Endocast and Bony Labyrinth of a Devonian "Placoderm" Challenges Stem Gnathostome Phylogeny.

Our understanding of the earliest evolution of jawed vertebrates depends on a credible phylogenetic framework for the jawed stem gnathostomes collectively known as "placoderms".1 However, their relationships, and whether placoderms represent a single radiation or a paraphyletic array, remain contentious.2-13 This uncertainty is compounded by an uneven understanding of anatomy across the group, particularly of the phylogenetically informative braincase and brain cavity-endocast. Based on new tomographic data, we here describe the endocast and bony labyrinth of Brindabellaspis stensioi from the Early Devonian of New South Wales.14 The taxon was commonly recovered as branching near the base of placoderms.5-9,11,12,15-17 Previous studies of Brindabellaspis emphasized its resemblances with fossil jawless fishes in the braincase anatomy14 and endocast proportions1,18 and its distinctive features were interpreted as autapomorphies, such as the elongated premedian region.19 Although our three-dimensional data confirmed the resemblance of its endocast to those of jawless vertebrates, we discovered that the inner ear and endolymphatic complex display a repertoire of previously unrecognized characters close to modern or crown-group jawed vertebrates, including a pronounced sinus superior and a vertical duct that connects the endolymphatic sac and the labyrinth cavity. Both parsimony and Bayesian analyses suggest that prevailing hypotheses of placoderm relationships are unstable, with newly revealed anatomy pointing to a radical revision of early gnathostome evolution. Our results call into question the appropriateness of arthrodire-like placoderms as models of primitive gnathostome anatomy and raise questions of homology relating to key cranial features.

New information on Brindabellaspis stensioi Young, 1980, highlights morphological disparity in Early Devonian placoderms.

Acid-prepared specimens of the placoderm Brindabellaspis stensioi (Early Devonian of New South Wales, Australia) revealed placoderm endocranial anatomy in unprecedented detail. Brindabellaspis has become a key taxon in discussions of early gnathostome phylogeny, and the question of placoderm monophyly versus paraphyly. The anterior orientation of the facial nerve and related hyoid arch structures in this taxon resemble fossil osteostracans (jawless vertebrates) rather than other early gnathostomes. New specimens of Brindabellaspis now reveal the previously unknown anterior region of the skull, including an exceptionally elongate premedian bone forming a long rostrum, supported by a thin extension of the postethmo-occipital unit of the braincase. Lateral overlap surfaces indicate an unusual anterior position for the jaws. Digital rendering of a synchrotron radiation scan reveals a uniquely specialized ethmoid commissure sensory canal, doubled back and fused into a midline canal. The visceral surface of the premedian bone has a plexus of perichondral bone canals. An updated skull roof reconstruction of Brindabellaspis adds to the highly variable dermal skull patterns of the probably non-monophyletic 'acanthothoracids'. The unusual morphology revealed by the new specimens suggests that the earliest known reef fish fauna contained a diverse range of fishes with specialized ecological roles.

Neurocranial anatomy of an enigmatic Early Devonian fish sheds light on early osteichthyan evolution.

The skull of 'Ligulalepis' from the Early Devonian of Australia (AM-F101607) has significantly expanded our knowledge of early osteichthyan anatomy, but its phylogenetic position has remained uncertain. We herein describe a second skull of 'Ligulalepis' and present micro-CT data on both specimens to reveal novel anatomical features, including cranial endocasts. Several features previously considered to link 'Ligulalepis' with actinopterygians are now considered generalized osteichthyan characters or of uncertain polarity. The presence of a lateral cranial canal is shown to be variable in its development between specimens. Other notable new features include the presence of a pineal foramen, the some detail of skull roof sutures, the shape of the nasal capsules, a placoderm-like hypophysial vein, and a chondrichthyan-like labyrinth system. New phylogenetic analyses place 'Ligulalepis' as a stem osteichthyan, specifically as the sister taxon to 'psarolepids' plus crown osteichthyans. The precise position of 'psarolepids' differs between parsimony and Bayesian analyses.

New findings in a 400 million-year-old Devonian placoderm shed light on jaw structure and function in basal gnathostomes.

Arthodire placoderms have been proposed as the sister group of Chinese 'maxillate' placoderms plus all the more crownward gnathostomes. These basal groups provide key information for understanding the early evolution of jaws. Here, we test previous assumptions about placoderm jaw structure and function by using high-resolution computed tomography, digital dissection, and enlarged 3D printouts on a unique articulated 400 million-year-old buchanosteid arthrodire. The upper jaw has a double ethmoid and a palatobasal connection, but no otic connection; the dermal bone attachment for the quadrate is different to other placoderms. A separately ossified cartilage behind the mandibular joint is comparable to the interhyal of osteichthyans. Two articular facets on the braincase associated with the hyomandibular nerve foramen supported a possible epihyal element and a separate opercular cartilage. Reassembling and manipulating 3D printouts demonstrates the limits of jaw kenetics. The new evidence indicates unrecognized similarities in jaw structure between arthrodires and osteichthyans, and will help to clarify the sequence of character acquisition in the evolution of basal gnathostome groups. New details on the hyoid arch will help to reformulate characters that are key in the heated debate of placoderm monophyly or paraphyly.

First shark from the Late Devonian (Frasnian) Gogo Formation, Western Australia sheds new light on the development of tessellated calcified cartilage.

BACKGROUND: Living 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. METHODOLOGY/PRINCIPAL FINDINGS: Here we present new data from the first well-preserved chondrichthyan fossil from the early Late Devonian (ca. 380-384 Mya) Gogo Formation Lägerstatte of Western Australia. The specimen is the first Devonian shark body fossil to be acid-prepared, revealing the endoskeletal elements as three-dimensional undistorted units: Meckel's cartilages, nasal, ceratohyal, basibranchial and possible epibranchial cartilages, plus left and right scapulocoracoids, as well as teeth and scales. This unique specimen is assigned to Gogoselachus lynnbeazleyae n. gen. n. sp. CONCLUSIONS/SIGNIFICANCE: The 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.

Copulation in antiarch placoderms and the origin of gnathostome internal fertilization.

Reproduction in jawed vertebrates (gnathostomes) involves either external or internal fertilization. It is commonly argued that internal fertilization can evolve from external, but not the reverse. Male copulatory claspers are present in certain placoderms, fossil jawed vertebrates retrieved as a paraphyletic segment of the gnathostome stem group in recent studies. This suggests that internal fertilization could be primitive for gnathostomes, but such a conclusion depends on demonstrating that copulation was not just a specialized feature of certain placoderm subgroups. The reproductive biology of antiarchs, consistently identified as the least crownward placoderms and thus of great interest in this context, has until now remained unknown. Here we show that certain antiarchs possessed dermal claspers in the males, while females bore paired dermal plates inferred to have facilitated copulation. These structures are not associated with pelvic fins. The clasper morphology resembles that of ptyctodonts, a more crownward placoderm group, suggesting that all placoderm claspers are homologous and that internal fertilization characterized all placoderms. This implies that external fertilization and spawning, which characterize most extant aquatic gnathostomes, must be derived from internal fertilization, even though this transformation has been thought implausible. Alternatively, the substantial morphological evidence for placoderm paraphyly must be rejected.

A gigantic sarcopterygian (tetrapodomorph lobe-finned fish) from the upper Devonian of Gondwana (Eden, New South Wales, Australia).

Edenopteron keithcrooki gen. et sp. nov. is described from the Famennian Worange Point Formation; the holotype is amongst the largest tristichopterids and sarcopterygians documented by semi-articulated remains from the Devonian Period. The new taxon has dentary fangs and premaxillary tusks, features assumed to be derived for large Northern Hemisphere tristichopterids (Eusthenodon, Hyneria, Langlieria). It resembles Eusthenodon in ornament, but is distinguished by longer proportions of the parietal compared to the post-parietal shield, and numerous differences in shape and proportions of other bones. Several characters (accessory vomers in the palate, submandibulars overlapping ventral jaw margin, scales ornamented with widely-spaced deep grooves) are recorded only in tristichopterids from East Gondwana (Australia-Antarctica). On this evidence Edenopteron gen. nov. is placed in an endemic Gondwanan subfamily Mandageriinae within the Tristichopteridae; it differs from the nominal genotype Mandageria in its larger size, less pointed skull, shape of the orbits and other skull characters. The hypothesis that tristichopterids evolved in Laurussia and later dispersed into Gondwana, and a derived subgroup of large Late Devonian genera dispersed from Gondwana, is inconsistent with the evidence of the new taxon. Using oldest fossil and most primitive clade criteria the most recent phylogeny resolves South China and Gondwana as areas of origin for all tetrapodomorphs. The immediate outgroup to tristichopterids remains unresolved - either Spodichthys from Greenland as recently proposed, or Marsdenichthys from Gondwana, earlier suggested to be the sister group to all tristichopterids. Both taxa combine two characters that do not co-occur in other tetrapodomorphs (extratemporal bone in the skull; non-cosmoid round scales with an internal boss). Recently both 'primitive' and 'derived' tristichopterids have been discovered in the late Middle Devonian of both hemispheres, implying extensive ghost lineages within the group. Resolving their phylogeny and biogeography will depend on a comprehensive new phylogenetic analysis.

Live birth in the Devonian period.

The extinct placoderm fishes were the dominant group of vertebrates throughout the Middle Palaeozoic era, yet controversy about their relationships within the gnathostomes (jawed vertebrates) is partly due to different interpretations of their reproductive biology. Here we document the oldest record of a live-bearing vertebrate in a new ptyctodontid placoderm, Materpiscis attenboroughi gen. et sp. nov., from the Late Devonian Gogo Formation of Australia (approximately 380 million years ago). The new specimen, remarkably preserved in three dimensions, contains a single, intra-uterine embryo connected by a permineralized umbilical cord. An amorphous crystalline mass near the umbilical cord possibly represents the recrystallized yolk sac. Another ptyctodont from the Gogo Formation, Austroptyctodus gardineri, also shows three small embryos inside it in the same position. Ptyctodontids have already provided the oldest definite evidence for vertebrate copulation, and the new specimens confirm that some placoderms had a remarkably advanced reproductive biology, comparable to that of some modern sharks and rays. The new discovery points to internal fertilization and viviparity in vertebrates as originating earliest within placoderms.

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.

An exceptional Devonian fish from Australia sheds light on tetrapod origins.

The transition from fishes to tetrapods was one of the most dramatic events in the evolution of vertebrates, but many pivotal fossils are incomplete, resulting in gaps in the data that are used for phylogenetic reconstruction. Here we present new observations from the most complete, acid-prepared Devonian tetrapodomorph fish yet discovered, Gogonasus, which was previously placed just crownward of Kenichthys and rhizodontids, the most primitive taxa on the tetrapod lineage. Unexpectedly, Gogonasus shows a mosaic of plesiomorphic and derived tetrapod-like features. Whereas the braincase and dermal cranial skeleton exhibit generalized morphologies with respect to Eusthenopteron or Panderichthys, taxa that are traditionally considered to be phyletically close to tetrapods, the presence of a deeply invaginated, wide spiracle, advanced internal spiracular architecture and near-horizontal hyomandibula are specialized features that are absent from Eusthenopteron. Furthermore, the pectoral fin skeleton of Gogonasus shares several features with that of Tiktaalik, the most tetrapod-like fish. A new phylogenetic analysis places Gogonasus crownward of Eusthenopteron as the sister taxon to the Elpistostegalia. Aspects of the basic tetrapod limb skeleton and middle ear architecture can now be traced further back within the tetrapodomorph radiation.

X-ray microtomography of 410 million-year-old optic capsules from placoderm fishes.

The structure of two small ossified optic capsules from mid-Palaeozoic placoderm fishes has been revealed in fine detail, by the use of X-ray microtomography analysis and 3D visualisation software. These two specimens are 410 million-year-old; they were collected from an Early Devonian (Lochkovian) limestone in central New South Wales, and are the oldest known optic capsules from jawed fishes. The capsules show attachment areas for seven extrinsic eye muscles, rather than the six until recently deemed universal for gnathostomes. The analysis also revealed structures within the ossified cartilage which covered the medial surface of the eyeball, including nerve tracts, vascular canals, and possibly a choroid rete mirabile.