Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
rspb.royalsocietypublishing.org
The oldest parareptile and the early
diversification of reptiles
Sean P. Modesto1, Diane M. Scott2, Mark J. MacDougall2, Hans-Dieter Sues3,
David C. Evans4 and Robert R. Reisz2
Research
Cite 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.
1
Department of Biology, Cape Breton University, Sydney, Nova Scotia, Canada B1P 6L2
Department of Biology, University of Toronto at Mississauga, Mississauga, Ontario, Canada L5L 1C6
3
National Museum of Natural History, Smithsonian Institution, MRC 121, PO Box 37012, Washington,
DC 20013-7012, USA
4
Department of Natural History, Royal Ontario Museum, 100 Queen’s Park, Toronto, Ontario, Canada
2
Amniotes, tetrapods that evolved the cleidoic egg and thus independence from
aquatic larval stages, appeared ca 314 Ma during the Coal Age. The rapid
diversification of amniotes and other tetrapods over the course of the Late
Carboniferous period was recently attributed to the fragmentation of coalswamp rainforests ca 307 Ma. However, the amniote fossil record during the
Carboniferous is relatively sparse, with ca 33% of the diversity represented
by single specimens for each species. We describe here a new species of
reptilian amniote that was collected from uppermost Carboniferous rocks of
Prince Edward Island, Canada. Erpetonyx arsenaultorum gen. et sp. nov. is a
new parareptile distinguished by 29 presacral vertebrae and autapomorphies
of the carpus. Phylogenetic analyses of parareptiles reveal E. arsenaultorum as
the closest relative of bolosaurids. Stratigraphic calibration of our results indicates that parareptiles began their evolutionary radiation before the close of the
Carboniferous Period, and that the diversity of end-Carboniferous reptiles is
80% greater than suggested by previous work. Latest Carboniferous reptiles
were still half as diverse as synapsid amniotes, a disparity that may be attributable to preservational biases, to collecting biases, to the origin of herbivory in
tetrapods or any combination of these factors.
1. Introduction
Phylogenetic studies of the past three decades confirm the basal dichotomy of
amniotes into synapsids (i.e. mammals and their fossil relatives) on the one
hand and reptiles (e.g. squamates, crocodiles, birds and their fossil relatives;
a.k.a. ‘sauropsids’) on the other hand [1–3]. Whereas the timing of the origin
and basal amniote dichotomy during the Carboniferous Period is highly debated
[4,5], the oldest unequivocal amniote fossils are known from the Joggins Formation of Nova Scotia, Canada, and are generally regarded to be 313–316
million years (Ma) in age [5].
Among the 10 tetrapod taxa described from the Joggins formation, only two
amniote species are recognized as valid [5,6]. The amniote fossil record continues
to be sparse at succeeding Carboniferous localities, with the exception of the Early
Kasimovian (ca 305 Ma) amniote-rich fauna at Garnett, Kansas [7,8]. Nevertheless, reviews of the alpha taxonomy of Carboniferous amniotes revealed that
the early diversification of synapsids outpaced that of reptiles, with the result
that, by the end of the Carboniferous, synapsid species outnumbered reptiles
approximately 2 to 1 [9,10]. An interesting corollary of the disparity in diversity
between these two great clades of amniotes is that Carboniferous reptiles are
substantially smaller animals than contemporaneous synapsids [9].
A more dramatic dichotomy exists within early Reptilia itself: all Carboniferous species of this group are classified as members of Eureptilia [3], whereas
contemporaneous members of the sister group Parareptilia have yet to be identified. Instead, a single ghost taxon has been reconstructed for Parareptilia,
inferred to extend from the Permian Period down to the origin of amniotes [11].
& 2015 The Author(s) Published by the Royal Society. All rights reserved.
Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
(a)
2
4
mt4
rspb.royalsocietypublishing.org
ca10
ul
as
ca15
h
un
ca5
fi
ti
cr1
sr3
is
fe
u
r
ul
pi
i1
h
pu
ca
ti
fi
23
fe
(b)
dca
5 cm
dca
Figure 1. Erpetonyx arsenaultorum n. gen. et sp., ROM 55402, holotype. (a) Interpretive drawing of skeleton in dorsal aspect. (b) Photograph of skeleton in dorsal
aspect. 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 cervical
vertebrae. (Online version in colour.)
We describe here the first Carboniferous parareptile, based on a
nearly complete, articulated skeleton from Prince Edward
Island, Canada. The early appearance and the phylogenetic
relationships of this new parareptile have dramatic implications for our understanding of the early diversification of
reptiles and amniotes.
2. Material
The study material (figure 1) comprises a nearly complete,
articulated skeleton preserved on a sandstone slab and reposited in the collections of the Royal Ontario Museum, Toronto,
as ROM 55402. The fossil was prepared mechanically by use
of air scribes and pin vices.
The presence of plicidentine and the similarity of the
dorsal vertebrae of ROM 55402 to those described for the
Early Permian parareptile Delorhynchus cifellii [12] strongly
suggested parareptilian affinities for the Prince Edward Island
reptile. For our phylogenetic analysis, we used an augmented
version of the characters and data matrix of Reisz et al. [12].
Although a recent study has resurrected the hypothesis that turtles are parareptiles [13], the problem of turtle origins is beyond
the scope of our study—the relationships of a Late Carboniferous reptile and its implications—so we did not include turtle
taxa (e.g. Odontochelys and/or Proganochelys) in our analysis.
We recoded some taxa for certain characters (see the electronic
supplementary material for data matrix), and performed a heuristic analysis, set to collapse branches with a maximum length of
zero, in PAUP 4.0a134 [14]. We also conducted a Bremer decay
analysis using the heuristic algorithm in PAUP, by relaxing parsimony a single step at a time and generating strict consensus
trees until resolution was completely lost in the ingroup. We
also conducted a bootstrap analysis (1000 replicates).
In addition to the traditional parsimony analysis, a Bayesian
analysis was also conducted on the dataset in order to assess its
Proc. R. Soc. B 282: 20141912
u
16
Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
Parareptilia Olson, 1947 [20].
Bolosauria Kuhn, 1959 [17].
Erpetonyx arsenaultorum n. gen. et sp.
(a) Etymology
The genus name is from classical Greek 1rp1ton, ‘crawler’,
and ony s, ‘claw’. The specific epithet honours the Arsenault
family of Prince County, Prince Edward Island, Canada, who
discovered and collected the specimen.
(b) Material
ROM 55402, holotype, a nearly complete, mostly articulated
skeleton (figure 1a,b).
(c) Locality and horizon
ROM 55402 was collected from a locality at Cape Egmont in
southwestern Prince Edward Island, Canada. The Egmont
Bay Formation crops out along the western part of the island,
and is regarded to be latest Pennsylvanian (Stephanian) in geological 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) Diagnosis
A small, basal parareptile that possesses 29 presacral vertebrae
(viz. five cervicals and 24 dorsals), relatively small carpal
bones (the radiale and the pisiform are ca one-half the size of
the ulnare and the fifth distal carpal, respectively), a femoral
distal end with an epicondylar axis at 458 to the shaft, a
fourth metatarsal with a relatively broad distal end, and
well-developed unguals with prominent flexor tubercles.
4. Description
ROM 55402 (figure 1) comprises a nearly complete articulated
skeleton that is preserved largely in dorsal view, and spanning
ca 20 cm across a sandstone block. The skull, both manus, the
left pes and the right hind limb are disarticulated to varying
(a) Skull
The skull of ROM 55402 is compressed obliquely and was
partly disarticulated prior to burial (figures 1 and 2a). Roughly
half of the skull bones, particularly those of the dermal skull
roof, are weathered, such that either their surficial details or
their outlines, or both, are indistinct. The immediately identifiable dermal bones are the premaxilla, the maxilla, the frontal,
the lacrimal, the prefrontal and the supratemporal. A large, partially moulded surface anteriorly represents the impressions of
the ventral surface of the nasals.
The premaxilla is preserved only as a section through
the left element. Both maxillae are present, but preserved
and/or exposed to varying degrees. The anterior end of the
left maxilla is exposed in medial aspect, and shows that the
maxilla formed the posteroventral corner of the external
naris. The dorsal portion of the right maxilla has been
eroded down to a spindle-shaped alveolar region anteriorly,
exposing the bases of 13 teeth. Two (missing) teeth could
have fit into the space between the last and penultimate
maxillary teeth preserved, such that the maxilla featured at
least 15 tooth positions.
The exposed bases of the anterior-most seven teeth show
the simple infolding that is indicative of the plicidentine that
is seen in Colobomycter pholeter and several other parareptiles
[23,24]. Infolding extends down the length of the largest
teeth (figure 2b). The teeth are slightly recurved, sharply
tipped conical structures that lack cutting edges. There is
neither a caniniform tooth nor caniniform region. The teeth
gradually diminish in both length and basal diameter as
one progresses posteriorly.
The left lacrimal is preserved in articulation with the
left maxilla, and is exposed here mostly in posteromedial
view, where it forms the anterolateral corner of the orbit
(figure 2a). The facial portion extends anteriorly, but is
mostly obscured by the nasal impression; it is not clear
how far anteriorly the lacrimal extended.
Both frontals are preserved as a motley of heavily
weathered bone and impression. Each frontal is least six
times longer than it is wide. The middle third of the lateral
margin is faintly concave and represents the dorsal margin
of 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 a
tongue-shaped facial process.
An irregularly shaped dermal bone, with what appears to
be a small posterior ‘hornlet’, is identified here as the right
supratemporal (figure 2a). Whereas the medial and posterior
margins are well preserved, the anterior and lateral margins
of this bone are heavily weathered (yielding an unnaturally
straight lateral or anterolateral margin). The well-preserved
posterior margin consists of a faintly sinusoidal free edge
from which projects a small, narrow, tongue-like projection
3
Proc. R. Soc. B 282: 20141912
3. Systematic palaeontology
degrees. Much of the skull roof, dorsal portions of most of
the presacral vertebrae and numerous trunk ribs have been
damaged by weathering. The tail, partly disarticulated and
missing an estimated 15 caudal vertebrae, is otherwise well
preserved. The well-ossified nature of the autopodia and the
closure of neurocentral sutures in the sacral and presacral
vertebrae indicate that the skeleton is that of an adult animal.
rspb.royalsocietypublishing.org
robusticity to different methods of phylogeny estimation [15].
The Bayesian analysis of the morphological data matrix was conducted using MRBAYES v. 3.1.2 [16], and employed the Mk model
(datatype ¼ standard) with the addition of a gamma shape parameter (rates ¼ variable) to allow for rates of change to vary
across characters, as recommended by Müller & Reisz [3]. The
analysis was run for 3 000 000 generations (Markov Chain
Monte Carlo (MCMC): four chains, two simultaneous independent runs), with a tree sampled every 100 generations, with the
first 10% of the sampled trees being discarded as the ‘burn-in’.
The majority-rule consensus tree with nodal clade credibility
values is presented in the electronic supplementary material.
The results of our analyses indicate that the new Prince
Edward Island reptile is closely related to bolosaurid parareptiles. Accordingly, we resurrect the name Bolosauria,
which was erected as an ordinal name by Kuhn [17] to contain the family Bolosauridae Cope, 1878, and define it as a
branch-based group: Bolosaurus striatus Cope, 1878 [18] and
all species related more closely to it than to Procolophon
trigoniceps Owen, 1876 [19].
Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
4
5 mm
(b)
1 cm
Eureptilia
(c)
Mesosauridae
Millerosauria
Australothyris
Lanthanosuchia
C
A
D
B
Microleter
E
Nyctiphruretidae
F
Pareiasauromorpha
G
Procolophonidae
Bolosauridae
Bolosauria
Erpetonyx
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 ¼ 557, consistency index (CI) ¼ 0.3429, CI excluding informative characters ¼ 0.3405, retention index ¼ 0.6355,
rescaled CI ¼ 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; clade
D (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 next
vertebra (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 identify
cervical vertebrae. (Online version in colour.)
of bone, slightly broader transversely than anteroposteriorly
long, with a saddle-shaped articulating surface for the articular. The dorsal lamella is a trapezoidal plate that is roughly as
tall as it is broad. In its general morphology, the quadrate of
ROM 55402 resembles that of Belebey vegrandis [26].
Most braincase elements are present, but overlying dermal
bone fragments preclude full descriptions (figure 2a). The parabasisphenoid is identifiable because of its prominent cultriform
process, which is present as a slender trough formed of thin,
low plates of bone. Although narrowing anteriorly, its
anterior-most tip is missing; what is present indicates a long
process, which is roughly equal in length to the body of the
braincase, and probably extended the entire length of the interpterygoid vacuity. The main body of the parabasisphenoid is
poorly preserved, bearing a weathered right clinoideus process
and a partly exposed, poorly ossified retractor pit.
What is exposed of the prootics largely conforms with the
general morphology of this element in other early reptiles. An
exception is a ventral concavity in the anterior end of the
right prootic, which possibly formed the dorsal half of a foramen that was completed ventrally by the parabasisphenoid,
and may represent the opening for the hyomandibular
branch of the facial nerve [27].
Immediately posterior to the prootics are the opisthotics,
with their deep, U-shaped excavations of unfinished bone
representing the posterior portions of the membranous labyrinths. A stubby paroccipital process extends laterally from
the main body of the right opisthotic. Between the opisthotics
Proc. R. Soc. B 282: 20141912
Parareptilia
or ‘hornlet’. Where the dorsal surface is well preserved, it is
smooth and featureless.
Various fragments of relatively thick bone that are clearly
dermal roofing elements, but are not informative morphologically, are tentatively identified as the parietal, the
postfrontal, the postorbital, the squamosal, the postparietal
and the tabular bones.
The palatal bones are not well exposed. The anterior ends
of the slender, paired vomers are preserved anteriorly in close
association with the premaxilla. The left palatine is preserved
in 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 denticulated
sheet of bone positioned posteriorly that, judging from the
relative thinness of the bone and its distinctive curvature,
probably represents parts of the base of the quadrate ramus
and the pterygoid transverse process. The palatal denticles
are tiny, simple cones. As in Feeserpeton and many other parareptiles [25], the denticles extend onto the quadrate ramus of
the pterygoid. There are fragments of thin, smoothly finished
bone elsewhere that may represent fragments of palatal
elements, but these are uninformative.
The dorsal columella of an epipterygoid projects from
beneath fragments of parietal bone. A remarkably robust
right quadrate is preserved in its expected position, in the
posterolateral corner of the skull, with the condyle directed
posteriorly and the anterolateral surface of the dorsal lamella
facing upwards. The quadrate condyle is a knuckle-like block
rspb.royalsocietypublishing.org
(a)
Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
The backbone is preserved as a sinusoidal, largely articulated
series of 65 vertebrae, plus 10 disarticulated caudal vertebrae
(figure 1). We estimate that an ‘arc’ between the two articulated caudal series would accommodate about 25 vertebrae,
suggesting that—minus the 10 disarticulated caudals—
about 15 caudal vertebrae from the middle to distal part of
the tail are not preserved. Nearly all neural spines have
been weathered down to low stumps.
There are 29 presacral vertebrae. Among non-mesosaurian
parareptiles, presacral vertebrae number 26 or fewer [28–30].
As is typical for early amniotes, there is no morphological distinction between the last cervical vertebra and the first dorsal
vertebra, but rib morphology suggests that there are five cervical vertebrae. A proatlas, portions of the atlas and the axis are
present, but not morphologically informative. Beginning with
the third cervical vertebra, the presacral neural arches exhibit
a distinctive hourglass-shaped outline in dorsal aspect. The
presacral neural arches are relatively narrow; the breadth
across the postzygapophyses of the fifth cervical is ca 62% of
the total anteroposterior length of the arch.
Twenty-four vertebrae form the dorsal series (figure 1). The
neural arches gradually increase in both breadth and length
posteriorly down the column, such that the 16th dorsal (twothirds of the way down the dorsal series) is approximately
25% broader and longer than an anterior dorsal vertebra. All
dorsal neural arches feature the conspicuous hourglass-shaped
organization seen in the posterior cervicals. The hourglass
shape seen in dorsal aspect is enhanced by oblique, paired excavations in the dorsolateral surfaces of the arch, positioned
between the transverse process and a ridge extending from the
posterior part of the prezygapophysis to the midpoint of
the dorsal midline of the arch. Because of the tight articulation
of the vertebrae, none of the zygopophyseal facets is fully visible,
but they appear to be subcircular in outline, and inclined very
(c) Appendicular skeleton
The appendicular bones are preserved in close association
with those of the axial skeleton (figure 1). However, except
for the left ilium, they are mostly overlain either by the vertebral column, or by neighbouring elements. Most elements
of the pectoral girdle are present, but they are not well
exposed. What is visible of each suggests a morphology
very similar to that of other early terrestrial reptiles [28,33].
Elements of the pectoral limb are well preserved and
exposed for the most part. The humerus is roughly the same
relative size and morphology as this element in other early
reptiles. However, there is little development of a trochlea
and a capitulum for articulation with the ulna and the radius,
respectively, suggesting more freedom of movement at
the elbow compared with early sprawling reptiles, such as
Captorhinus [34]. The radius and the ulna are just under 80%
of the length of the humerus. The olecranon process of the
ulna is not well developed, being little more than a nubbin.
Neither manus is complete and both are disarticulated to
varying degrees. The right carpus is preserved fully articulated as a mosaic of irregular tile-like polygons. The radiale,
the pisiform, and the first and fifth distal carpals are unusually small for an early reptile. The elements distal to the
carpus are not articulated well enough to provide a good
understanding of the structure of the digits in either manus.
Apart from the right fifth metatarsal, none of the metacarpals
remains in articulation with its respective distal carpal. Some
12 non-ungual phalanges and a single unequivocal ungual
(less than 40% of the 34 phalanges that are expected, assuming a plesiomorphic phalangeal formula of 2–3 –4–5–3 [2])
are all that remain of the manual digits. The non-terminal
5
Proc. R. Soc. B 282: 20141912
(b) Postcranial axial skeleton
weakly from the horizontal—those of the prezygapophyses
facing slightly medially, perhaps as much as 108, whereas
those of the postzygapophyses tilt slightly laterally in
complementary fashion.
There are three sacral vertebrae. As is typical of early
terrestrial tetrapods [31,32], the first sacral has a neural arch
morphology that is transitional to that seen in the preceding dorsal vertebra and the succeeding caudals in that the
prezygapophyses are relatively broad, matching the broad
postzygapophyses of the dorsal vertebra, but with the postzygapophyses forming a distinctly narrow posterior end to the
first sacral neural arch, commensurate with the relatively
narrow arches of the anterior-most caudals. There are three
pairs of sacral ribs. The first and second ribs are flared laterally
and similar in size, but the third sacral rib is a finger-like
projection that had only a touch contact with the iliac blade.
Forty-three caudal vertebrae are preserved (figure 1). The
base of the tail forms a tightly articulated series up to, and
including, caudal 20, and there is an articulated series of 13
distal caudals preserved adjacent to presacrals 19– 25. If the
latter series is preserved in normal position with respect to
the proximal articulated series (i.e. the base of the tail), we
estimate that approximately 25 caudal vertebrae would arc
along this ‘missing’ part of the tail. Ten caudals of intermediate size, including several single disarticulated caudals, two
pairs of caudals and a loose articulated series of three caudals,
are scattered loosely in this area, indicating that about 15
caudal vertebrae are not preserved. Altogether, at least 58
caudal vertebrae were present, a number closely comparable
to that described for other early reptiles [29,32,33].
rspb.royalsocietypublishing.org
lies the broad, plate-like supraoccipital, identifiable by
the embayment in its ventral margin forming the dorsal
portion of the foramen magnum. Only the ventral portion
of the left exoccipital is preserved, as a slightly curved,
hourglass-shaped bone.
The mandible is represented by the dentary, splenial and
articular of the right ramus and the angular, the surangular
and the prearticular of the left ramus (figure 2a). The dentary
is worn down by weathering and is identifiable by its position and its outline, but it is not preserved well enough for
description. Closely appressed to the dentary is the better
preserved splenial; it has a smooth lingual surface and does
not contribute to the mandibular symphysis. The angular
and the surangular are low, elongate and slightly curved
bones; the dorsal margin of the latter bone is a low, weakly
convex edge. The prearticular is a slender, slightly curved
element with a dorsoventrally expanded posterior end. The
articular is preserved upside-down with respect to the skull
and rotated slightly more than 908 anticlockwise, such that
both the posterior-most end of the ventral edge of the mandible and the pterygoideus process are exposed in ventral
view. It is an irregularly shaped bone with a well-developed
retroarticular process, the ventral surface of which is
damaged. The insertion surface for the pterygoideus musculature is visible as a slightly sigmoidal depression between
the planed-down ventral extremities of the articular.
Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
their respective penultimate phalanges, the pedal unguals are
ca 33% longer than the penultimate pedal phalanges.
5. Discussion
Proc. R. Soc. B 282: 20141912
Our parsimony analysis (figure 2c) positions Erpetonyx
arsenaultorum as the sister taxon of Bolosauridae, which is represented 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 phylogenetic
analysis and the electronic supplementary material for list of
characters and data matrix). Support for Bolosauria and Bolosauridae is moderate, with Bremer support values of 3 and 4,
respectively; all clades except Pareiasauridae collapse with the
addition of six extra steps. The Bayesian analysis also recovered Bolosauria, but the overall phylogeny differs in the
transposition of Bolosauria and Australothyris, and in the placement of Mesosauridae at the base of Eureptilia (see the
electronic supplementary material).
A bolosaurian identification for Erpetonyx arsenaultorum,
together with its latest Carboniferous age, has important
implications for early parareptile diversification and reptilian
evolution. Prior to the discovery of ROM 55402, the oldest
parareptilian fossils were known from the Asselian Stage of
the Permian Period of New Mexico, USA [39], and phylogenetic reconstructions required a long ghost taxon for
Parareptilia to extend from the Asselian (ca 295 Ma) down to
the latest Moscovian Stage (ca 314 Ma) of the Carboniferous
period (figure 3).
The inclusion of Erpetonyx arsenaultorum in a phylogenetic
analysis of Parareptilia results in bolosaurs being positioned
closer to the base of the parareptilian tree (as the basal-most
members of Procolophonomorpha; sensu Modesto et al. [40])
and the Richards Spur taxon Microleter mckinsieorum moving
deeper into the tree with respect to previous phylogenetic
studies of Parareptilia [12,14,25,40]. The sister-group relationship between Erpetonyx arsenaultorum and Bolosauridae
necessitates the extension of four parareptilian ghost lineages
or ghost taxa (for Mesosauridae, Millerosauria, Bolosauridae
and the clade of Australothyris smithi and Ankyramorpha)
from the Early Permian down into the Gzhelian Stage of the Carboniferous Period. This results in a fivefold increase (from one to
five lineages) for the diversity of parareptiles at the end of the
Carboniferous, and an 80% increase (from five to nine lineages)
for the diversity of reptiles at the end of the Carboniferous (see
electronic supplementary material, figure S4).
Our results are consonant with previous work by Reisz
[10], who reported that Carboniferous species of reptiles
were outnumbered ca 2 to 1 by contemporaneous synapsids.
Owing to lack of phylogenetic resolution among Palaeozoic
reptiles at the time, Reisz [10] relied on comparisons of
group diversity (sensu Norell [41]), i.e. direct counts of taxic
occurrences. Our phylogenetic results, when calibrated stratigraphically and compared with stratigraphic calibrations of
eureptilian [3] and synapsid [42,43] trees, confirm that reptilian diversification during the Carboniferous was outpaced
by that of synapsids, but only during the Gzhelian Stage
(303.4–299.0 Ma), with synapsids numbering 17 species per
lineages versus reptiles numbering only 9.
Recently, Sahney et al. [44] inferred that the fragmentation
and collapse of coal-swamp forests ca 307 Ma promoted
diversification of post-Moscovian (latest Carboniferous)
6
rspb.royalsocietypublishing.org
phalanges are dorsoventrally compressed, gently waisted
bow ties of bone. The ungual is a distinctly claw-like element
which has a relatively broad, elliptical articulating head, a
prominent flexor tubercle (roughly the same relative size as
in the synapsid Dimetrodon [35]), and an acute tip.
All of the pelvic girdle elements are present in varying
degrees of exposure and completeness, and are closely associated with each other and with neighbouring bones (figure 1).
Only the left ilium is fully exposed (in medial aspect). It exhibits a relatively deep, posterodorsally directed iliac blade;
there is no anterodorsal process. The pubes are largely
obscured by overlying elements, but what is visible indicates
that these bones are relatively flat and very short, subrectangular elements. The ischia are slightly better exposed than the
pubes, revealing that each ischium is a flat tongue of bone
that closely resembles the ischia of other early reptiles
[36,37]. The ischium is primitive in being substantially
longer than the pubis.
The femur closely resembles that of other early reptiles,
except that the distal end features a strong, ca 458 angle
formed by the condyles with respect to the long axis of
the bone (this angle ranges from 10 to 308 in most early reptiles
[35–38]). The tibia and the fibula are slender, slightly bowed
rods of bone that are ca 75% the length of the femur. The
pedes are almost entirely disarticulated; neither tarsus is
intact, and only the astragalus on the left side and the calcaneum on the right side remain of the proximal tarsals. The
astragalus is a rectangular (or transversely compressed,
L-shaped) plate that is nearly twice as long as it is broad. The
calcaneum is a D-shaped plate of bone, thickest along its
straight, medial edge, and it thins gradually laterally. Five
robust, polygonal distal tarsals are preserved. Three on the
left side are semi-articulated; two smaller, irregular bones
appear to be (because of their associations with distal tarsal 4
and the metatarsals) distal tarsals 3 and 5. The metatarsals
are gently to moderately waisted rods of bone. The longest is
interpreted here to be the fourth metatarsal; it is about 66%
of the total length of the fibula. Apart from the relatively
broad distal end of the fourth metatarsal, the morphology of
the metatarsus is consonant with what has been described
and illustrated for other early, terrestrial reptiles. A total of
21 pedal phalanges, including four unguals, are preserved.
The left pes, with 12 non-terminal phalanges, preserves
the majority of these. The non-terminal phalanges have
hourglass-shaped outlines in dorsal aspect. Whereas the
non-terminal toe bones are dorsoventrally compressed, and
thus most of them are preserved in dorsal or ventral aspect,
the unguals are mediolaterally compressed, and all are preserved on their sides. The ungual of the fourth digit is
preserved on its lateral surface, and has a distinctly clawshaped profile, with a remarkably robust, polygonal proximal
end giving rise to a dorsoventrally narrow, weakly curving
distal tip, accentuated by the slightly more convex dorsal
margin of the entire element. A shallow groove runs the
length of the medial surface of the claw-like tip. The ventral surface of the proximal portion bears a broadly rounded flexor
tubercle that, commensurate with the position of the end of
the longest pedal digit, is the largest among the preserved
unguals. An equally well-preserved ungual lies close by and presumably belongs to a more medial digit. It is slightly longer, and
has a more acute profile as a result of having a less robust proximal portion and smaller flexor tubercle. The pedal unguals are
the longest phalanges present, and if correctly associated with
Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
323.2
Permian
252.2
272.3 Guadalupian 259.8 Lopingian global standard series
Kungur Road Word Capit Wuchia Ch global standard stages
Synapsida
Mesosauridae
Millerosauria
Parareptilia
Erpetonyx
Bolosauridae
Australothyris
Lanthanosuchia
Reptilia
Microleter
Nyctiphruretidae
Procolophonia
Eureptilia
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 ghost
lineages. Timescale from International Commission on Stratigraphy [22].
tetrapods, including the amniotes. Sahney et al. [44] inferred a
vicariant mode of diversification for Coal Age tetrapods
resulting from coal-forest fragmentation. If this is the case,
we should expect to see similar diversity in closely related
groups. Because sister taxa are the same age [41], a comparison of the numbers of species in sister taxa is an appropriate
test [45]. If reptiles and synapsids (sister taxa) responded
vicariantly to coal-forest fragmentation, they should show
similar taxic diversity, particularly because both reptiles
and synapsids are found at the same localities (indicating
that both groups were equally widespread and thus susceptible to fragmentation). Our examination of Carboniferous
amniote phylogenetic diversity provides a more complete
and detailed timeline of diversification in Carboniferous
taxa than provided by Sahney et al. [44]. For instance, there
is evidence for a single species each for synapsids and reptiles
during the Moscovian Stage (311.7–307.2 Ma), and for the
late Kasimovian (ca 305 Ma)—a time when coal-swamp forests were reduced to ‘tiny wet spots’ [44]—our study
indicates that reptiles and synapsids were, indeed, equally
diverse (8 reptilian species versus 10 synapsids). Accordingly,
late Kasimovian amniote diversity patterns are consonant
with the hypothesis of Sahney et al. [44]. Amniote diversity
patterns change during the succeeding Gzhelian Stage, however, and by the end of the Carboniferous—and more than
4.5 Ma after coal forests were little more than isolated refugia—synapsids outnumbered reptiles ca 2 to 1 (17 synapsid
species versus 9 reptiles).
If fragmentation of the Carboniferous coal swamps drove
the diversification of amniotes and other tetrapods during
the Kasimovian Stage, what might account for the disparity
seen between synapsid and reptilian diversity by the end of
the Gzhelian Stage? Our results do not reject the possibility
that coal-forest fragmentation drove amniote diversification
during the Gzhelian Stage [44]. However, preservational bias
may be responsible for the low diversity of Gzhelian reptiles,
for such diversity rests entirely upon Erpetonyx as the sole
datum point for Reptilia in this 4.8-Myr-long stage. Previous
workers [43] had regarded Hamilton Quarry, which preserves
the (previous) youngest Carboniferous reptile (Spinoaequalis
schultzei) as 303 Ma, or Gzhelian in age. As recognized by
Sahney et al. [44], this locality is actually late Kasimovian in
age (¼early Virgilian Age of North American Carboniferous
system). Thus, the greater diversity of Gzhelian synapsids is
partly a reflection of the astonishingly poor fossil record of reptiles during this stage. Gzhelian amniotes may have been
subject to a strong collecting bias, in which the larger synapsid
fragmentary remains were more easily discovered and deemed
sufficiently significant to be collected and described, whereas
very small, fragmentary reptilian remains either were much
more difficult to find at Gzhelian localities, or were deemed
unworthy to receive attention and a formal name, thereby
failing to enter the scientific literature. To examine this possibility, we used the body–mass–distribution methodology of
Brown et al. [46], who concluded that the smaller members of
the dinosaurian fauna of the Upper Cretaceous Dinosaur
Park Formation of Alberta, Canada, were subjected to preservational bias. Our results (see the electronic supplementary
material) confirm that Carboniferous reptiles cluster at the
small end of the size spectrum and, on average, exhibit greater
skeletal completeness than the larger contemporaneous synapsids. Erpetonyx, the sole Gzhelian reptile represented by a body
fossil, was dwarfed by its larger synapsid contemporaries.
Finally, another possibility is the strong correlation
between the increase in synapsid diversity and the origin of
herbivory. The oldest herbivores are known from Gzhelian
Stage, with both synapsids and diadectomorphs evolving
this novel feeding strategy [42]. The adoption of high-fibre herbivory by two synapsid lineages may have fostered further
diversification among synapsids, and represent a pattern that
was superimposed over the older vicariant mode promoted
by coal-forest fragmentation. Reptiles are exclusively represented by small animals in the Carboniferous, mainly
insectivorous forms or carnivorous species, which could not
readily prey on the much larger herbivores. In strong contrast,
the Synapsida of the latest Carboniferous include several predators of relatively large size that would have been able to
prey on diadectomorphs and herbivorous synapsids [42].
The discovery of the first Carboniferous parareptile is critical to our understanding of the early evolution of amniotes
because it shows that reptiles were undergoing a dramatic
diversification throughout the Carboniferous since the initial
appearance of amniotes ca 311 Ma. Erpetonyx arsenaultorum is
the first Carboniferous reptile to be described in nearly two
decades. We anticipate that future field and laboratory studies
on Palaeozoic reptiles will help to test hypotheses of preservational bias and vicariance that operated on the earliest fully
terrestrial tetrapods.
Proc. R. Soc. B 282: 20141912
Ankyramorpha
7
rspb.royalsocietypublishing.org
298.9
Carboniferous
Cisuralian
Pennsylvanian
Bashkir Moscov Kas Gzhel Assel Sakmar Artinsk
Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
Funding statement. This research was supported by Discovery Grants
the specimen and K. Seymour for procuring the specimen for the
ROM via the Louise Hawley Stone Charitable Trust. We thank
N. Wong Ken, for additional preparation and for the illustration
shown in figure 1, and O. Haddrath (ROM), for assistance with the
Bayesian analysis.
from the Natural Sciences and Engineering Research Council
(NSERC) of Canada to S.P.M., R.R.R. and D.C.E. The first author
was also supported by a New Opportunities Fund Award from the
Canadian Foundation for Innovation (CFI), and by a grant from the
Nova Scotia Research and Innovation Trust.
References
1.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14. Swofford DL. 2014 Phylogenetic analysis using
parsimony (and other methods). Sunderland, MA:
Sinauer Associates.
15. Brooks DR et al. 2007 Quantitative phylogenetic
analysis in the 21st century. Revista Mexicana de
Biodiversidad 78, 225 –252.
16. Ronquist F, Huelsenbeck JP. 2003 MrBayes 3:
Bayesian phylogenetic inference under mixed
models. Bioinformatics 19, 1572 –1574. (doi:10.
1093/bioinformatics/btg180)
17. Kuhn O. 1959 Die Ordnungen der fossilen
‘Amphibien’ und ‘Reptilien’. N. Jahr. Geol. Palaont.,
Monat. 1959, 337–347.
18. Cope ED. 1878 Descriptions of extinct Batrachia and
Reptilia from the Permian formation of Texas. Proc.
Am. Phil. Soc. 17, 505 –530.
19. Owen R. 1876 Catalogue of the fossil Reptilia of
South Africa. London, UK: British Museum.
20. Olson EC. 1947 The family Diadectidae and its
bearing on the classification of reptiles. Fieldiana
Geol. 11, 1 –53.
21. van de Poll HW. 1998 Lithostratigraphy of the
Prince Edward Island redbeds. Atl. Geol. 25, 23 –35.
22. International Commission on Stratigraphy. 2014
International chronostratigraphic chart. See www.
stratigraphy.org (accessed 13 July 2014).
23. Modesto SP, Reisz RR. 2008 New material of
Colobomycter pholeter, a small parareptile from the
Lower Permian of Oklahoma. J. Vert. Paleontol. 28,
677 –684. (doi:10.1671/0272-4634(2008)28[677:
NMOCPA]2.0.CO;2)
24. MacDougall MJ, LeBlanc ARH, Reisz RR. 2014
Plicidentine in the Early Permian parareptile
Colobomycter pholeter, and its phylogenetic and
functional significance among coeval members of
the clade. PLoS ONE 9, e96559. (doi:10.1371/
journal.pone.0096559)
25. MacDougall MJ, Reisz RR. 2012 A new parareptile
(Parareptilia, Lanthanosuchoidea) from the Early
Permian of Oklahoma. J. Vert. Paleontol.
32, 1018–1026. (doi:10.1080/02724634.2012.
679757)
26. Reisz RR, Müller J, Tsuji LA, Scott D. 2007 The
cranial osteology of Belebey vegrandis (Parareptilia:
Bolosauridae), from the Middle Permian of Russia,
and its bearing on reptilian evolution. Zool. J. Linn.
Soc. 151, 191– 214. (doi:10.1111/j.1096-3642.2007.
00312.x)
27. Langston Jr W, Reisz RR. 1981 Aerosaurus wellesi,
new species, a varanopseid mammal-like reptile
(Synapsida: Pelycosauria) from the Lower Permian
of New Mexico. J. Vert. Paleontol. 1, 73– 96.
(doi:10.1080/02724634.1981.10011881)
28. Gow CE. 1972 The osteology and relationships of
the Millerettidae (Reptilia: Cotylosauria). J. Zool.
Lond. 167, 219 –264. (doi:10.1111/j.1469-7998.
1972.tb01731.x)
29. Berman DS, Reisz RR, Scott D, Henrici AC, Sumida
SS, Martens T. 2001 Early Permian bipedal reptile.
Science 290, 969–972. (doi:10.1126/science.290.
5493.969)
30. Reisz RR, Scott D. 2002 Owenetta kitchingorum, sp.
nov., a small parareptile (Procolophonia:
Owenettidae) from the Lower Triassic of South
Africa. J. Vert. Paleontol. 22, 244 –256. (doi:10.
1671/0272-4634(2002)022[0244:OKSNAS]2.0.CO;2)
31. Watson DMS. 1914 Procolophon trigoniceps, a
cotylosaurian reptile from South Africa. Proc. Zool.
Soc. 84, 735 –748. (doi:10.1111/j.1469-7998.1914.
tb07060.x)
32. Heaton MJ, Reisz RR. 1980 A skeletal reconstruction
of the Early Permian captorhinid reptile
Eocaptorhinus laticeps (Williston). J. Paleontol. 54,
136–143.
33. Modesto SP. 2010 The postcranial skeleton of the
aquatic parareptile Mesosaurus tenuidens from the
Gondwanan Permian. J. Vert. Paleontol. 30,
1378– 1395. (doi:10.1080/02724634.2010.501443)
34. Holmes R. 1977 The osteology and musculature
of the pectoral limb of small captorhinids.
J. Morph. 152, 101– 140. (doi:10.1002/jmor.
1051520107)
35. Maddin HC, Reisz RR. 2007 The morphology of the
terminal phalanges in Permo-Carboniferous
synapsids: an evolutionary perspective. Can. J. Earth
Sci. 44, 267–274. (doi:10.1139/e06-076)
36. Carroll RL. 1969 A Middle Pennsylvanian
captorhinomorph, and the interrelationships of
primitive reptiles. J. Paleontol. 43, 151–170.
37. Holmes RB. 2003 The hind limb of Captorhinus aguti
and the step cycle of basal amniotes. Can. J. Earth Sci.
40, 515–526. (doi:10.1139/e02-039)
38. deBraga M. 2003 The postcranial skeleton,
phylogenetic position, and probable lifestyle of the
Early Triassic reptile Procolophon trigoniceps.
Can. J. Earth Sci. 40, 527–556. (doi:10.1139/e02-082)
39. Lucas SG, Berman DS, Henrici AC, Hunt AP. 2005
Bolosaurus from the Lower Permian at Arroyo de
Agua, New Mexico and its biostratigraphic
significance. In The Permian of central New Mexico
(eds SG Lucas, M Morales), pp. 125 –127. Bull. New
Mexico Mus. Nat. Hist. Sci. 31.
40. Modesto SP, Scott DM, Reisz RR. 2009 A new
parareptile with temporal fenestration from the
Middle Permian of South Africa. Can. J. Earth Sci.
46, 9 –20. (doi:10.1139/E09-001)
Proc. R. Soc. B 282: 20141912
2.
Gauthier J, Kluge AG, Rowe T. 1988 The early
evolution of the Amniota. In The phylogeny and
classification of the tetrapods (ed. MJ Benton), pp.
103–155. Oxford, UK: Clarendon Press.
Laurin M, Reisz RR. 1995 A reevaluation of early
amniote phylogeny. Zool. J. Linn. Soc. 113, 165–223.
(doi:10.1111/j.1096-3642.1995.tb00932.x)
Müller J, Reisz RR. 2006 The phylogeny of early
eureptiles: comparing parsimony and Bayesian
approaches in the investigation of a basal fossil
clade. Syst. Biol. 55, 503– 511. (doi:10.1080/
10635150600755396)
Reisz RR, Müller J. 2004 Molecular timescales and
the fossil record: a paleontological perspective.
Trends Genet. 20, 237– 241. (doi:10.1016/j.tig.2004.
03.007)
Müller J, Reisz RR. 2005 Four well-constrained
calibration points from the vertebrate fossil record
for molecular clock estimates. Bioessays 27,
1069–1075. (doi:10.1002/bies.20286)
Reisz RR, Modesto SP. 1996 Archerpeton anthracos
from the Joggins Formation of Nova Scotia: a
microsaur, not a reptile. Can. J. Earth Sci. 33,
703–709. (doi:10.1139/e96-053)
Reisz RR. 1981 A diapsid reptile from the
Pennsylvanian of Kansas. Spec. Publ. Mus. Nat. Hist.
Univ. Kansas 7, 1 –74.
Reisz RR, Heaton MJ, Pynn BR. 1982 Vertebrate
fauna of Late Pennsylvanian Rock Lake shale near
Garnett, Kansas: Pelycosauria. J. Paleontology 56,
741–750.
Reisz RR. 1972 Pelycosaurian reptiles from the
Middle Pennsylvanian of North America. Bull. Mus.
Comp. Zool. 144, 27 –62.
Reisz RR. 2003 Cotylosaur phylogeny and the initial
diversification of amniotes. J. Vert. Paleontol. 23(3
Suppl.), 1 –24. (doi:10.1080/02724634.2003.
10010538)
Tsuji LA, Müller J, Reisz RR. 2010 Microleter
mckinzieorum gen. et sp. nov. from the Lower
Permian of Oklahoma: the basalmost parareptile
from Laurasia. J. Syst. Paleont. 8, 245– 255. (doi:10.
1080/14772010903461099)
Reisz RR, MacDougall MJ, Modesto SP. 2014 A new
species of the parareptile genus Delorhynchus,
based on articulated skeletal remains from Richards
Spur, lower Permian of Oklahoma. J. Vert. Paleontol.
34, 1033 –1043. (doi:10.1080/02724634.2013.
829844)
Lyson TR, Bever GS, Bhullar B-AS, Joyce WG,
Gauthier JA. 2010 Transitional fossils and the origin
of turtles. Biol. Lett. 6, 830 –833. (doi:10.1098/rsbl.
2010.0371)
8
rspb.royalsocietypublishing.org
Acknowledgement. We thank the family of M. Arsenault for collecting
Downloaded from http://rspb.royalsocietypublishing.org/ on June 18, 2017
43. Reisz RR, Fröbisch J. 2014 The oldest caseid
synapsid from the late Pennsylvanian of Kansas, and
the evolution of herbivory in terrestrial vertebrates.
PLoS ONE 9, e94518. (doi:10.1371/journal.pone.
0094518)
44. Sahney S, Benton MJ, Falcon-Lang HJ. 2010
Rainforest collapse triggered Carboniferous tetrapod
diversification in Euramerica. Geology 38,
1079 –1082. (doi:10.1130/G31182.1)
45. Brooks DR, McLennan DA. 2002 The nature of
diversity: an evolutionary voyage of discovery.
Chicago, IL: Chicago University Press.
46. Brown CM, Evans DC, Campione NE, O’Brien LJ.
2012 Evidence for taphonomic size bias in the
Dinosaur Park Formation (Campanian, Alberta), a
model Mesozoic terrestrial alluvial-paralic system.
Palaeogeogr. Palaeoclimatol. Palaeoecol. 372,
108–122. (doi:10.1016/j.palaeo.2012.06.027)
9
rspb.royalsocietypublishing.org
41. Norell MA. 1992 Taxic origin and temporal diversity:
the effect of phylogeny. In Extinction and phylogeny
(eds MJ Novacek, QD Wheeler), pp. 89 –118.
New York, NY: Columbia University Press.
42. Fröbisch J, Schoch RR, Müller J, Schindler T,
Schweiss D. 2011 A new basal sphenacodontid
synapsid from the Late Carboniferous of the
Saar-Nahe Basin, Germany. Acta Palaeont. Pol. 56,
113–120. (doi:10.4202/app.2010.0039)
Proc. R. Soc. B 282: 20141912