rsosroyalsocietypublishingorg

ResearchCite this article Johanson Z Smith MSanchez S Senden T Trinajstic K Pfaff C 2017Questioning hagfish affinities of the enigmaticDevonian vertebrate Palaeospondylus R Socopen sci 4 170214httpdxdoiorg101098rsos170214

Received 8 March 2017Accepted 20 June 2017

Subject CategoryEarth science

Subject Areasevolutionpalaeontology

KeywordsPalaeospondylus X-ray tomography hagfishChondrichthyes jawed vertebrateschondrocranium

Author for correspondenceZerina Johansone-mail zjohansonnhmacuk

Electronic supplementary material is availableonline at httpsdxdoiorg106084m9figsharec3817855

Questioning hagfishaffinities of the enigmaticDevonian vertebratePalaeospondylusZerina Johanson1 Moya Smith12 Sophie Sanchez34

Tim Senden5 Kate Trinajstic6 and Cathrin Pfaff71Department of Earth Sciences Natural History Museum London UK2Tissue Engineering and Biophotonics Dental Institute Kingrsquos College LondonLondon UK3Department of Organismal Biology Uppsala University Uppsala Sweden4European Synchrotron Radiation Facility Grenoble France5Department of Applied Mathematics Research School of Physics and EngineeringAustralian National University Canberra Australian Capital Territory 2601 Australia6Environment and Agriculture Curtin University Kent Street Bentley Perth Australia7Department of Palaeontology University of Vienna Vienna Austria

ZJ 0000-0002-8444-6776 CP 0000-0001-5539-2097

Palaeospondylus gunni Traquair 1890 is an enigmatic Devonianvertebrate whose taxonomic affinities have been debatedsince it was first described Most recently Palaeospondylushas been identified as a stem-group hagfish (Myxinoidea)However one character questioning this assignment is thepresence of three semicircular canals in the otic region of thecartilaginous skull a feature of jawed vertebrates Additionallynew tomographic data reveal that the following characters ofcrown-group gnathostomes (chondrichthyans + osteichthyans)are present in Palaeospondylus a longer telencephalic regionof the braincase separation of otic and occipital regionsby the otico-occipital fissure and vertebral centra As wella precerebral fontanelle and postorbital articulation of thepalatoquadrate are characteristic of certain chondrichthyansSimilarities in the structure of the postorbital process to taxasuch as Pucapampella and possible presence of the ventralcranial fissure both support a resolution of Pa gunni as astem chondrichthyan The internally mineralized cartilaginousskeleton in Palaeospondylus may represent a stage in the loss ofbone characteristic of the Chondrichthyes

1 IntroductionPalaeospondylus gunni Traquair 1890 is commonly found in theMiddle Devonian Achanarras fish beds Achanarras Quarry

2017 The Authors Published by the Royal Society under the terms of the Creative CommonsAttribution License httpcreativecommonsorglicensesby40 which permits unrestricteduse provided the original author and source are credited

on June 27 2018httprsosroyalsocietypublishingorgDownloaded from

2

rsosroyalsocietypublishingorgRSocopensci4170214

(Scotland) part of a deeper-water lake fauna including jawless fishes ([1ndash3] but see [4] for possiblemarine influence) and gnathostomes including placoderms acanthodians and osteichthyans The fishesoccur throughout several beds with Palaeospondylus co-occurring with the lungfish Dipterus theacanthodian Mesacanthus and the placoderm Pterichthyodes [5] Previously Palaeospondylus has beenassigned to almost every major jawless and jawed vertebrate group and identified as both larval andadult [6ndash11] Most recently Hirasawa et al [12] described similarities between Palaeospondylus and larvaeof the extant hagfish Eptatretus burgeri suggesting a hagfish affinity and more particularly as a stemhagfish However new X-ray tomographic scans of Palaeospondylus provide important new details ofcranial anatomy particularly with respect to the otic capsule and vestibular system allowing us toidentify Palaeospondylus as a jawed vertebrate rather than a jawless hagfish More specifically crown-group gnathostome characteristics (elongate telencephalon of the braincase vertebral centra) are presentin Palaeospondylus additionally the large L-shaped element on the lateral braincase is identified as apostorbital process with the palatoquadrate articulating posteroventrally on this process Along with aprecerebral fontanelle these suggest a chondrichthyan affinity for Palaeospondylus with similarity to thestem chondrichthyans such as Pucapampella [13ndash15]

2 Material and methods21 SpecimensSpecimens of Pa gunni examined are from the Middle Old Red Sandstone Achanarras Quarry Scotlandincluding NHMUK PV P22392 P59351 P66582 P59333 P59645 P66582 (Department of Earth SciencesNatural History Museum London)

22 X-ray tomographyThe Palaeospondylus chondrocranium was scanned from 10 micro slices by the ultrafine computedtomography (CT) scanner in the Department of Applied Mathematics Australian National UniversityAustralia and at beamline ID19 European Synchrotron Radiation Facility France (see the electronicsupplementary material for technical details) The high-resolution scans presented here all have a voxelsize of 5 microm A movie of the TIFF stack from lateral to medial is available at the Natural History Museum(NHM) Data Portal (see Data accessibility below) Scans were three-dimensional volume rendered usingDRISHTI v 24 software (sfanueduauVizlabdrishti)

23 Three-dimensional volumetric renderingWe analysed the synchrotron data with the software CT-ANALYSER (v 11441) and CTVOX (v 270)by BrukerSkyscan Working with different grey-values and transparency CT-ANALYSER allowed usto distinguish the Pa gunni specimen (P66582) from the surrounding sediment Details of the CTVOX

settings are found in the electronic supplementary material Three-dimensional segmentation of internalstructures was not possible

24 MacrophotographySpecimens were photographed with a Canon EOS 1100D and a Leica MZ microscope (Leica ApplicationSuite 281) with images processed in ADOBE PHOTOSHOP (CC 201422) to improve contrast

3 ResultsIndividuals of Pa gunni have a distinctive morphology with a large chondrocranium mandibulararch skeleton and extensive vertebral column with a well-developed caudal fin (figure 1eg [6])More posterior branchial arches and paired appendages appear to be absent even as imprints as dounpaired dorsal and anal fins The vertebral column comprises stout elements through most of itslength but anteriorly displays an unusual series of vertebrae associated with two blade-like posteriorlydirected structures (figure 1 electronic supplementary material figure S1) Palaeospondylus is normallypreserved in dorsal (figure 1abdf ) or ventral view (figure 1eg) new X-ray tomographic data allowfor a modified three-dimensional visualization in lateral view (figure 1h [16]) allowing for a revised

on June 27 2018httprsosroyalsocietypublishingorgDownloaded from

3

rsosroyalsocietypublishingorgRSocopensci4170214

interpretation of the prominent L-shaped structure on the lateral face of the chondrocranium and theelement articulating to the posteroventral margin of this structure A more complete examination ofPalaeospondylus morphology is provided in the electronic supplementary material phylogeneticallyrelevant characters particularly with respect to the recent identification of Palaeospondylus as a hagfishare described below

31 Phylogenetically important characters of PalaeospondylusThe most recognizable parts of the Pa gunni chondrocranium are the otic capsules at the posterior marginof the braincase (figure 1abdf ot figure 2ab) which occupy almost one-third of the cranium Internallythe otic region preserves three relatively wide semicircular canals (figure 2 ASC anterior semicircularcanal PSC posterior semicircular canal HSC horizontal semicircular canal) and the three associatedampullae (aa anterior ampulla pa posterior ampulla ha horizontal ampulla figure 2b) which arefilled partially with sediment Additionally an endolymphatic duct between the ASC and PSC may berecognized opening onto the dorsal surface of the braincase (figure 2bd ed electronic supplementarymaterial figure S1c ed) A large sac-like region the saccular or sacculo-lagenar sac is present belowand medial to the ASC and PSC shifted from its usual ventral position during post-mortem compression(figure 2b lagsac) Otoliths within this sac are absent

Immediately posterior to the otic capsules and separate from these [16] are small comma-shapedstructures Given their position relative to the otic capsules and their similarity to comparablestructures in some bony fishes ([17] pls 24 66) they are identified as the occipitals (figure 1ceh occ)Separation of the occipitals implies the presence of a fissure between the otic and occipital regionsAdditionally a ventral cranial fissure may be present separating the otic capsules from the more anteriorethmosphenoid region of the braincase (figure 1abf electronic supplementary material figure S1a vcf)At the posterior margin of the chondrocranium paired foraminae are visible (electronic supplementarymaterial figure S1bd lda) an assumed entrance of the lateral dorsal aorta

Anterior to the otic capsules on the lateral chondrocranium is a large L-shaped structure enclosinga foramen near its base (figure 1h electronic supplementary material figure S1bd asterisk) Dorsallythis structure is flat and is associated with a foramen for cranial nerve II (optic nerve) in the sidewallof the chondrocranium (figure 1d electronic supplementary material figure S1a orb II [1819]) Thisassociation and location anterior to the otic capsule suggests that this is the floor of the orbit Nerve IImarks the anterior border of the diencephalon with the telencephalon suggesting that this is relativelylong in Palaeospondylus The L-shaped structure beneath and behind the orbit is interpreted as thepostorbital process Two elements articulate with the postorbital process forming a V-shaped structureventrally (figure 1ceg) these are interpreted as the palatoquadrate and Meckelrsquos cartilage forming themandibular arch Generally the hyomandibular (hyoid arch) articulates posterior to the ventral cranialfissure on a process associated with the otic region [20] suggesting that these structures anterior to thefissure are reasonably identified as the mandibular arch

The chondrocranium anterior to the orbit is difficult to interpret although this region must includethe nasal capsules (see the electronic supplementary material) Medially a pair of elongate elementsforms the roof of the chondrocranium but do not extend to the anterior margin of the chondrocraniumThis leaves a substantial open area anteriorly [18] reminiscent of the precerebral fontanelle (figure 1abfbrr electronic supplementary material figure S1a asterisk [21]) Additional morphological features aredescribed in the electronic supplementary material

32 Palaeospondylus as a stem-group hagfishPreviously Palaeospondylus was identified as either a member of the Cyclostomata or related to this groupin some way [22ndash26] and most recently as a stem-group hagfish based on similarities of Palaeospondylusto specific embryonic developmental stages of the hagfish E burgeri [12] However our new data showthat several structures have been misidentified in Palaeospondylus including a cage-shaped nasal capsuletwo pairs of dorsal longitudinal cartilage bars linked by commissures and a velar bar and large lingualplates ventrally In E burgeri embryos the pairs of longitudinal cartilages run anteroposteriorly along thechondrocranium linked by transverse commissures and are continuous with the otic capsule posteriorlyIn Palaeospondylus the more medial of these putative longitudinal cartilages (forming the braincase roofas described above figure 1abf brr) were reconstructed as continuous with the anterior margin ofthe otic capsule [12 fig 3ab] but in fact these elements are distinct from the otic region markingthe position of the possible ventral cranial fissure (figure 1abf vcf) Transverse commissures 1 and 2

on June 27 2018httprsosroyalsocietypublishingorgDownloaded from

4

rsosroyalsocietypublishingorgRSocopensci4170214

ro

ro

pq

Mk

orb

n1

II

po pro

ot

syn

occ

7

8

2 1

orb

ot

lopv1ndash3

v4na

syn

ro

Mk

po pro

pq

syn

syn occ

v

pq po pro orb

n1

5

2

vcf

br r

occ

81

br r

2

orb

vcf

ot

v1ndash4

2 mm

5 mm

3 mm

(a) (c) (d )(b)

(e)

( f ) (g)

(h)

Figure 1 Palaeospondylus gunni Achanarras Quarry (Devonian) Scotland (ab) NHMUKPVP22393 stereopair Asterisk indicates positionof the precerebral fontanelle (ce) NHMUK PVP59563 macrophotograph of ventral chondrocranium (c) and entire specimen (e) (dfh)NHMUK PVP66582 chondrocranium and anterior vertebrae including lateral elements (syn) forming synarcual anteriorly Detailedmineralized tissue structure is resolved in the entire skeleton round lacunae surrounded by interlacunar mineralization and denseperilacunar tissue (d) Ventral (f ) dorsal and (h) ventrolateral views three-dimensional volume rendered (Drishti) Asterisk in (h)indicates position of jugular canal white arrowhead the posteroventral articulation of the palatoquadrate on the postorbital process(g) ventral viewof entire specimenmacrophotograph 1ndash5 elements of thenasal capsule 6ndash8 elements associatedwith rostral structure(see the electronic supplementary material figure S1 for numbers not shown here) II optic cranial nerve brr braincase roof lop lateralotic process Mk Meckelrsquos cartilage n1 nerve foramen (medial supraopthalmic branches of trigeminal facial cranial nerves) na neuralarch occ occipital orb orbit popro postorbital process ot otic capsule pq palatoquadrate ro rostral sensory structure syn lateralelements forming synarcual with anterior vertebral elements tr trabeculae vcf ventral cranial fissure v vertebral elements

on June 27 2018httprsosroyalsocietypublishingorgDownloaded from

5

rsosroyalsocietypublishingorgRSocopensci4170214

aa

ASC

edlag sac

PSC

HSC

pa

ed

pa

HSC

ha

(a)

(c) (d )

(b)

Figure 2 Palaeospondylus gunni Achanarras Quarry (Devonian) Scotland (ab) NHMUK PVP P66582 ventral view of the otic regionvolumetric rendered (CTvox) for better visualization of internal structures dorsal and ventral parts of the specimen are removed(cd) More ventral tilted lsquovirtualrsquo plane through the specimen ASC anterior semicircular canal PSC posterior semicircular canal HSChorizontal semicircular canal aa anterior ampulla ed endolymphatic duct pa posterior ampulla ha horizontal ampulla lagsacsacculo-lagenar sac

are also incorrectly identified in Palaeospondylus with the first being a distinct and separate elementidentified here as part of the nasal capsule (electronic supplementary material figure S1b 5) This elementis entirely within the chondrocranium (although visible in external view figure 1f ) rather than being anexternal commissure [12 fig 3a comm1] Commissure 2 is also a separate element in Palaeospondylusforming an anterior wall to the orbit (figure 1abf electronic supplementary material figure S1b)In both cases these elements are not continuous or contiguous with other cartilaginous parts of thebraincase

Following Bulman [18] Hirasawa et al [12 fig 3bd] identified a series of ventral elements inPalaeospondylus (eg figure 1ceg) as the velar bar and lingual bar comparable to E burgeri Thevelar bar was reconstructed as a single continuous element [12] but it is composed of two opposingstructures (figure 1g pq Mk) moreover as described above these were identified as the palatoquadratearticulating with Meckelrsquos cartilage with the palatoquadrate articulating to the ventral postorbitalprocess Hirasawa et al [12 fig 3b] reconstructed what is clearly the separate palatoquadrate (eg

on June 27 2018httprsosroyalsocietypublishingorgDownloaded from

6

rsosroyalsocietypublishingorgRSocopensci4170214

figure 1cg electronic supplementary material figure S1b) as incorporated into the anterior margin ofthe otic capsule (also [18])

One of the two elements forming the putative lingual bar [12] was identified above as the occipital(also [16]) while the second element articulates to these occipitals and is associated with the unusualanterior region of the vertebral column comprising narrow rounded centra and more posterior vertebralelements Centra are absent from the hagfish vertebral column ([27] present only in certain crowngnathostome taxa [28]) and we provide a novel interpretation of this region that it represents the regionof the anterior vertebral column the synarcual (electronic supplementary material) The presence ofcentra within the synarcual of Palaeospondylus is reminiscent of the synarcual in batoid chondrichthyans[2930]

Hirasawa et al [12] also focused on the crown-like structure at the anterior chondrocraniumidentifying this as a nasal capsule comparable to embryos of E burgeri This comparison depends onidentification of anterior and posterior transverse bars connecting the separate longitudinal bars of thecrown to form a cage-like structure as in the E burgeri nasal capsule (stage 60 [12] fig 3a) Howeverthe transverse anterior bar does not exist ([6162122] contra [31] figure 1 electronic supplementarymaterial figure S1b) and there is no particular resemblance to the nasal capsule which we identify asbeing paired and positioned more posteriorly to the rostral crown-like structure instead this region isidentified as a rostrum at the anterior chondrocranium and potentially an innervated sensory organ(electronic supplementary material) Cumulatively these misidentifications [12] strongly argue againstPalaeospondylus being a hagfish (also recently rejected by Janvier amp Sansom [32]) moreover charactersdiscussed above in particular the vestibular system with its three semicircular canals within theotic capsule suggest that Palaeospondylus is a jawed vertebrate with several characters shared withcrown-group gnathostomes

4 DiscussionThe characters described above establish Palaeospondylus as a jawed vertebrate contrary to recentsuggestions by Hirasawa et al [12] Apart from the mineralized vertebrae (eg centra) the mostconvincing new character arguing against a myxinoid and agnathan relationship is the third semicircularcanal in the otic region of Palaeospondylus and associated ampullae This is characteristic of jawedvertebrates (eg [33]) but not extant agnathans (one semicircular canal [12]) or extinct taxa (anterior andposterior canals) lacking the horizontal canal [34ndash37] However the isolation of posterior semicircularcanals from the other canals in modern elasmobranchs [3839] is not seen in Palaeospondylus Additionallya potential endolymphatic duct can be identified via an opening into the duct (figure 2bndashd electronicsupplementary material figure S1c) a character of extinct and extant craniates [39]

Crown-group gnathostome characters in Palaeospondylus also include the elongate telencephalonvertebral centra and possibly the ventral cranial fissure [4041] although the former may also becharacteristic of the closely related stem gnathostome Janusiscus [20] The precerebral fontanelle [2142]and the articulation of the palatoquadrate on the large L-shaped postorbital process on the lateralchondrocranium [13144243] indicate a closer relationship with chondrichthyans Certain Palaeozoicstem chondrichthyans have a postorbital process that includes a ventral contribution from the lateralcommissure (processes of the otic region) to enclose the jugular vein [14] If this were the case inPalaeospondylus the postorbital process would cross onto the otic capsule and run across the ventralcranial fissure However in the stem chondrichthyan Pucapampella it is the postorbital process thatextends ventrally to enclose the jugular canal (also in other taxa such as Cobelodus Tamiobatis andOrthacanthus [43]) more comparable to Palaeospondylus Pucapampella also possesses an otico-occipitalfissure which is lost in more derived chondrichthyans [44] Hence characters present in Palaeospondylusare also present in stem chondrichthyans

5 ConclusionPalaeospondylus gunni has been a perplexing vertebrate fossil since Traquair first described it in 1890 hereX-ray tomography provides new data and morphological characters demonstrating that Palaeospondylusis a jawed vertebrate Our interpretation of key jawed vertebrate characters in Palaeospondylus includethree semicircular canals with a horizontal canal prominent in the vestibular system the synarcual andjointed elements of the mandibular arch (palatoquadrate Meckelrsquos cartilage) Moreover multiple crown-group gnathostome characters are present (otico-occipital fissure (but also in ptyctodont placoderms

on June 27 2018httprsosroyalsocietypublishingorgDownloaded from

7

rsosroyalsocietypublishingorgRSocopensci4170214

[45])) elongate telencephalon and vertebral centra Characters that associate Palaeospondylus withchondrichthyans are a precerebral fontanelle foramina for lateral dorsal aorta in the chondrocraniumand the articulation of the palatoquadrate to the ventral postorbital process

This new analysis of Palaeospondylus strongly suggests that an assignment to the myxinoid (hagfish)stem group is based on misinterpretation of various characters [12] However the absencenon-preservation of teeth scales and fins continues to be problematic in determination of Palaeospondylus as ajawed vertebrate Nevertheless a number of acanthodian taxa resolved as stem chondrichthyans [4042]also lack teeth [46] As well Miller [31] described maceration of the lungfish Lepidosiren resulting in lossof the fins girdles and branchial arches comparable to post-mortem degradation potentially responsiblefor the absence of these elements in Palaeospondylus

Also problematic with regards to a chondrichthyan association is the composition of thePalaeospondylus cartilaginous skeleton that includes hypertrophied chondrocyte lacunae surroundedby mineralized matrix previously interpreted as representing an early stage in endochondral bonedevelopment [1047] a type of bone found in bony fishes (Osteichthyes) [48] The presence ofhypertrophied cells in chondrichthyan cartilage is disputed [4950] with mineralization characteristicallyonly in the perichondral tesserae [51] Nevertheless chondrichthyans are characterized by loss ofbone [4852] Palaeospondylus also lacks bone and instead manifests an entirely mineralized cartilagein the endoskeleton with matrix mineralization between and around the cell lacunae (interlacunarperilacunar) clearly illustrated in details of tissue structure (figure 1fh) The fact that this mineralizedtissue can be observed and not perichondral bone which normally forms in the connective tissuesurrounding the cartilage implies that the latter is indeed absent As a stem chondrichthyanPalaeospondylus may mark the loss of perichondral bone as well as dermal bone as part of the overallloss of bone within chondrichthyans including acanthodians [48]

These novel characters and newly evaluated ones allow a more precise relationship of Palaeospondylusto be proposed that can be challenged with new data or new imaging techniques directed towards thesehypotheses

Data accessibility Data files including movie through individual slices can be found at the NHM Data Portal (httpdatanhmacukdatasetpalaeospondylus)Authorsrsquo contributions ZJ CP MMS KT and SS conceived of the study CP carried out CTVOX analysis andprepared the figures SS carried out the synchrotron analysis (France) TS carried out the CT-analysis (Australia)ZJ CP MMS and KT drafted the manuscript and carried out the revision All authors gave final approval forpublicationCompeting interests We declare we have no competing interestsFunding ZJ and KT are funded by an Australian Research Council Discovery grant no DP110101127 KT is fundedby an Australian Research Council QE II Fellowship Synchrotron scanning was funded by the ESRF (proposalEC690 and inhouse beamtime) SS was supported by a young-researcher grant from the Swedish Research Council(Vetenskapsraringdet 2015ndash04335) TJS gratefully acknowledges the Australian Research Council for supportAcknowledgements We thank Paul Tafforeau (European Synchrotron Radiation Facility Grenoble France) for his helpwith the scanning and reconstructing the data as well as Juumlrgen Kriwet and Gerlinde Kaineder (University ofVienna) Farah Ahmed and Amin Garbout (NHM London) for access to three-dimensional rendering programmesand computer facilities Emma Bernard (NHM London) is thanked for access to Palaeospondylus specimens

References1 Newman MJ Trewin NH 2001 A new jawless

vertebrate from the Middle Devonian of ScotlandPalaeontology 44 43ndash51 (doi1011111475-498300168)

2 Newman MJ 2002 A new naked jawless vertebratefrom the Middle Devonian of ScotlandPalaeontology 45 933ndash941 (doi1011111475-498300269)

3 Andrews SD Hartely AJ 2015 The response of lakemargin sedimentary systems to climatically drivenlake level fluctuations Middle Devonian OrcadianBasin Scotland Sedimentology 62 1693ndash1716(doi101111sed12200)

4 Newman MJ Mark-Kurik E Den Blaauwen JLZupins I 2015 Scottish Middle Devonian fishes inEstonia Scot J Geol 51 141ndash147 (doi101144sjg2014-006)

5 Trewin NH 1986 Palaeoecology andsedimentology of the Achanarras bed of the MiddleOld Red Sandstone Scotland Trans R Soc EdinEarth Sci 77 21ndash46 (doi101017S0263593300010737)

6 Moy-Thomas JA 1940 The Devonian fishPalaeospondylus gunni Traquair Phil Trans R Soc B230 391ndash413 (doi101098rstb19400004)

7 Newman MJ den Blauuwen JL 2008 Newinformation on the enigmatic Devonian vertebratePalaeospondylus gunni Scot J Geol 44 89ndash91(doi101144sig44010089)

8 Forey PL Gardiner BG 1981 J A Moy-Thomas andhis association with the British Museum (NaturalHistory) Bull Br Mus Nat Hist Geol 35 131ndash144

9 Joss JMP Johanson Z 2007 Is Palaeospondylusgunni a fossil larval lungfish Insights from

Neoceratodus forsteri development J Exp Zool PartB 308 163ndash171 (doi101002jezb21125)

10 Johanson Z Kearsley A den Blaauwen J NewmanM Smith MM 2012 Ontogenetic development of anexceptionally preserved Devonian cartilaginousskeleton J Exp Zool Part B 318 50ndash58 (doi101002jezb21441)

11 Gardiner JD 2016 The fossil record of tadpoles FossilImp 72 17ndash44 (doi1014446FI201617)

12 Hirasawa T Oisi Y Kuratani S 2016 Palaeospondylusas a primitive hagfish Zool Lett 2 20 (doi101186s40851-016-0057-0)

13 Maisey JG Anderson ME 2001 A primitivechondrichthyan braincase from the EarlyDevonian of South Africa J Vert Paleo 21 702ndash713(doi1016710272-4634(2001)021[0702APCBFT]20CO2)

on June 27 2018httprsosroyalsocietypublishingorgDownloaded from

8

rsosroyalsocietypublishingorgRSocopensci4170214

14 Maisey JG 2008 The postorbital palatoquadrate

articulation in elasmobranchs J Morph 2691022ndash1040 (doi101002jmor10642)

15 Maisey JG Miller R Turner S 2009 The braincase ofthe chondrichthyan Doliodus from the LowerDevonian Campbellton Formation of NewBrunswick Canada Acta Zool 90 109ndash122(doi101111j1463-639520080030x)

16 Thomson KS Sutton M Thomas B 2003 A larvalDevonian lungfish Nature 426 833ndash834(doi101038nature02175)

17 De Beer G 1971 Development of the vertebrate skull552 p Oxford UK Oxford University Press

18 Bulman OMB 1931 Note on Palaeospondylus gunniTraquair Ann Mag Nat Hist 10 170ndash190

19 Sollas WJ Sollas IBJ 1904 An account of theDevonian fish Palaeospondylus gunni TraquairPhil Trans R Soc Lond B 196 267ndash294(doi101098rstb19040009)

20 Giles S Friedman M Brazeau MD 2015Osteichthyan-like cranial conditions in an EarlyDevonian stem gnathostome Nature 520 82ndash85(doi101038nature14065)

21 Schultze H-P 1993 Patterns of diversity in the skullsof jawed fishes In The skull vol 2 (eds J Hanken BKHall) pp 189ndash254 Chicago IL University ofChicago Press

22 Traquair RH 1890 On the fossil fishes atAchanarras Quarry Caithness Ann Mag NatHist Ser 6 479ndash486 (doi10108000222939008694071)

23 Traquair RH 1893 A still further contribution to ourknowledge of Palaeospondylus gunni Proc R SocEdin B 12 312ndash321

24 Traquair RH 1894 Palaeospondylus gunni Traq fromthe Caithness Flagstones Ann Scot Nat Hist Edin94ndash99

25 Dean B 1900 The so-called Devonian lampreyPalaeospondylusMem New York Acad Sci 2 1ndash32

26 Stensiouml EA 1927 The Devonian and Downtonianvertebrates of Spitzbergen 1 Family CephalaspidaeSkrift Svalbard Ish 12 1ndash139 (doi101604978045127472)

27 Ota KG Fujimoto S Oisi Y Kuratani S 2011Identification of vertebra-like elements and theirpossible differentiation from sclerotomes in thehagfish Nat Commun 373 1255 (doi101038ncomms1355)

28 Fleming A Kishida MG Kimmel CB Keynes RJ 2015Building the backbone the development and

evolution of vertebral patterning Development 1421733ndash1744 (doi101242dev118950)

29 Claeson K 2011 The synarcual cartilage of batoidswith emphasis on the synarcual of Rajidae JMorph 212 1444ndash1463 (doi101002jmor10996)

30 Johanson Z Trinajstic K Carr R Ritchie A 2013Evolution and development of the synarcual in earlyvertebrates Zoomorphology 132 95ndash110(doi101007s00435-012-0169-9)

31 Miller AE 1930 Notes on the tail skeleton ofLepidosiren paradoxa with remarks on theaffinities of Palaeospondylus Proc Zool Soc Lond1930 783ndash789 (doi101111j1096-36421930tb00997x)

32 Janvier P Sansom RS 2015 Fossil hagfishes fossilcyclostomes and the lost world of lsquoostracodermsrsquoIn Hagfish biology (eds SL Edwards GG Goss)pp 73ndash94 Boca Raton FL CRC Press

33 Ladich F Schulz-Mirbach T 2016 Diversity in fishauditory systems one of the riddles of sensorybiology Front Ecol Evol 4 28 (doi103389fevo201600028)

34 Stensiouml EA 1958 Les cyclostomes fossiles ouostracodermes In Traiteacute de Paleontologie 13(ed J Piveteau) pp 173ndash425 Paris France Masson

35 Stensiouml EA 1963 The brain and the cranial nerves infossil lower craniate vertebrates Skrift UtgittNorske Vidensk-Akad 13 5ndash120

36 Janvier P 1981 The phylogeny of the Craniata withparticular reference to the significance of fossillsquoagnathansrsquo J Vert Paleo 1 121ndash159 (doi10108002724634198110011886)

37 Janvier P 1981 Early vertebrates 393p Oxford UKClarenodon Press

38 Retzius G 1881 Das Gehoumlrorgan der Wirbelthiere vol1 226 p Stockholm Sweden Samson andWallin

39 Maisey JG 2001 Remarks on the inner ear ofelasmobranchs and its interpretation from skeletallabyrinth morphology J Morph 250 236ndash264(doi101002jmor1068)

40 Dupret V Sanchez S Goujet D Tafforeau P AhlbergPE 2014 A primitive placoderm sheds light on theorigin of the jawed vertebrate face Nature 507500ndash503 (doi101038nature12980)

41 Brazeau MD Friedman M 2014 The characters ofPalaeozoic jawed vertebrates Zool J Linn Soc 170779ndash821 (doi101111zoj12111)

42 Davis SP Finarelli JA Coates MI 2012 Acanthodesand shark-like conditions in the last common

ancestor of modern gnathostomes Nature 486247ndash250 (doi101038nature11080)

43 Maisey JG 2007 The braincase in Paleozoicsymmoriiform and cladoselachian sharks Bull AmMus Nat Hist 541 1ndash122 (doi1012060003-0090(2007)307[1TBIPSA]20CO2)

44 Coates MI Sequiera SEK 1998 The braincase of aprimitive shark Trans R Soc Edin Earth Sci 8963ndash85 (doi101017S026359330000701X)

45 Trinajstic K Long JA Johanson Z Young G SendenT 2012 Newmorphological information on thePtyctodontid fishes (Placodermi Ptyctodontida)fromWestern Australia J Vert Paleo 32 757ndash780(doi101080027246342012661379)

46 Hanke GF Wilson MVH 2004 New teleostome fishesand acanthodian systematics In Recent advancesin the origin and early radiation of vertebrates (edsG Arratia MVHWilson R Cloutier) pp 189ndash216Munich Germany Verlag Dr Friedrich Pfeil

47 Johanson Z Kearsley A den Blaauwen J NewmanM Smith MM 2010 No bones about it an enigmaticDevonian fossil reveals a new skeletal framework -a potential role of loss of gene regulation Sem CellDev Biol 21 414ndash423 (doi101016jsemcdb200910011)

48 Ryll B Sanchez S Haitina T Tafforeau P Ahlberg PE2014 The genome of Callorhinchus and the fossilrecord a new perspective on SCPP gene evolutionin gnathostomes Evol Dev 16 123ndash124(doi101111ede12071)

49 Eames BF Allen N Young J Kaplan A Helms JASchneider RA 2007 Skeletogenesis in the swellshark Cephaloscyllium ventriosum J Anat 210542ndash554 (doi101111j1469-7580200700723x)

50 Dean MN Mull CG Gorb SN Summers AP 2009Ontogeny of the tessellated skeleton insight fromthe skeletal growth of the round stingray Urobatishalleri J Anat 215 227ndash239 (doi101111j1469-7580200901116x)

51 Dean MN Ekstrom L Monsonego-Ornanc EBallantyne E Witten PE Riley C Habrakena WOmelon S 2015 Mineral homeostasis and regulationof mineralization processes in the skeletons ofsharks rays and relatives (Elasmobranchii) SemCell Dev Biol 46 51ndash67 (doi101016jsemcdb201510022)

52 Venkatesh B et al 2014 Elephant shark genomeprovides unique insights into gnathostomeevolution Nature 505 174ndash179 (doi101038nature12826)

on June 27 2018httprsosroyalsocietypublishingorgDownloaded from