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.     

Vascularization of the osteostracan and antiarch (Placodermi) pectoral fin: similarities, and implications for placoderm relationships

Phylogenetic analyses frequently resolve the extinct group Placodermi at the base of the clade of jawed fishes (traditionally known as the Gnathostomata), with the jawless fish group Osteostraci as sister taxon to this clade. Both gnathostomes and osteostracans possess pectoral fins supported by a radial(s) articulating on a cartilaginous scapulocoracoid. Blood vessels and nerves pass by or through the scapulocoracoid to supply the musculature of the pectoral fin, and in the Osteostraci also pass through the postbranchial lamina backing the gill chamber before reaching the scapulocoracoid. This course also characterizes the placoderm group Antiarchi. Other placoderms retain the condition typical of other jawed fishes in which the scapulocoracoid, as well as the subclavian veins and arteries, are entirely posterior to the back wall of the gill chamber, lying within the internal region of the trunkshield. These observations suggest that these placoderm groups are more closely related to other jawed fishes than are the Antiarchi, challenging the monophyly of the Placodermi.     

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.     

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.     

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.     

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.     

Fins,limbs, and tails: outgrowths and axial patterning in vertebrate evolution

Current phylogenies show that paired fins and limbs are unique to jawed vertebrates and their immediate ancestry. Such fins evolved first as a single pair extending from an anterior location, and later stabilized as two pairs at pectoral and pelvic levels. Fin number, identity, and position are therefore key issues in vertebrate developmental evolution. Localization of the AP levels at which developmental signals initiate outgrowth from the body wall may be determined by Hox gene expression patterns along the lateral plate mesoderm. This regionalization appears to be regulated independently of that in the paraxial mesoderm and axial skeleton. When combined with current hypotheses of Hox gene phylogenetic and functional diversity, these data suggest a new model of fin/limb developmental evolution. This coordinates body wall regions of outgrowth with primitive boundaries established in the gut, as well as the fundamental nonequivalence of pectoral and pelvic structures. BioEssays 20 :371–381, 1998. © 1998 John Wiley & Sons Inc.     

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     

Genome biology of the cyclostomes and insights into the evolutionary biology of vertebrate genomes

The jawless vertebrates (lamprey and hagfish) are the closest extant outgroups to all jawed vertebrates (gnathostomes) and can therefore provide critical insight into the evolution and basic biology of vertebrate genomes. As such, it is notable that the genomes of lamprey and hagfish possess a capacity for rearrangement that is beyond anything known from the gnathostomes. Like the jawed vertebrates, lamprey and hagfish undergo rearrangement of adaptive immune receptors. However, the receptors and the mechanisms for rearrangement that are utilized by jawless vertebrates clearly evolved independently of the gnathostome system. Unlike the jawed vertebrates, lamprey and hagfish also undergo extensive programmed rearrangements of the genome during embryonic development. By considering these fascinating genome biologies in the context of proposed (albeit contentious) phylogenetic relationships among lamprey, hagfish, and gnathostomes, we can begin to understand the evolutionary history of the vertebrate genome. Specifically, the deep shared ancestry and rapid divergence of lampreys, hagfish and gnathostomes is considered evidence that the two versions of programmed rearrangement present in lamprey and hagfish (embryonic and immune receptor) were present in an ancestral lineage that existed more than 400 million years ago and perhaps included the ancestor of the jawed vertebrates. Validating this premise will require better characterization of the genome sequence and mechanisms of rearrangement in lamprey and hagfish.     

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.     

Evolutionary crossroads in developmental biology: cyclostomes (lamprey and hagfish)

Lampreys and hagfish, which together are known as the cyclostomes or 'agnathans', are the only surviving lineages of jawless fish. They diverged early in vertebrate evolution, before the origin of the hinged jaws that are characteristic of gnathostome (jawed) vertebrates and before the evolution of paired appendages. However, they do share numerous characteristics with jawed vertebrates. Studies of cyclostome development can thus help us to understand when, and how, key aspects of the vertebrate body evolved. Here, we summarise the development of cyclostomes, highlighting the key species studied and experimental methods available. We then discuss how studies of cyclostomes have provided important insight into the evolution of fins, jaws, skeleton and neural crest.     

Middle-late devonian placoderms (Pisces: Antiarchi) from Central and northern Asia

Antiarch placoderms (Pisces, Placodermi, Antiarchi) from the Middle-Upper Devonian of Central and northern Asia (Asian part of the former Soviet Union) are described. Available antiarch specimens belong to 28 species (eight of which are described in open nomenclature), of 9 genera, 5 subfamilies, 6 families, 2 orders. The main localities of Middle-Late Devonian antiarchs are listed and provided with the data on stratigraphic distribution. The morphological structure of antiarchs and history of their study in Central and northern Asia are briefly considered. The principles of systematics and phylogeny of antiarchs, feature of their historical development in the Middle and Late Devonian of this area, and their paleozoogeographic relationships are discussed.     

新型有原始肢突胴甲鱼的发现及胴甲鱼早期演化的初步探讨

本文记述的曲靖始突鱼(Procondylolepis qujingensis gen.et sp.nov.)是近几年在云南曲靖早泥盆世地层中发现的有肢突胴甲鱼一原始类型。它和已知胴甲鱼(包括早泥盆世无肢突的和中、晚泥盆世有“盔”状肢突的)不同的最大特点是在其肩带与胸鳍相接的肩关节处有原始的肢突和简单的关节窝;胸鳍甲近端的关节区很小。它展现出胴甲鱼类这一高度特化、长期使人迷惑不解的肢突,在胴甲鱼演化史上发展变化的梗概,填补了肢突从无到有中间的缺环,使人了解到胸鳍的具体结构。文中主要根据肢突的有无和特化程度等,对胴甲鱼早期演化史作了初步探讨,将胴甲鱼分为无肢突超目(Abrachicondylia)和有肢突超目(Brachicondylia)两大部分。始突鱼则代表有肢突超目一早期成员。     

Vertebrate Axial and Appendicular Patterning: The Early Development of Paired Appendages

Determination of paired fin or limb number, identity and positionare key issues in vertebrate development and evolution. Phylogeniesincluding fossil data show that paired appendages are uniqueto jawed vertebrates and their immediate ancestry; that suchfins evolved first as a single pair in an anterior location;that appendicular endoskeletons are primitively AP asymmetric;and that pectoral and pelvic fins primitively differ. It isconjectured that Hox gene expression patterns along the lateralplate mesoderm establish boundaries that contribute to localisationof AP levels at which signals initiate outgrowth from the bodywall. Such regionalisation may be regulated independently ofthat in the paraxial mesoderm and axial skeleton. When combinedwith current hypotheses of Hox gene phylogenetic and functionaldiversity, these data suggest a new model of fin/limb developmentalevolution. This coordinates body wall outgrowth regions withprimitive boundaries established in the gut, and the fundamentalnon-equivalence of pectoral and pelvic structures.     

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.     

The origin of the myelination program in vertebrates

The myelin sheath was a transformative vertebrate acquisition, enabling great increases in impulse propagation velocity along axons. Not all vertebrates possess myelinated axons, however, and when myelin first appeared in the vertebrate lineage is an important open question. It has been suggested that the dual, apparently unrelated acquisitions of myelin and the hinged jaw were actually coupled in evolution [1,2]. If so, it would be expected that myelin was first acquired during the Devonian period by the oldest jawed fish, the placoderms [3]. Although myelin itself is not retained in the fossil record, within the skulls of fossilized Paleozoic vertebrate fish are exquisitely preserved imprints of cranial nerves and the foramina they traversed. Examination of these structures now suggests how the nerves functioned in vivo. In placoderms, the first hinge-jawed fish, oculomotor nerve diameters remained constant, but nerve lengths were ten times longer than in the jawless osteostraci. We infer that to accommodate this ten-fold increase in length, while maintaining a constant diameter, the oculomotor system in placoderms must have been myelinated to function as a rapidly conducting motor pathway. Placoderms were the first fish with hinged jaws and some can grow to formidable lengths, requiring a rapid conduction system, so it is highly likely that they were the first organisms with myelinated axons in the craniate lineage.