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ResearchCite this article: Modesto SP, Scott DM,MacDougall MJ, Sues H-D, Evans DC, Reisz RR.

2015 The oldest parareptile and the early

diversification of reptiles. Proc. R. Soc. B 282:20141912.

http://dx.doi.org/10.1098/rspb.2014.1912

Received: 31 July 2014

Accepted: 10 December 2014

Subject Areas:palaeontology, taxonomy and systematics

Keywords:carboniferous, diversification, evolution,

parareptile

Author for correspondence:Robert R. Reisz

e-mail: [email protected]

Electronic supplementary material is available

at http://dx.doi.org/10.1098/rspb.2014.1912 or

via http://rspb.royalsocietypublishing.org.

& 2015 The Author(s) Published by the Royal Society. All rights reserved.

The oldest parareptile and the earlydiversification of reptiles

Sean P. Modesto1, Diane M. Scott2, Mark J. MacDougall2, Hans-Dieter Sues3,David C. Evans4 and Robert R. Reisz2

1Department of Biology, Cape Breton University, Sydney, Nova Scotia, Canada B1P 6L22Department of Biology, University of Toronto at Mississauga, Mississauga, Ontario, Canada L5L 1C63National Museum of Natural History, Smithsonian Institution, MRC 121, PO Box 37012, Washington,DC 20013-7012, USA4Department of Natural History, Royal Ontario Museum, 100 Queens Park, Toronto, Ontario, Canada

Amniotes, tetrapods that evolved the cleidoic egg and thus independence fromaquatic larval stages, appeared ca 314 Ma during the Coal Age. The rapiddiversification of amniotes and other tetrapods over the course of the LateCarboniferous period was recently attributed to the fragmentation of coal-swamp rainforests ca 307 Ma. However, the amniote fossil record during theCarboniferous is relatively sparse, with ca 33% of the diversity representedby single specimens for each species. We describe here a new species ofreptilian amniote that was collected from uppermost Carboniferous rocks ofPrince Edward Island, Canada. Erpetonyx arsenaultorum gen. et sp. nov. is anew parareptile distinguished by 29 presacral vertebrae and autapomorphiesof the carpus. Phylogenetic analyses of parareptiles reveal E. arsenaultorum asthe closest relative of bolosaurids. Stratigraphic calibration of our results indi-cates that parareptiles began their evolutionary radiation before the close of theCarboniferous Period, and that the diversity of end-Carboniferous reptiles is80% greater than suggested by previous work. Latest Carboniferous reptileswere still half as diverse as synapsid amniotes, a disparity that may be attribu-table to preservational biases, to collecting biases, to the origin of herbivory intetrapods or any combination of these factors.

1. IntroductionPhylogenetic studies of the past three decades confirm the basal dichotomy ofamniotes into synapsids (i.e. mammals and their fossil relatives) on the onehand and reptiles (e.g. squamates, crocodiles, birds and their fossil relatives;a.k.a. sauropsids) on the other hand [13]. Whereas the timing of the originand basal amniote dichotomy during the Carboniferous Period is highly debated[4,5], the oldest unequivocal amniote fossils are known from the Joggins For-mation of Nova Scotia, Canada, and are generally regarded to be 313316million years (Ma) in age [5].

Among the 10 tetrapod taxa described from the Joggins formation, only twoamniote species are recognized as valid [5,6]. The amniote fossil record continuesto be sparse at succeeding Carboniferous localities, with the exception of the EarlyKasimovian (ca 305 Ma) amniote-rich fauna at Garnett, Kansas [7,8]. Neverthe-less, reviews of the alpha taxonomy of Carboniferous amniotes revealed thatthe early diversification of synapsids outpaced that of reptiles, with the resultthat, by the end of the Carboniferous, synapsid species outnumbered reptilesapproximately 2 to 1 [9,10]. An interesting corollary of the disparity in diversitybetween these two great clades of amniotes is that Carboniferous reptiles aresubstantially smaller animals than contemporaneous synapsids [9].

A more dramatic dichotomy exists within early Reptilia itself: all Carbonifer-ous species of this group are classified as members of Eureptilia [3], whereascontemporaneous members of the sister group Parareptilia have yet to be ident-ified. Instead, a single ghost taxon has been reconstructed for Parareptilia,inferred to extend from the Permian Period down to the origin of amniotes [11].

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Figure 1. Erpetonyx arsenaultorum n. gen. et sp., ROM 55402, holotype. (a) Interpretive drawing of skeleton in dorsal aspect. (b) Photograph of skeleton in dorsalaspect. as, astragalus; ca, calcaneum; ca5, caudal vertebra 5; ca15, caudal vertebra 15; cr1, caudal rib 1; dca, distal caudal vertebra; fe, femur; fi, fibula; h, humerus;il, ilium; is, ischium; mt, metatarsal; pi, pisiform; pu, pubis; r, radius; sr3, sacral rib 3; ti, tibia; u, ulna; ul, ulnare; un, unguals. Arabic numerals identify cervicalvertebrae. (Online version in colour.)

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We describe here the first Carboniferous parareptile, based on anearly complete, articulated skeleton from Prince EdwardIsland, Canada. The early appearance and the phylogeneticrelationships of this new parareptile have dramatic impli-cations for our understanding of the early diversification ofreptiles and amniotes.

2. MaterialThe study material (figure 1) comprises a nearly complete,articulated skeleton preserved on a sandstone slab and repos-ited in the collections of the Royal Ontario Museum, Toronto,as ROM 55402. The fossil was prepared mechanically by useof air scribes and pin vices.

The presence of plicidentine and the similarity of thedorsal vertebrae of ROM 55402 to those described for theEarly Permian parareptile Delorhynchus cifellii [12] strongly

suggested parareptilian affinities for the Prince Edward Islandreptile. For our phylogenetic analysis, we used an augmentedversion of the characters and data matrix of Reisz et al. [12].Although a recent study has resurrected the hypothesis that tur-tles are parareptiles [13], the problem of turtle origins is beyondthe scope of our studythe relationships of a Late Carbonifer-ous reptile and its implicationsso we did not include turtletaxa (e.g. Odontochelys and/or Proganochelys) in our analysis.We recoded some taxa for certain characters (see the electronicsupplementary material for data matrix), and performed a heur-istic analysis, set to collapse branches with a maximum length ofzero, in PAUP 4.0a134 [14]. We also conducted a Bremer decayanalysis using the heuristic algorithm in PAUP, by relaxing par-simony a single step at a time and generating strict consensustrees until resolution was completely lost in the ingroup. Wealso conducted a bootstrap analysis (1000 replicates).

In addition to the traditional parsimony analysis, a Bayesiananalysis was also conducted on the dataset in order to assess its

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robusticity to different methods of phylogeny estimation [15].The Bayesian analysis of the morphological data matrix was con-ducted using MRBAYES v. 3.1.2 [16], and employed the Mk model(datatype standard) with the addition of a gamma shape par-ameter (rates variable) to allow for rates of change to varyacross characters, as recommended by Muller & Reisz [3]. Theanalysis was run for 3 000 000 generations (Markov ChainMonte Carlo (MCMC): four chains, two simultaneous indepen-dent runs), with a tree sampled every 100 generations, with thefirst 10% of the sampled trees being discarded as the burn-in.The majority-rule consensus tree with nodal clade credibilityvalues is presented in the electronic supplementary material.

The results of our analyses indicate that the new PrinceEdward Island reptile is closely related to bolosaurid para-reptiles. Accordingly, we resurrect the name Bolosauria,which was erected as an ordinal name by Kuhn [17] to con-tain the family Bolosauridae Cope, 1878, and define it as abranch-based group: Bolosaurus striatus Cope, 1878 [18] andall species related more closely to it than to Procolophontrigoniceps Owen, 1876 [19].
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3. Systematic palaeontologyParareptilia Olson, 1947 [20].Bolosauria Kuhn, 1959 [17].Erpetonyx arsenaultorum n. gen. et sp.

(a) EtymologyThe genus name is from classical Greek 1rp1ton, crawler,and onys, claw. The specific epithet honours the Arsenaultfamily of Prince County, Prince Edward Island, Canada, whodiscovered and collected the specimen.

(b) MaterialROM 55402, holotype, a nearly complete, mostly articulatedskeleton (figure 1a,b).

(c) Locality and horizonROM 55402 was collected from a locality at Cape Egmont insouthwestern Prince Edward Island, Canada. The EgmontBay Formation crops out along the western part of the island,and is regarded to be latest Pennsylvanian (Stephanian) in geo-logical age on the basis of plant body fossils and pollen [21].Thus, the fossil is Gzhelian in age (303.7 to 298.9 Ma) [22].

(d) DiagnosisA small, basal parareptile that possesses 29 presacral vertebrae(viz. five cervicals and 24 dorsals), relatively small carpalbones (the radiale and the pisiform are ca one-half the size ofthe ulnare and the fifth distal carpal, respectively), a femoraldistal end with an epicondylar axis at 458 to the shaft, afourth metatarsal with a relatively broad distal end, andwell-developed unguals with prominent flexor tubercles.

4. DescriptionROM 55402 (figure 1) comprises a nearly complete articulatedskeleton that is preserved largely in dorsal view, and spanningca 20 cm across a sandstone block. The skull, both manus, theleft pes and the right hind limb are disarticulated to varying

degrees. Much of the skull roof, dorsal portions of most ofthe presacral vertebrae and numerous trunk ribs have beendamaged by weathering. The tail, partly disarticulated andmissing an estimated 15 caudal vertebrae, is otherwise wellpreserved. The well-ossified nature of the autopodia and theclosure of neurocentral sutures in the sacral and presacralvertebrae indicate that the skeleton is that of an adult animal.

(a) SkullThe skull of ROM 55402 is compressed obliquely and waspartly disarticulated prior to burial (figures 1 and 2a). Roughlyhalf of the skull bones, particularly those of the dermal skullroof, are weathered, such that either their surficial details ortheir outlines, or both, are indistinct. The immediately identifi-able dermal bones are the premaxilla, the maxilla, the frontal,the lacrimal, the prefrontal and the supratemporal. A large, par-tially moulded surface anteriorly represents the impressions ofthe ventral surface of the nasals.

The premaxilla is preserved only as a section throughthe left element. Both maxillae are present, but preservedand/or exposed to varying degrees. The anterior end of theleft maxilla is exposed in medial aspect, and shows that themaxilla formed the posteroventral corner of the externalnaris. The dorsal portion of the right maxilla has beeneroded down to a spindle-shaped alveolar region anteriorly,exposing the bases of 13 teeth. Two (missing) teeth couldhave fit into the space between the last and penultimatemaxillary teeth preserved, such that the maxilla featured atleast 15 tooth positions.

The exposed bases of the anterior-most seven teeth showthe simple infolding that is indicative of the plicidentine thatis seen in Colobomycter pholeter and several other parareptiles[23,24]. Infolding extends down the length of the largestteeth (figure 2b). The teeth are slightly recurved, sharplytipped conical structures that lack cutting edges. There isneither a caniniform tooth nor caniniform region. The teethgradually diminish in both length and basal diameter asone progresses posteriorly.

The left lacrimal is preserved in articulation with theleft maxilla, and is exposed here mostly in posteromedialview, where it forms the anterolateral corner of the orbit(figure 2a). The facial portion extends anteriorly, but ismostly obscured by the nasal impression; it is not clearhow far anteriorly the lacrimal extended.

Both frontals are preserved as a motley of heavilyweathered bone and impression. Each frontal is least sixtimes longer than it is wide. The middle third of the lateralmargin is faintly concave and represents the dorsal marginof the orbit. There is a distinct posterolateral process,which bears a shallow shelf for the reception of the parietal.Closely associated with the left frontal is the left prefrontal,which consists of a slightly curved antorbital flange and atongue-shaped facial process.

An irregularly shaped dermal bone, with what appears tobe a small posterior hornlet, is identified here as the rightsupratemporal (figure 2a). Whereas the medial and posteriormargins are well preserved, the anterior and lateral marginsof this bone are heavily weathered (yielding an unnaturallystraight lateral or anterolateral margin). The well-preservedposterior margin consists of a faintly sinusoidal free edgefrom which projects a small, narrow, tongue-like projection


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Figure 2. Erpetonyx arsenaultorum n. gen. et sp., ROM 55402, holotype. (a) Interpretive drawing of skull. (b) Photograph of right maxillary dentition in lateral view.(c) Results of phylogenetic analysis; tree length 557, consistency index (CI) 0.3429, CI excluding informative characters 0.3405, retention index 0.6355,rescaled CI 0.2179. Bootstrap/Bremer support values: Bolosauria: 39/3; Parareptilia: 13/1; clade A: 33/2; clade B (Procolophonomorpha): 32/2; clade C: 11/2; cladeD (Ankyramorpha): 12/2; clade E: 19/2; clade F: 44/1; clade G: 15/1. Bolosauria is diagnosed by the following unambiguous synapomorphies: postparietal small(character 9, state 1); transverse flange of pterygoid dentition present (character 70, state 1); anterior caudal ribs elongate and extend posteriorly to end of nextvertebra (character 132, state 0); greater trochanter of femur present (character 156, state 1); maxillary tooth positions number 15 or fewer (character 167, state 0).Anatomical abbreviations: an, angular; ar, articular; at.na, atlantal neural arch; ax, axis; cl, clavicle; cth, cleithrum; d, dentary; dc2, distal carpal 2; dc4, distal carpal 4;c.pr, cultriform process of parasphenoid; eo, exoccipital; ep, epipterygoid; f, frontal; int, intermedium; j, jugal; l, lacrimal; m, maxilla; n, nasal; op, opisthotic; p,parietal; pal, palatine; pf, postfrontal; pm, premaxilla; po, postorbital; pra, prearticular; pro, prootic; prf, prefrontal; prt, proatlas; pt, pterygoid; q, quadrate; qj,quadratojugal; rd, radiale; sa, surangular; sc, scapula; so, supraoccipital; sp, splenial; sq, squamosal; st, supratemporal; t, tabular; v, vomer. Arabic numerals identifycervical vertebrae. (Online version in colour.)


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or hornlet. Where the dorsal surface is well preserved, it issmooth and featureless.

Various fragments of relatively thick bone that are clearlydermal roofing elements, but are not informative morpho-logically, are tentatively identified as the parietal, thepostfrontal, the postorbital, the squamosal, the postparietaland the tabular bones.

The palatal bones are not well exposed. The anterior endsof the slender, paired vomers are preserved anteriorly in closeassociation with the premaxilla. The left palatine is preservedin articulation with the left lacrimal in its expected position,partly exposed between the two separated frontal bones.The only other unequivocal palatal bone is a denticulatedsheet of bone positioned posteriorly that, judging from therelative thinness of the bone and its distinctive curvature,probably represents parts of the base of the quadrate ramusand the pterygoid transverse process. The palatal denticlesare tiny, simple cones. As in Feeserpeton and many other para-reptiles [25], the denticles extend onto the quadrate ramus ofthe pterygoid. There are fragments of thin, smoothly finishedbone elsewhere that may represent fragments of palatalelements, but these are uninformative.

The dorsal columella of an epipterygoid projects frombeneath fragments of parietal bone. A remarkably robustright quadrate is preserved in its expected position, in theposterolateral corner of the skull, with the condyle directedposteriorly and the anterolateral surface of the dorsal lamellafacing upwards. The quadrate condyle is a knuckle-like block

of bone, slightly broader transversely than anteroposteriorlylong, with a saddle-shaped articulating surface for the articu-lar. The dorsal lamella is a trapezoidal plate that is roughly astall as it is broad. In its general morphology, the quadrate ofROM 55402 resembles that of Belebey vegrandis [26].

Most braincase elements are present, but overlying dermalbone fragments preclude full descriptions (figure 2a). The para-basisphenoid is identifiable because of its prominent cultriformprocess, which is present as a slender trough formed of thin,low plates of bone. Although narrowing anteriorly, itsanterior-most tip is missing; what is present indicates a longprocess, which is roughly equal in length to the body of thebraincase, and probably extended the entire length of the inter-pterygoid vacuity. The main body of the parabasisphenoid ispoorly preserved, bearing a weathered right clinoideus processand a partly exposed, poorly ossified retractor pit.

What is exposed of the prootics largely conforms with thegeneral morphology of this element in other early reptiles. Anexception is a ventral concavity in the anterior end of theright prootic, which possibly formed the dorsal half of a fora-men that was completed ventrally by the parabasisphenoid,and may represent the opening for the hyomandibularbranch of the facial nerve [27].

Immediately posterior to the prootics are the opisthotics,with their deep, U-shaped excavations of unfinished bonerepresenting the posterior portions of the membranous labyr-inths. A stubby paroccipital process extends laterally fromthe main body of the right opisthotic. Between the opisthotics



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lies the broad, plate-like supraoccipital, identifiable bythe embayment in its ventral margin forming the dorsalportion of the foramen magnum. Only the ventral portionof the left exoccipital is preserved, as a slightly curved,hourglass-shaped bone.

The mandible is represented by the dentary, splenial andarticular of the right ramus and the angular, the surangularand the prearticular of the left ramus (figure 2a). The dentaryis worn down by weathering and is identifiable by its pos-ition and its outline, but it is not preserved well enough fordescription. Closely appressed to the dentary is the betterpreserved splenial; it has a smooth lingual surface and doesnot contribute to the mandibular symphysis. The angularand the surangular are low, elongate and slightly curvedbones; the dorsal margin of the latter bone is a low, weaklyconvex edge. The prearticular is a slender, slightly curvedelement with a dorsoventrally expanded posterior end. Thearticular is preserved upside-down with respect to the skulland rotated slightly more than 908 anticlockwise, such thatboth the posterior-most end of the ventral edge of the mand-ible and the pterygoideus process are exposed in ventralview. It is an irregularly shaped bone with a well-developedretroarticular process, the ventral surface of which isdamaged. The insertion surface for the pterygoideus muscu-lature is visible as a slightly sigmoidal depression betweenthe planed-down ventral extremities of the articular.

(b) Postcranial axial skeletonThe backbone is preserved as a sinusoidal, largely articulatedseries of 65 vertebrae, plus 10 disarticulated caudal vertebrae(figure 1). We estimate that an arc between the two articu-lated caudal series would accommodate about 25 vertebrae,suggesting thatminus the 10 disarticulated caudalsabout 15 caudal vertebrae from the middle to distal part ofthe tail are not preserved. Nearly all neural spines havebeen weathered down to low stumps.

There are 29 presacral vertebrae. Among non-mesosaurianparareptiles, presacral vertebrae number 26 or fewer [2830].As is typical for early amniotes, there is no morphological dis-tinction between the last cervical vertebra and the first dorsalvertebra, but rib morphology suggests that there are five cervi-cal vertebrae. A proatlas, portions of the atlas and the axis arepresent, but not morphologically informative. Beginning withthe third cervical vertebra, the presacral neural arches exhibita distinctive hourglass-shaped outline in dorsal aspect. Thepresacral neural arches are relatively narrow; the breadthacross the postzygapophyses of the fifth cervical is ca 62% ofthe total anteroposterior length of the arch.

Twenty-four vertebrae form the dorsal series (figure 1). Theneural arches gradually increase in both breadth and lengthposteriorly down the column, such that the 16th dorsal (two-thirds of the way down the dorsal series) is approximately25% broader and longer than an anterior dorsal vertebra. Alldorsal neural arches feature the conspicuous hourglass-shapedorganization seen in the posterior cervicals. The hourglassshape seen in dorsal aspect is enhanced by oblique, paired exca-vations in the dorsolateral surfaces of the arch, positionedbetween the transverse process and a ridge extending from theposterior part of the prezygapophysis to the midpoint ofthe dorsal midline of the arch. Because of the tight articulationof the vertebrae, none of the zygopophyseal facets is fully visible,but they appear to be subcircular in outline, and inclined very

weakly from the horizontalthose of the prezygapophysesfacing slightly medially, perhaps as much as 108, whereasthose of the postzygapophyses tilt slightly laterally incomplementary fashion.

There are three sacral vertebrae. As is typical of earlyterrestrial tetrapods [31,32], the first sacral has a neural archmorphology that is transitional to that seen in the preced-ing dorsal vertebra and the succeeding caudals in that theprezygapophyses are relatively broad, matching the broadpostzygapophyses of the dorsal vertebra, but with the postzy-gapophyses forming a distinctly narrow posterior end to thefirst sacral neural arch, commensurate with the relativelynarrow arches of the anterior-most caudals. There are threepairs of sacral ribs. The first and second ribs are flared laterallyand similar in size, but the third sacral rib is a finger-likeprojection that had only a touch contact with the iliac blade.

Forty-three caudal vertebrae are preserved (figure 1). Thebase of the tail forms a tightly articulated series up to, andincluding, caudal 20, and there is an articulated series of 13distal caudals preserved adjacent to presacrals 1925. If thelatter series is preserved in normal position with respect tothe proximal articulated series (i.e. the base of the tail), weestimate that approximately 25 caudal vertebrae would arcalong this missing part of the tail. Ten caudals of intermedi-ate size, including several single disarticulated caudals, twopairs of caudals and a loose articulated series of three caudals,are scattered loosely in this area, indicating that about 15caudal vertebrae are not preserved. Altogether, at least 58caudal vertebrae were present, a number closely comparableto that described for other early reptiles [29,32,33].

(c) Appendicular skeletonThe appendicular bones are preserved in close associationwith those of the axial skeleton (figure 1). However, exceptfor the left ilium, they are mostly overlain either by the ver-tebral column, or by neighbouring elements. Most elementsof the pectoral girdle are present, but they are not wellexposed. What is visible of each suggests a morphologyvery similar to that of other early terrestrial reptiles [28,33].

Elements of the pectoral limb are well preserved andexposed for the most part. The humerus is roughly the samerelative size and morphology as this element in other earlyreptiles. However, there is little development of a trochleaand a capitulum for articulation with the ulna and the radius,respectively, suggesting more freedom of movement atthe elbow compared with early sprawling reptiles, such asCaptorhinus [34]. The radius and the ulna are just under 80%of the length of the humerus. The olecranon process of theulna is not well developed, being little more than a nubbin.

Neither manus is complete and both are disarticulated tovarying degrees. The right carpus is preserved fully articu-lated as a mosaic of irregular tile-like polygons. The radiale,the pisiform, and the first and fifth distal carpals are unu-sually small for an early reptile. The elements distal to thecarpus are not articulated well enough to provide a goodunderstanding of the structure of the digits in either manus.Apart from the right fifth metatarsal, none of the metacarpalsremains in articulation with its respective distal carpal. Some12 non-ungual phalanges and a single unequivocal ungual(less than 40% of the 34 phalanges that are expected, assum-ing a plesiomorphic phalangeal formula of 23453 [2])are all that remain of the manual digits. The non-terminal



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phalanges are dorsoventrally compressed, gently waistedbow ties of bone. The ungual is a distinctly claw-like elementwhich has a relatively broad, elliptical articulating head, aprominent flexor tubercle (roughly the same relative size asin the synapsid Dimetrodon [35]), and an acute tip.

All of the pelvic girdle elements are present in varyingdegrees of exposure and completeness, and are closely associ-ated with each other and with neighbouring bones (figure 1).Only the left ilium is fully exposed (in medial aspect). It exhi-bits a relatively deep, posterodorsally directed iliac blade;there is no anterodorsal process. The pubes are largelyobscured by overlying elements, but what is visible indicatesthat these bones are relatively flat and very short, subrectan-gular elements. The ischia are slightly better exposed than thepubes, revealing that each ischium is a flat tongue of bonethat closely resembles the ischia of other early reptiles[36,37]. The ischium is primitive in being substantiallylonger than the pubis.

The femur closely resembles that of other early reptiles,except that the distal end features a strong, ca 458 angleformed by the condyles with respect to the long axis ofthe bone (this angle ranges from 10 to 308 in most early reptiles[3538]). The tibia and the fibula are slender, slightly bowedrods of bone that are ca 75% the length of the femur. Thepedes are almost entirely disarticulated; neither tarsus isintact, and only the astragalus on the left side and the calca-neum on the right side remain of the proximal tarsals. Theastragalus is a rectangular (or transversely compressed,L-shaped) plate that is nearly twice as long as it is broad. Thecalcaneum is a D-shaped plate of bone, thickest along itsstraight, medial edge, and it thins gradually laterally. Fiverobust, polygonal distal tarsals are preserved. Three on theleft side are semi-articulated; two smaller, irregular bonesappear to be (because of their associations with distal tarsal 4and the metatarsals) distal tarsals 3 and 5. The metatarsalsare gently to moderately waisted rods of bone. The longest isinterpreted here to be the fourth metatarsal; it is about 66%of the total length of the fibula. Apart from the relativelybroad distal end of the fourth metatarsal, the morphology ofthe metatarsus is consonant with what has been describedand illustrated for other early, terrestrial reptiles. A total of21 pedal phalanges, including four unguals, are preserved.The left pes, with 12 non-terminal phalanges, preservesthe majority of these. The non-terminal phalanges havehourglass-shaped outlines in dorsal aspect. Whereas thenon-terminal toe bones are dorsoventrally compressed, andthus most of them are preserved in dorsal or ventral aspect,the unguals are mediolaterally compressed, and all are pre-served on their sides. The ungual of the fourth digit ispreserved on its lateral surface, and has a distinctly claw-shaped profile, with a remarkably robust, polygonal proximalend giving rise to a dorsoventrally narrow, weakly curvingdistal tip, accentuated by the slightly more convex dorsalmargin of the entire element. A shallow groove runs thelength of the medial surface of the claw-like tip. The ventral sur-face of the proximal portion bears a broadly rounded flexortubercle that, commensurate with the position of the end ofthe longest pedal digit, is the largest among the preservedunguals. An equally well-preserved ungual lies close by and pre-sumably belongs to a more medial digit. It is slightly longer, andhas a more acute profile as a result of having a less robust prox-imal portion and smaller flexor tubercle. The pedal unguals arethe longest phalanges present, and if correctly associated with

their respective penultimate phalanges, the pedal unguals areca 33% longer than the penultimate pedal phalanges.

5. DiscussionOur parsimony analysis (figure 2c) positions Erpetonyxarsenaultorum as the sister taxon of Bolosauridae, which is rep-resented in our analysis by the genera Belebey and Eudibamus.We attach the name Bolosauria to the clade of Erpetonyx,Belebey and Eudibamus (see Material section for phylogeneticanalysis and the electronic supplementary material for list ofcharacters and data matrix). Support for Bolosauria and Bolo-sauridae is moderate, with Bremer support values of 3 and 4,respectively; all clades except Pareiasauridae collapse with theaddition of six extra steps. The Bayesian analysis also recov-ered Bolosauria, but the overall phylogeny differs in thetransposition of Bolosauria and Australothyris, and in the place-ment of Mesosauridae at the base of Eureptilia (see theelectronic supplementary material).

A bolosaurian identification for Erpetonyx arsenaultorum,together with its latest Carboniferous age, has importantimplications for early parareptile diversification and reptilianevolution. Prior to the discovery of ROM 55402, the oldestparareptilian fossils were known from the Asselian Stage ofthe Permian Period of New Mexico, USA [39], and phyloge-netic reconstructions required a long ghost taxon forParareptilia to extend from the Asselian (ca 295 Ma) down tothe latest Moscovian Stage (ca 314 Ma) of the Carboniferousperiod (figure 3).

The inclusion of Erpetonyx arsenaultorum in a phylogeneticanalysis of Parareptilia results in bolosaurs being positionedcloser to the base of the parareptilian tree (as the basal-mostmembers of Procolophonomorpha; sensu Modesto et al. [40])and the Richards Spur taxon Microleter mckinsieorum movingdeeper into the tree with respect to previous phylogeneticstudies of Parareptilia [12,14,25,40]. The sister-group relation-ship between Erpetonyx arsenaultorum and Bolosauridaenecessitates the extension of four parareptilian ghost lineagesor ghost taxa (for Mesosauridae, Millerosauria, Bolosauridaeand the clade of Australothyris smithi and Ankyramorpha)from the Early Permian down into the Gzhelian Stage of the Car-boniferous Period. This results in a fivefold increase (from one tofive lineages) for the diversity of parareptiles at the end of theCarboniferous, and an 80% increase (from five to nine lineages)for the diversity of reptiles at the end of the Carboniferous (seeelectronic supplementary material, figure S4).

Our results are consonant with previous work by Reisz[10], who reported that Carboniferous species of reptileswere outnumbered ca 2 to 1 by contemporaneous synapsids.Owing to lack of phylogenetic resolution among Palaeozoicreptiles at the time, Reisz [10] relied on comparisons ofgroup diversity (sensu Norell [41]), i.e. direct counts of taxicoccurrences. Our phylogenetic results, when calibrated strati-graphically and compared with stratigraphic calibrations ofeureptilian [3] and synapsid [42,43] trees, confirm that repti-lian diversification during the Carboniferous was outpacedby that of synapsids, but only during the Gzhelian Stage(303.4299.0 Ma), with synapsids numbering 17 species perlineages versus reptiles numbering only 9.

Recently, Sahney et al. [44] inferred that the fragmentationand collapse of coal-swamp forests ca 307 Ma promoteddiversification of post-Moscovian (latest Carboniferous)


323.2 Carboniferous 298.9272.3 259.8

Permian 252.2

global standard stages

global standard series

Parareptilia

Bashkir Moscov Kas Gzhel Assel Sakmar Artinsk Kungur Road Word Capit Wuchia ChPennsylvanian Cisuralian Guadalupian Lopingian

Ankyramorpha

Erpetonyx Millerosauria

Synapsida

Eureptilia

MicroleterReptilia

Bolosauridae

Mesosauridae

Australothyris

Lanthanosuchia

Nyctiphruretidae Procolophonia

Figure 3. Temporal calibration of Reptilia composed of parareptilian phylogeny shown in figure 2c. Black bars are known ranges, open bars are ghost taxa and ghostlineages. Timescale from International Commission on Stratigraphy [22].


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tetrapods, including the amniotes. Sahney et al. [44] inferred avicariant mode of diversification for Coal Age tetrapodsresulting from coal-forest fragmentation. If this is the case,we should expect to see similar diversity in closely relatedgroups. Because sister taxa are the same age [41], a compari-son of the numbers of species in sister taxa is an appropriatetest [45]. If reptiles and synapsids (sister taxa) respondedvicariantly to coal-forest fragmentation, they should showsimilar taxic diversity, particularly because both reptilesand synapsids are found at the same localities (indicatingthat both groups were equally widespread and thus suscep-tible to fragmentation). Our examination of Carboniferousamniote phylogenetic diversity provides a more completeand detailed timeline of diversification in Carboniferoustaxa than provided by Sahney et al. [44]. For instance, thereis evidence for a single species each for synapsids and reptilesduring the Moscovian Stage (311.7307.2 Ma), and for thelate Kasimovian (ca 305 Ma)a time when coal-swamp for-ests were reduced to tiny wet spots [44]our studyindicates that reptiles and synapsids were, indeed, equallydiverse (8 reptilian species versus 10 synapsids). Accordingly,late Kasimovian amniote diversity patterns are consonantwith the hypothesis of Sahney et al. [44]. Amniote diversitypatterns change during the succeeding Gzhelian Stage, how-ever, and by the end of the Carboniferousand more than4.5 Ma after coal forests were little more than isolated refu-giasynapsids outnumbered reptiles ca 2 to 1 (17 synapsidspecies versus 9 reptiles).

If fragmentation of the Carboniferous coal swamps drovethe diversification of amniotes and other tetrapods duringthe Kasimovian Stage, what might account for the disparityseen between synapsid and reptilian diversity by the end ofthe Gzhelian Stage? Our results do not reject the possibilitythat coal-forest fragmentation drove amniote diversificationduring the Gzhelian Stage [44]. However, preservational biasmay be responsible for the low diversity of Gzhelian reptiles,for such diversity rests entirely upon Erpetonyx as the soledatum point for Reptilia in this 4.8-Myr-long stage. Previousworkers [43] had regarded Hamilton Quarry, which preservesthe (previous) youngest Carboniferous reptile (Spinoaequalisschultzei) as 303 Ma, or Gzhelian in age. As recognized bySahney et al. [44], this locality is actually late Kasimovian inage (early Virgilian Age of North American Carboniferoussystem). Thus, the greater diversity of Gzhelian synapsids is

partly a reflection of the astonishingly poor fossil record of rep-tiles during this stage. Gzhelian amniotes may have beensubject to a strong collecting bias, in which the larger synapsidfragmentary remains were more easily discovered and deemedsufficiently significant to be collected and described, whereasvery small, fragmentary reptilian remains either were muchmore difficult to find at Gzhelian localities, or were deemedunworthy to receive attention and a formal name, therebyfailing to enter the scientific literature. To examine this possi-bility, we used the bodymassdistribution methodology ofBrown et al. [46], who concluded that the smaller members ofthe dinosaurian fauna of the Upper Cretaceous DinosaurPark Formation of Alberta, Canada, were subjected to preser-vational bias. Our results (see the electronic supplementarymaterial) confirm that Carboniferous reptiles cluster at thesmall end of the size spectrum and, on average, exhibit greaterskeletal completeness than the larger contemporaneous synap-sids. Erpetonyx, the sole Gzhelian reptile represented by a bodyfossil, was dwarfed by its larger synapsid contemporaries.

Finally, another possibility is the strong correlationbetween the increase in synapsid diversity and the origin ofherbivory. The oldest herbivores are known from GzhelianStage, with both synapsids and diadectomorphs evolvingthis novel feeding strategy [42]. The adoption of high-fibre her-bivory by two synapsid lineages may have fostered furtherdiversification among synapsids, and represent a pattern thatwas superimposed over the older vicariant mode promotedby coal-forest fragmentation. Reptiles are exclusively rep-resented by small animals in the Carboniferous, mainlyinsectivorous forms or carnivorous species, which could notreadily prey on the much larger herbivores. In strong contrast,the Synapsida of the latest Carboniferous include several pre-dators of relatively large size that would have been able toprey on diadectomorphs and herbivorous synapsids [42].

The discovery of the first Carboniferous parareptile is criti-cal to our understanding of the early evolution of amniotesbecause it shows that reptiles were undergoing a dramaticdiversification throughout the Carboniferous since the initialappearance of amniotes ca 311 Ma. Erpetonyx arsenaultorum isthe first Carboniferous reptile to be described in nearly twodecades. We anticipate that future field and laboratory studieson Palaeozoic reptiles will help to test hypotheses of preserva-tional bias and vicariance that operated on the earliest fullyterrestrial tetrapods.


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Acknowledgement. We thank the family of M. Arsenault for collectingthe specimen and K. Seymour for procuring the specimen for theROM via the Louise Hawley Stone Charitable Trust. We thankN. Wong Ken, for additional preparation and for the illustrationshown in figure 1, and O. Haddrath (ROM), for assistance with theBayesian analysis.

Funding statement. This research was supported by Discovery Grantsfrom the Natural Sciences and Engineering Research Council(NSERC) of Canada to S.P.M., R.R.R. and D.C.E. The first authorwas also supported by a New Opportunities Fund Award from theCanadian Foundation for Innovation (CFI), and by a grant from theNova Scotia Research and Innovation Trust.
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The oldest parareptile and the early diversification of reptilesIntroductionMaterialSystematic palaeontologyEtymologyMaterialLocality and horizonDiagnosis

DescriptionSkullPostcranial axial skeletonAppendicular skeleton

DiscussionAcknowledgementFunding statementReferences

the oldest parareptile and the early diversification of...

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