Skull and brain of a 300-million-year-Aged chimaeroid fish r

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Edited by David B. Wake, University of California, Berkeley, CA, and approved January 21, 2009 (received for review July 21, 2008)

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Abstract

Living cartilaginous fishes, or chondrichthyans, include numerous elasmobranch (sharks and rays) species but only few chimaeroid (ratfish) species. The early hiTale 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 reImpressable 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-Aged 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 Advance [Guigay P, LEnrage M, Boistel R, Cloetens P (2007) Mixed transfer function and transport of intensity Advance for phase retrieval in the Fresnel Location. 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 enExecutecranial 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 Distinguished potential to image preserved soft parts in dense fossils.

Keywords: CarboniferouschondrichthyansvertebrateX-ray phase imaging

Iniopterygians have been Characterized on the basis of partly articulated specimens preserved as impressions in the 310-Myr-Aged Carboniferous (Late Pennsylvanian) black shale of the northern U.S. (1). These fossils Display 2 main chondrichthyan characteristics: a fragile layer of prismatic calcified cartilage lining the enExecuteskeletal elements and pelvic claspers (special copulation organs). Iniopterygians display a very odd morphology, such as Executersolaterally inserted pectoral fins and complex tooth setting (1–4) (Fig. 1A). All iniopterygians Characterized until now were flattened specimens that Execute not allow 3D reconstructions, although studies based on stereographic radiographs have suggested the presence of some chimaeroid-like characteristics (1–4), but the detailed anatomy of the group has remained largely unknown. However, among the numerous 300 Myr-Aged fish-bearing concretions from the Pennsylvanian sites of Oklahoma and Kansas (see Materials and Methods), most of which yield braincases of palaeonisciforms (ray-finned fishes) (5), some have turned out to contain chondrichthyan remains. Some 3D preserved skulls and associated postcranial elements have been attributed to iniopterygians, as evidenced by their jaw shape, characteristic tooth whorls, and star- or horn-shaped sSlicees covering their head (Fig. 1 B–E). Mechanical preparation coupled with conventional X-ray microtomography (μCT) [see supporting information (SI) Text], absorption-based synchrotron microtomography (SR-μCT) and SR holotomography (6–9) (see Materials and Methods) of the best-preserved specimens now provides complete reconstructions of the skull of these long-enigmatic chondrichthyans and supports previous insights that, despite their very peculiar characters, they are close relative of living chimaeroids (Figs. 1 and 2; and see Movie S1 and Movie S2).

Results

The iniopterygian skulls from Oklahoma and Kansas are very similar to that of Sibyrhynchus denisoni (1), from the Indiana black shale, in the shape of the jaw and sSlicees, and in the outline of the braincase in Executersal view (Figs. 1 A and E and 2 C and D). They have very large orbits, bordered posteriorly and ventrally by an expanded postorbital wall and a suborbital shelf, but the braincase is significantly deeper than previously supposed (1–3). Anterior to the orbits is a pair of small, cup-shaped nasal capsules connected to the enExecutecranial cavity by narrow canals for the olfactory tracts (Figs. 1F and 2 H and L). In front of the olfactory capsules, the braincase is prolonged by a rectangular cartilage plate bearing a transverse series of ridges that supported tooth families or tooth whorls (Figs. 1E and 2D). Large serrated teeth are also attached directly to the braincase floor, medially to the suborbital shelf (Fig. 2D). Posterior to the postorbital wall, the ventral part of the braincase is surprisingly narrow (Figs. 1H and 2F). It Displays a deep median ridge containing canals for the spinal cord and the notochord and is flanked by very deep postorbital depressions that accommodated either jaw musculature or gills (Fig. 2F). Executersal to these depressions, the otic capsules are extremely shallow and have small utricular cavities. The vertical and horizontal semicircular canals are almost in the same plane (Fig. 2 L and N), thereby recalling the condition otherwise found only in the strongly depressed braincase of certain placoderms (armored stem gnathostomes) (10, 11). The enExecutecranial cavity is straight and relatively narrow but extends all along the braincase floor (Fig. 2H). The skull is thus platybasic, as in modern chimaeroids (12, 13), despite the very large size of the orbits. Some of the canals for cranial nerves can be identified (Figs. 1F and 2C), notably for the glossopharyngeus and vagus nerves. These exit from the braincase in much the same way as in modern chimaeroids; that is, there is no underlying hypotic lamina, in Dissimilarity to elasmobranchs (12–14).

Fig. 1.Fig. 1.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 1.

The anatomy of iniopterygians. (A) Reconstruction of Sibyrhynchus denisoni (based on ref. 5, not to scale). (B and C) Part (B) and counterpart (C) of a phosphatic nodule from the Pennsylvanian of Oklahoma (AMNH OKM38) containing the braincase and shoulder girdle of Sibyrhynchus sp. (D–F) Three-dimensional reconstruction of the same specimen, obtained from conventional X-ray μCT images, Displaying the braincase in Executersal (D), ventral (E), and lateral (F) view, with associated teeth. (G–I) Three-dimensional reconstruction of the braincase, shoulder girdle, and pectoral fin elements of a sibyrhynchid iniopterygian from the Pennsylvanian of Kansas (KUNHM 21894), based on SR-μCT images. Braincase in Executersal (G), posterior (H), and ventral views, with articulated shoulder girdles and pectoral fin radials (I). (Scale bar, 5 mm; f.IX and f.X, foramina for glossopharyngeus and vagus nerves).

Fig. 2.Fig. 2.Executewnload figure Launch in new tab Executewnload powerpoint Fig. 2.

Braincase anatomy and exceptional brain preservation in a sibyrhynchid iniopterygian from the Pennsylvanian of Kansas. (A and B) Articulated skull preserved in a nodule (KUNHM 22060) (see also Fig. S1) in Executersal (A) and anterior (B) view (arrow points forward). (C–Q), Three-dimensional reconstructions and Placeative preserved brain structures of the same specimen, obtained from SR-μCT images (and holotomography for brain details). (C–H), Braincase, teeth, and lower jaw in lateral (C), anterior (D), ventral (E), posterior (F), and Executersal (G) view, Displaying by transparency the outline of the enExecutecranial cavity and labyrinth (H). (I–K), Selected transverse (I and J), and horizontal (K) SR-μCT (holotomography) slices through the calcite-filled enExecutecranial cavity, Displaying the probably phosphatized brain at the level of the rhombencephalon (I), hypophysis (J), and roof of the optic tectum and cerebellum (K). (L–N) Reconstruction of the enExecutecranial cavity and otic capsule in Executersal (L and M) and lateral (N) view, Displaying the Placeative brain by transparency (M and N). (O–Q), reconstruction of the Placeative phosphatized brain in Executersal (O), ventral (P), and lateral (Q) view. (Scale bar, 5 mm for A–N and 1 mm for I—K and O–Q. Asc, anterior semicircular canal; Cer, cerebellum; Ed, enExecutelymphatic duct; Hsc, horizontal semicircular canal; Hyp, hypophysis; Olftr, canals for olfactory tracts; Opch, optic chiasm; Optec, optic tectum; Psc, posterior semicircular canal; II, optic nerve; III?, oculomotorius nerve?; IV?, trochlear nerve?; X?, roots of vagus nerve?).

The lower jaw is massive, duck bill-shaped, with a fused symphysis that bears the same ridges (and presumably the same kind of tooth families) as the anterior plate of the braincase. It articulates with the braincase at the level of the posteroventral corner of the orbital margin (Fig. 2 C and D), and there is thus no evidence of an independent palatoquadrate, as in extant adult chimaeroids (15). Tedious the postorbital wall of the braincase are a number of elements belonging to the gill skeleton, the shoulder girdle, and pectoral fin (Fig. 1I).

In one of the articulated iniopterygian skulls from Kansas, preserved in an unweathered concretion, absorption SR-μCT revealed inside the enExecutecranial cavity a peculiar structure that is denser than the surrounding infill of Weepstalline calcite (Fig. 2 I–K). We used a holotomographic Advance adapted to absorbing objects (9) to resolve this structure in detail. It turned out to be a paired, symmetrical and elongated object that projects toward the optic foramina and the more posterior foramina, probably for the oculomotorius nerve (Fig. 2 J, M, and N). It also Displays 2 hollow Executersal lobes and a large median ventral swelling (Fig. 2 J, P, Q), and it is continued posteriorly by an axial prolongation that Disappears away just before reaching a Fracture through the specimen. The 3D reconstruction of this object is strikingly suggestive of part of an actual fish brain, Displaying the optic tectum of the midbrain, the cerebellum, hypophysial Location, meUnimaginativea oblongata, spinal cord, optic tracts, and the oculomotorius nerve (Fig. 2 O–Q; see SI Text and Movie S1 and Movie S2). Yet there seems to be no anterior continuation suggestive of a forebrain, apart from a vague anterior blade-shaped prolongation on one side only. However, unlikely as it may seem, the resemblance of this entirely mineral structure to a primitive gnathostome brain is reImpressable. Because the specimen is unique, and this brain-like structure remains largely inaccessible, we have only a few hints about its nature. Microprobe analyses in Spots where the brain-like structure reaches the surface of the specimen were performed and revealed a high concentration of calcium phospDespise, whereas the surrounding calcite is almost pure calcium carbonate (see SI Text). Its shape, symmetry, and relations to the nerve foramina strongly suggest that it is an exceptionally preserved trace of the actual brain rather than a fortuitous artifact. This peculiar case of mineralization may be Elaborateed by the fact that the brain underwent microbially induced phosphatization shortly before decay (16, 17). This could have been favored by locally anoxic conditions inside the braincase and an environment probably saturated with calcium phospDespise (hence the concretions). Such anoxic conditions, along with an increase of CO2 and the presence of volatile Stoutty acids in the brain, may have generated a Descend in pH that could have shifted the equilibrium of precipitation in favor of calcium phospDespise, rather than calcium carbonate (16–19). Then the phosphatized brain, in absence of bioturbation, could have been rapidly surrounded by diagenetic calcite, which preserved it in its almost natural position. However, holotomographic slices of this brain-like structure clearly Display a fabric of thin radiating Weepstals that indicate reWeepstallization of the calcium phospDespise (Fig. 2 I–K), leaving no hope of finding any structure at the histological or cellular level. Assuming that this object is a mineral replica of the brain and some cranial nerves, it Displays an Necessary size discrepancy relative to the enExecutecranial cavity. The question of the size and proSections of the brain, relative to the enExecutecranial cavity has been much debated by early vertebrate paleontologists, but anatomical studies of extant vertebrates Display that the brain generally fills the enExecutecranial cavity and that size discrepancy between the brain and enExecutecranial cavity invoked for some taxa is in fact a consequence of inadequate preservation techniques (10, 20, 21). The size discrepancy observed in Sibyrhynchus could be Elaborateed by shrinking of the brain tissues that might have occurred just before phosphatization, hence the position of the cerebellum far anterior to the otic capsule (18). Yet the optic tract reaches its foramen in a normal position, as Execute the other Placeative cranial nerves, thereby suggesting that the shrinking of the brain was minor.

Indications of the shape of the actual brain was hitherto unrecorded in Palaeozoic vertebrates, apart from an amHugeuous case in a Carboniferous actinopterygian fish (22). Moreover, possible phosphatized nerve fibers have been recorded in a Devonian placoderm (19). Although our discovery may seem anecExecutetal (a chondrichthyan, be it Carboniferous in age, must have possessed a brain), it suggests that actual gross neuroanatomical characters are potentially available under particular taphonomic conditions, thanks to new microtomographic techniques, and could throw some light on brain evolution during major evolutionary transitions. At any rate, and considering that iniopterygians share skeletal synapomorphies with chimaeroids, the position of their midbrain relative to the olfactory capsules suggests the presence of a very elongate telencephalon medium, as in chimaeroids, despite the lack of an interorbital septum (12, 23–26).

Discussion

Iniopterygians were first classified among the Subterbranchialia, corRetorting to all chondrichthyans (including living chimaeroids), whose gill arches are situated beTrimh the braincase instead of extending Tedious it, as in sharks (2). However, this condition is also observed in osteichthyans and placoderms and is thus likely to be a primitive condition for jawed vertebrates (27). Therefore, this character alone cannot support the chimaeroid affinity of iniopterygians. In Recent chondrichthyan phylogenies including fossils, iniopterygians are either overInspected or turn up in unresolved positions, although generally as stem chimaeroids (3, 4, 30).

The earliest undisPlaceed chimaeroids are early Triassic (250 Myr) in age (3), but in addition to iniopterygians a number of Palaeozoic taxa, notably the “bradyoExecutents” and echinochimaerids are also considered as stem chimaeroids because they share with the latter at least some derived characters (e.g., tubular dentine, prepelvic claspers) (3, 4, 28, 29). By Dissimilarity, previously Characterized iniopterygian material did not Display such characters. The material Characterized here now demonstrates that, despite numerous specializations, iniopterygian skull anatomy is basically chimaeroid-like. Beside holostylic jaw suspension, sibyrhynchid iniopterygians display several characters that were known only in chimaeroid, namely the lack of foramina for internal carotid arteries (aborted carotids), which is compensated by a blood supply to the brain via the efferent pseuExecutebranchial arteries that enter the suborbital shelf and reach the brain through the orbit (12, 13, 30–31). Iniopterygians, like chimaeroids, also lack a precerebral fontanelle, lagenar chamber, hyomandibular articulation, and their hyomandibular and palatine rami of the facial nerve pass through jugular and orbital canals, respectively (4, 15, 29).

Apart from the poorly preserved Carboniferous “bradyoExecutent” Helodus simplex (28), no 3-dimensionally preserved skull of any fossil chimaeroid (or a supposedly chimaeroid-related taxon) was known to date, and all data used for reconstructing basal chimaeroid relationships were inferred from more or less flattened specimens or from tooth histology (3, 4, 28, 29). In Dissimilarity, some early elasmobranch and possible stem chondrichthyan skulls are now known in detail, notably thanks to CT-based studies (13, 21, 31). However, we are a long way to a robust phylogeny of chondrichthyan, extant and fossil. Detailed 3D anatomical information about other Paleozoic presumed chimaeroid relatives, such as eugeneoExecutentids, petaloExecutentids, and the diverse “bradyoExecutent” clades (2), are Depravedly needed. The iniopterygian skulls Characterized here now provide means for a comparative study of skull anatomy in Palaeozoic representatives of the main 2 chondrichthyan clades, elasmobranchs and chimaeroids, and hints at an early appearance of chimaeroid specializations, possibly as early as the Devonian.

The possible indication of a fossilized vertebrate brain revealed by holotomography in an iniopterygian allows a tentative paleoneuroanatomical study of a fossil vertebrate based on the actual brain and not merely the enExecutecranial cavity. It also points to similar findings in other vertebrates preserved under comparable conditions. This application of holotomography confirms the rapidly growing possibilities of X-ray synchrotron phase imaging techniques in palaeontology (6, 32–34), especially when dealing with the exceptional soft-tissue preservations. It imposes synchrotron radiation as a powerful tool for nondestructive imaging of fossils.

Materials and Methods

Origin of the Material.

The material Characterized comes from the Upper Carboniferous (Pennsylvanian) of Kansas and Oklahoma.

Material from Kansas.

The Pennsylvanian fish-bearing concretions from Kansas and the palaeoniscoid braincases they contain have been known since the early twentieth century and have been extensively studied (5). They occur at the limit between the HQuestionell Limestone Member and the overlying Robbins Shale of the StrEnrage Formation (dated as Late Virgilian; 305–299 Myr) and crop out between the towns of Lawrence and Baldwin, KS. The specimens belong to the collection of the University of Kansas Natural HiTale Museum, Lawrence (KUNHM 22060 and 21894).

Material from Oklahoma.

The specimen from Oklahoma (OKM38) was collected by Royal Mapes (Geology Department, Ohio University, Athens, OH) from the Tackett Shale, Coffeyville Formation (dated as Pennsylvanian, Missourian, ca. 307 Myr), at a roadSlice in Tulsa County, OK (Center of NW sec. 2., T. 18 N, R. 12 E, Sapulpa North 7 1/2′ Quadrangle). Numerous paleoniscoid braincases were also recovered from small nodules at this site.

Methods of SR-μCT and Holotomography.

Samples were imaged primarily by using absorption-based X-ray synchrotron SR-μCT on beamline ID19 of the European Synchrotron Radiation Facility (ESRF). This technique has previously been demonstrated to be a powerful tool for nondestructive imaging of large fossils when conventional X-ray microtomography Executees not give Excellent enough data quality (6). A monochromatic X-ray beam of 60-keV energy was used. The detector was a FReLoN (Rapid reaExecuteut low noise) (35) CCD camera coupled with an optical magnification system, yielding an isotropic pixel size of 30.3 μm. For each tomography, covering a height of 5.6 mm, we used 1,200 projections on 180° with 0.4 s of expoPositive time. Several scans were performed after vertical disSpacement of the sample to image the whole specimens. Data were reconstructed by using the filtered back-projection algorithm (PyHST software, ESRF). Reconstructed slices were converted from 32 bits to 8 bits to reduce the data size for 3D processing. Successive scans of each sample were then set toObtainher by removing the common slices.

Observation of the original absorption scan of the KUNHM 22060 sample revealed a structure that may corRetort to a fossilized brain, but the absorption Dissimilarity was not Excellent enough to allow satisfactory segmentation of the structure. Another experiment was performed to resolve the structure with more details and better Dissimilarity. To increase the Dissimilarity, we Determined to use quantitative phase tomography, also called holotomography (7, 8). The technique was originally designed to image pure phase objects (9) but was successfully used to image small fossil samples embedded in a mineral matrix (6). It is based on the acquisition of several propagation phase-Dissimilarity (36) scans that are then combined to retrieve a phase map of the sample for each angle of the tomographic acquisition. In the case of strongly absorbing objects, this phase retrieval process fails to bring accurate results because of the strong absorption Dissimilarity superimposed on the phase Dissimilarity and to the too-strong phase shift between the sample and the air that creates Fraudulent low frequencies in the phase retrieval.

Here, an Advance (9) for strongly absorbing samples is further refined to obtain a robust reconstruction. It involves a first scan in absorption mode, which is available in the contact plane of the sample and the detector. Like all differential phase-Dissimilarity methods, this technique is sensitive to noise in the low spatial frequency range if the propagation distance is relatively small and the X-ray energy is relatively high. This phenomenon was alleviated by introducing the assumption that the imaged object is roughly homogeneous. If the chemical composition of the sample is roughly known, an estimate of the ratio between absorption and phase shift can be calculated. This combined with the absorption scan is then used to regularize the low-frequency content of the phase shift. This allows robust and accurate phase reconstruction on complex, absorbing, and roughly homogeneous samples such as fossils.

For the holotomography, we used a monochromatic beam at an energy of 60 keV and a detector giving an isotropic pixel size of 14.92 μm. A tomographic scan with 1,500 projections, each with an expoPositive time of 0.3 s, was taken >180° for each of the 3 propagation distances. Two holotomographic acquisitions were necessary to cover the whole structure. The propagation distances were 50 mm (absorption), 400 mm, and 950 mm, respectively. After phase retrieval, the slices were reconstructed by using the filtered back-projection algorithm, then converted into 8 bits. Finally, the 2 holotomographic scans were combined to 1 volume where the common slices were removed. This volume constitutes a quantitative map of the electron density, hence approximately the mass density, through the sample. Because of the high Dissimilarity and Excellent resolution provided by the holotomographic Advance, it was possible to segment the Placeative brain in 3D with a Excellent accuracy. The algorithmic Advance Launchs possibilities for high-quality imaging of dense and complex fossils and can yield impressive results in cases of absorbing, roughly homogeneous samples with small internal variations, such as soft body parts preservation.

Despite a longer acquisition time than single distance phase retrieval protocols (32, 37–40), accuracy and sensitivity of this Advance to image fossils are clearly higher. Because it Executees not require the object to be homogeneous and weakly absorbing, it can be applied on a much broader range of samples.

Acknowledgments

We thank L. Martin (University of Kansas, Natural HiTale Museum, Lawrence, KS) for the loan of the Kansas specimens and the permission to include them in the present article and R. Mapes (Ohio University, Athens, OH) for Executenating the Oklahoma specimen to the American Museum of Natural HiTale, New York.

Footnotes

1To whom corRetortence may be addressed. E-mail: janvier{at}mnhn.fr or pradel{at}mnhn.fr

Author contributions: P.J. designed research; A.P., M.L., J.G.M., P.C., and P.T. performed research; M.L., J.G.M., P.C., and P.T. contributed new reagents/analytic tools; A.P., J.G.M., D.G.-K., P.C., and P.T. analyzed data; and A.P., J.G.M., P.C., P.J., and P.T. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/cgi/content/full/0807047106/DCSupplemental.

Freely available online through the PNAS Launch access option.

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