been found in the ptyctodontid, Austroptyctodus gardineri. The specimens display primitive vertebrate muscle structures; in particular, shallow W-shaped muscle blocks such as those observed in lampreys. New information from fossilized soft tissues thus elucidates the affinities of the placoderms and provides new insights into the evolution and radiation of gnathostomes.     

The hyoid arch and braincase anatomy of Acanthodes support chondrichthyan affinity of ‘acanthodians’

Solving the evolutionary relationships of the acanthodians is one of the key problems in reconstructing ancestral anatomical conditions for the jawed vertebrates (gnathostomes). Current debate concerns whether acanthodians are an assemblage of stem chondrichthyans, or a more generalized grade encompassing some early stem osteichthyans. The skull anatomy of Acanthodes bronni has been pivotal in these debates, owing to tension between chondrichthyan- and osteichthyan-like models of reconstruction. We use computed tomography scanning and traditional palaeontological techniques to resolve the long-standing debate about the anatomy of the jaw suspension. We establish the correct length of the hyomandibula and show that it attaches to a process on the ventrolateral angle of the braincase below the jugular vein groove. This condition corresponds precisely to that in chondrichthyans. This character represents an unambiguously optimized synapomorphy with chondrichthyans given current gnathostome phylogenies, corroborating the growing consensus of the chondrichthyan affinity of acanthodians.     

Fossilized ontogenies: the contribution of placoderm ontogeny to our understanding of the evolution of early gnathostomes

Placoderms, representing phylogenetically more inclusive jawed vertebrates and successive sister taxa to crown‐group gnathostomes, are critical to our understanding of character evolution within the crown‐group (chondrichthyans + osteichthyans), including developmental characters. Early ontogenetic stages of placoderms are generally poorly known, although some exceptional faunas preserve both embryonic (e.g. from the Gogo Formation, Western Australia) and post‐embryonic individuals (the Miguasha Formation, Canada; Lode Formation, Latvia; Merriganowry Formation, Gogo Formation, Australia). Information provided by these ontogenies is relevant to questions of placoderm taxonomy and phylogeny, but also to broader questions pertinent to vertebrate evolution as a whole, for example, evolution of bone development, evolution of the axial skeleton and evolution of reproduction.     

HEADS AND TAILS: A CHORDATE PHYLOGENY

Abstract— A cladistic analysis of chordates is presented, based on some 320 nested characters. All the principal higher taxa are defined by synapomorphies, including extinct acanthodians and placoderms. The data base draws broadly from adult anatomy (including osteological data for Recent and fossil taxa), embryology, physiology, and biochemistry. A conventional sequence of chordate higher taxa is generated (hemichordates, urochordates, cephalochordates, craniates). Among the craniates, cyclostomes are considered paraphyletic. Gnathostomes are monophyletic, but two fossil "agnathan" groups (galeaspids, osteostracans) are regarded as stem gnathostomes. Chondrichthyans and osteichthyans are monophyletic. New arguments for osteichthyan affinity of acanthodians are presented. The phylogenetic position of placoderms is still problematic, but they can no longer be perceived as stem chondrichthyans or even as "elasmobranchiomorphs." Recent dipnoans and tetrapods are sister groups, but new paleontological discoveries refute many of their supposed osteological synapomorphies, thereby reopening the possibility of a closer relationship between tetrapods and osteolepiform rhipidistians.     

A three‐dimensional placoderm (stem‐group gnathostome) pharyngeal skeleton and its implications for primitive gnathostome pharyngeal architecture

The pharyngeal skeleton is a key vertebrate anatomical system in debates on the origin of jaws and gnathostome (jawed vertebrate) feeding. Furthermore, it offers considerable potential as a source of phylogenetic data. Well‐preserved examples of pharyngeal skeletons from stem‐group gnathostomes remain poorly known. Here, we describe an articulated, nearly complete pharyngeal skeleton in an Early Devonian placoderm fish, Paraplesiobatis heinrichsi Broili, from Hunsrück Slate of Germany. Using synchrotron light tomography, we resolve and reconstruct the three‐dimensional gill arch architecture of Paraplesiobatis and compare it with other gnathostomes. The preserved pharyngeal skeleton comprises elements of the hyoid arch (probable ceratohyal) and a series of branchial arches. Limited resolution in the tomography scan causes some uncertainty in interpreting the exact number of arches preserved. However, at least four branchial arches are present. The final and penultimate arches are connected as in osteichthyans. A single median basihyal is present as in chondrichthyans. No dorsal (epibranchial or pharyngobranchial) elements are observed. The structure of the pharyngeal skeleton of Paraplesiobatis agrees well with Pseudopetalichthys from the same deposit, allowing an alternative interpretation of the latter taxon. The phylogenetic significance of Paraplesiobatis is considered. A median basihyal is likely an ancestral gnathostome character, probably with some connection to both the hyoid and the first branchial arch pair. Unpaired basibranchial bones may be independently derived in chondrichthyans and osteichthyans.     

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     

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.     

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.     

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.