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B RE VI O R A 



M 



mseuinri 



mi p <a r a 1 1 v 



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©logy 



US ISSN 0006-9698 



Cambridge, Mass. 



19 October 2009 



Number 518 



AN ARCHOSAUR-LIKE LATEROSPHENOID IN EARLY TURTLES 
(REPTILIA: PANTESTUDINES) 

Bhart-Anjan S. Bhullar 1 and Gabe S. Bever 2 

Abstract. Turtles are placed with increasing consistency by molecular phylogenetic studies within Diapsida as 
sister to Archosauria, but published gross morphology-based phylogenetic analyses do not recover this position. 
Here, we present a previously unrecognized unique morphological character offering support for this hypothesis: the 
presence in stem turtles of a laterosphenoid ossification identical to that in Archosauriformes. The laterosphenoid is a 
tripartite chondrocranial ossification, consisting of an ossified pila antotica, pila metoptica, and taenia medialis + 
planum supraseptale. It forms the anterior border of the exit for the trigeminal nerve (V) and partially encloses the 
exits for cranial nerves III, IV, and II. This ossification is unique to turtles and Archosauriformes within Vertebrata. 
It has been mistakenly dismissed as anatomically dissimilar in these two groups in the past, so we provide a complete 
description and detailed analysis of correspondence between turtles and Archosauriformes in each of its 
embryologically distinct components. A preliminary phylogenetic analysis suggests other potential synapomorphies 
of turtles and archosaurs, including a row or rows of mid-dorsal dermal ossifications. 

Key words: Archosauria; Archosauriformes; Diapsida; turtle origins; chondrocranium; Proganochelys; 
Kayentachelys; fossil; braincase; interorbital ossification; Testudines 



Turtles (Pantestudines; Joyce et al., 2004) 
have traditionally been classified as "ana- 
psid" reptiles owing to their lack of the 
lateral and dorsal fenestration of the skull 



1 Department of Organismic and Evolutionary Biology, 
Harvard University, Biolabs room 4110, 16 Divinity 
Avenue, Cambridge, Massachusetts 02138, U.S.A.; e- 
mail: bhartanjan.bhullar@gmail.com 

2 Division of Paleontology, American Museum of 
Natural History, Central Park West at 79th Street, 
New York, New York 10024, U.S.A. 



that is ancestral for diapsid reptiles, includ- 
ing tuatara, lizards, crocodiles, and birds 
(Gauthier et al., 1988, and references there- 
in). Early gross morphology-based phyloge- 
netic analyses suggested that turtles are the 
sister taxon to Diapsida and thus one of the 
two branches of the initial reptilian diver- 
gence (Gauthier et al., 1988). Most subse- 
quent morphological analyses have either 
supported this position (Brochu, 2001; 
Laurin and Reisz, 1995; Lee, 1997) or have 



® The President and Fellows of Harvard College 2009. 



BREVIORA 



No. 518 



placed turtles close to the marine Euryapsida 
along the stem of the lizard/tuatara clade 
Lepidosauria (Li et al., 2008; Rieppel and 
Reisz, 1999), thus suggesting that they are 
highly modified diapsids. One analysis 
(Merck, 1997) similarly indicated affinities 
to the Euryapsida but recovered a novel 
result because the included characters of 
non-turtle euryapsids placed the entire turtle 
+ euryapsid clade as sister to the archosaur 
lineage (Brochu, 2001). 

In contrast, a growing body of molecular 
phylogenetic work strongly supports a posi- 
tion of turtles within Diapsida as sister to the 
crocodile/bird clade Archosauria (Cao et al., 
2000; Iwabe et al., 2005; Kumazawa and 
Nishida, 1999; Organ et al., 2008). Until 
now, no unique gross morphological support 
has been reported for archosaur affinities of 
turtles (Rieppel, 2000), and in particular, no 
morphological evidence has been forthcom- 
ing that would help place turtles along the 
archosaur stem. However, such evidence has 
existed, largely overlooked, since the further 
preparation and monographic description by 
Gaffney of the best-preserved stem turtle, 
Proganochelys quenstedti, from the Late 
Triassic (Norian) of Germany (Gaffney, 
1990). 

A single specimen of P. quenstedti (SMNS 
15759) preserves the region anterior to the 
braincase. In this region, which would in life 
have been occupied by the membranous 
anterior braincase, a pair of dorsoventrally 
tall, flat ossifications articulate with the 
prootic and basisphenoid on each side 
(Fig. 1A). The initial description of this 
region by Gaffney (1990) documented the 
form of these bones but did not treat the 
detailed morphology of each of their pro- 
cesses. It was noted that they are similar to a 
pair of ossifications synapomorphic for the 
clade Archosauriformes, the pleurosphe- 
noids (Fig. IB), which are now usually called 
laterosphenoids (Clark et al., 1993). Howev- 



er, the general consensus at the time, 
including the hypothesis presented by Gaff- 
ney (1990), was that turtles were sister to all 
other extant reptiles. These elements were 
thus termed "pleurosphenoids," with the 
quotation marks indicating probable non- 
homology with those of Archosauriformes. 
We posit, in contrast, that they are in fact 
homologous to the laterosphenoids of Arch- 
osauriformes. 

MATERIALS AND METHODS 

All specimens examined are from the 
collections of the Museum of Comparative 
Zoology, Harvard University. The following 
specimens from the Herpetology collection 
were examined: Alligator mississippiensis 
MCZ 17711, 34323; Caiman crocodilus 
MCZ 5031; Crocodylus cataphractus MCZ 
13985, 175004; C niloticus MCZ 4372; C 
porosus MCZ 72937; Gavialis gangeticus 
MCZ 33950; Osteolaemus tetraspis MCZ 
22913; Paleosuchus palpebrosus MCZ 
84030; Tomistoma schlegeli MCZ 12459. 
From the Ornithology collection: Tinamus 
major MCZ 342723, 342774. From the 
Vertebrate Paleontology collection: Eothyris 
parkeyiMCZ 1161. 

Phylogenetic analyses, as described below, 
used a modified version of the matrix from 
Dilkes (1998). Both used parsimony searches 
in PAUP* v4.0bl0 (Swofford, 2001) with the 
branch-and-bound search option (1,000 rep- 
licates), specifying Petrolacosaurus as the 
outgroup as in Dilkes (1998). The con- 
strained search used the monophyly con- 
straint option to unite Proganochelys with 
the archosauriform clade, including Eupar- 
keria and Proterosuchus. 

DESCRIPTION OF THE LATEROSPHE- 
NOID IN PROGANOCHELYS 

Following is a more complete description 
of the left laterosphenoid in Proganochelys 



2009 



ARCHOSAUR-LIKE LATEROSPHENOID IN EARLY TURTLES 



fenestra epiotica 



pila antotica 




fenestra 
prootica (V) 



pila metoptica 

fenestra metoptica (III) ' 

fenestra prootica (V) 
fenestra epiotica 
;'!."H»MiM<pr.r,<^3k' / ^taenia marginalis 

.taenia medialis 
pila metoptica ^^^ K^\>C / lv 

-pila antotica 




fenestra prootica (V) 



Figure 1 . (A) Left laterosphenoid of Proganochelys quenstedti SMNS 1 5759 in lateral view, after Gaffney (1990). 
(B) Right laterosphenoid of Proterosuchus fergusi NMQR 1484 in lateral view, reflected, after Clark et al. (1993). (C) 
Chondrocranium of Crocodylus porosus after ref 1 with region ossified as laterosphenoid filled in. BS, basisphenoid; 
FR, frontal; EP, epipterygoid; LS, laterosphenoid; OP, opisthotic; PA, parietal; PF, postfrontal; PO, postorbital; 
PR, prootic; Q, quadrate. 



BREVIORA 



No. 518 



than was offered in the original monograph. 
Our goal is to elucidate the developmental 
origins of the turtle laterosphenoid and thus 
demonstrate its exact correspondence to the 
archosauriform morphology. 

Mediolaterally, the laterosphenoid is thin, 
especially near its periphery, and it is inclined 
ventromedially, reflecting the angulation of 
the wall of the membranous braincase within 
which it ossified (Fig. 1A). It has three major 
components. The first is a strut that extends 
anterodorsally from the clinoid process of 
the basisphenoid, but whose posterodorsal 
portion forms a small contact with the 
anterodorsal portion of the prootic. The 
posterior margin of the strut forms the 
anterior half of the border of the trigeminal 
(prootic) foramen transmitting cranial nerve 
V, which is fully encircled by virtue of its 
dual contacts — the ventral, broad contact 
with the clinoid process of the basisphenoid 
and the dorsal, attenuate contact with the 
prootic. The anterior margin of the strut 
forms the posterior border of a ventrally 
incomplete aperture that in life would have 
been formed around cranial nerves III and 
IV. Topologically and morphologically, this 
strut corresponds exactly to the pila antotica 
of the embryonic amniote chondrocranium 
(Fig. 1C; Bellairs and Kamal, 1981), as 
suggested but not fully explicated in the 
description by Gaffney (1990). The meeting 
with the prootic and thus closure of the 
trigeminal foramen, however, is a unique 
feature of laterosphenoids. 

The second major component of the 
laterosphenoid is a broad, dorsoventrally 
oriented strut whose posterior margin arches 
over to form the anterior half of the aperture 
for cranial nerves III and IV (Fig. 1A). The 
strut becomes anteroposteriorly wider at its 
base and then ends, presumably where it 
would have sat upon the unossified fused 
trabeculae cranii. Its anterior margin forms 
the lower portion of an emargination that 



would have formed around cranial nerve II 
(optic nerve) and its associated neurovascu- 
lar structures. Thus, topologically and mor- 
phologically, this strut corresponds to the 
pila metoptica of the embryonic amniote 
chondrocranium (Fig. 1C), an observation 
not made in the description by Gaffney 
(1990). 

The third major component of the latero- 
sphenoid is an anterodorsally directed, ter- 
minally expanded lobe (Fig. 1A) connected 
basally to both of the other two components 
whose broadly curved anteroventral margin 
forms the majority of the emargination for 
cranial nerve II and whose posterodorsal 
margin borders an aperture that might 
represent the fenestra epioptica of the 
diapsid embryo (Bellairs and Kamal, 1981). 
As noted in the description by Gaffney 
(1990), the dorsal and anterior margins of 
the lobe appear unfinished. This morphology 
could represent breakage, but considering 
the general completeness of the surrounding 
elements, we think it more plausible that it is 
instead the border between the ossified and 
cartilaginous portions of the structure. The 
rough but not jagged texture of the surfaces 
supports this interpretation. The original 
description emphasizes that there are no 
signs on the parietal of a bony suture with 
the laterosphenoid. Topologically and mor- 
phologically, the lobe corresponds to the 
taenia medialis and perhaps a portion of the 
planum supraseptale of the chondrocranium 
(Fig. 1C) — not the planum supraseptale ex- 
clusively as suggested by Gaffney (1990). 

COMPARATIVE NOTES 

The laterosphenoid of Proganochelys is 
identical to the laterosphenoid present in the 
clade Archosauriformes (Clark et al., 1993) 
with the sole exception that it retains an open 
suture with the skull roof. The stem turtle 
Kayentachelys aprix, closer to the crown than 



2009 



ARCHOSAUR-LIKE LATEROSPHENOID IN EARLY TURTLES 



Proganochelys, also possesses laterosphe- 
noids (again described as "pleurosphe- 
noids"), though in existing specimens their 
detailed morphology is not discernable 
(Sterli and Joyce, 2007). This distribution 
suggests their ancestral presence in the turtle 
lineage. Unfortunately, specimens of the 
oldest known stem turtle, Odontochelys 
semitestacea, are dorsoventrally crushed, 
obscuring the relevant region (Li et al., 
2008). In modern turtles, ventral down- 
growths of the parietal articulate directly 
with the prootic and have thus obliterated 
any remnant of the laterosphenoids. 

The archosauriform laterosphenoid shows 
the three components listed above in every 
case where it is known, though there is some 
variation in their relative prominence 
(Fig. 1C). In crocodylians, for instance, and 
particularly Alligator, the pila metoptica 
component is reduced but present. The 
morphology and topology of the latero- 
sphenoid in turtles and Archosauriformes 
are unique among all vertebrates. It appears 
that the identity of the turtle laterosphenoid 
has simply been overlooked. The element is 
not mentioned in comprehensive reviews of 
the archosaur condition (Clark et al., 1993). 

As noted in the original description of 
Proganochelys and in subsequent works, 
stem reptiles had a more anterior spheneth- 
moid ossification, Y-shaped or V-shaped in 
transverse section. This ossification is lost in 
diapsids (de Braga and Rieppel, 1997). There 
is limited overlap between the region of 
ossification of the stem reptile sphenethmoid 
and the turtle/archosauriform laterosphe- 
noid. The posteriormost interorbital region, 
notably the base of the pila antotica, is only 
ossified in Archosauriformes and turtles (de 
Braga and Rieppel, 1997; Gaffney, 1990). 

The stem reptile sphenethmoid and turtle 
laterosphenoid were confounded and 
claimed to be homologous in some recent 
work, suggesting pareiasaur affinities for 



turtles (Lee, 1993, 1995, 1997). Interestingly, 
a rebuttal of many of the conclusions of that 
work (de Braga and Rieppel, 1997) asserted 
that both stem turtles and pareiasaurs have 
sphenethmoids. However, the anatomical 
criteria they set out for a sphenethmoid 
(e.g., complete enclosure of the optic nerve 
foramen) do not describe the structure in 
Proganochelys, although it does fit the 
structure in pareiasaurs. Simultaneously, 
their criteria for a true laterosphenoid 
("pleurosphenoid ,, ) precisely describe the 
structure in Proganochelys. The only plausi- 
ble explanation for this oversight is that the 
authors of that paper accepted the homology 
assessments of the study they were rebutting 
(Lee, 1995) without referring to the descrip- 
tion of Proganochelys by Gaffney (1990). 

CHARACTER DISTRIBUTION ON THE 

ARCHOSAUR STEM WITH 

TURTLES INCLUDED 

Not all stem archosaurs have a latero- 
sphenoid — as described earlier, the bone is a 
synapomorphy of Archosauriformes (Clarke 
et al., 1993), which excludes protorosaurs, 
rhynchosaurs, and Trilophosaurus (Dilkes, 
1998; Modesto and Sues, 2004; Sues, 2003). 
The presence of a laterosphenoid in turtles 
suggests a close relationship to Archosaur- 
iformes to the exclusion of non-archosauri- 
form archosauromorphs. Additionally, the 
presence of a tight suture of the latero- 
sphenoid to the parietal might unite Arch- 
osauriformes to the exclusion of turtles, 
suggesting, on the basis of this character, a 
sister-group relationship between the two. 
Unfortunately, the highly derived nature of 
the remainder of the turtle skull and post- 
cranium results in widely inconsistent results 
when turtles are included in morphological 
character matrices taken from other studies 
of reptilian relationships that did not initially 
include turtles. Typically, these analyses have 



B REV 10 R A 



No. 518 



not included a large number of characters 
within Archosauromorpha that would allow 
the precise placement of turtles within that 
clade (e.g., Miiller and Reisz, 2006, and 
references therein). A full analysis of rela- 
tionships will require considerable additional 
work. 

As a preliminary exercise, we scored P. 
quenstedti using the 144-character matrix by 
Dilkes (1998), the most comprehensive arch- 
osauromorph matrix in the literature. The 
characters listed by Dilkes (1998) as candi- 
dates for ordering were ordered. To his 
matrix, we added three characters: 

145. Laterosphenoid (0) not sutured to parietal or (1) 
sutured to parietal. 

146. Skull (0) broadly wedge-shaped or (1) tall and 
mediolaterally narrow. 

147. Mid-dorsal region dermal ossifications (0) absent or 
(1) present. 

We briefly discuss each of these in turn. 
See the Appendix for individual character 
scores. 

The skull of Euparkeria and archosaurs is 
tall and mediolaterally compressed com- 
pared with that of non-Archosauriformes 
and to an extent Proterosuchus. Progano- 
chelys shows what appears to be the primi- 
tive condition. Scoring of this character does 
not affect the current analysis, but it is a 
codification of this basic observation on 
skull proportions and will be useful as more 
taxa within Archosauria are added to the 
analyses. A row of ossifications close to the 
midline of the back is another overlooked 
potential synapomorphy of turtles and Arch- 
osauriformes. It is especially interesting 
because Odontochelys has only the mid- 
dorsal ossifications, the rest of the carapace 
remaining unossified (Li et al, 2008). If this is 
the primitive condition in the turtle lineage, 
it would be even more similar to the state in 
Archosauriformes, which have a pair of rows 
of osteoderms running down the center of 
the back (Gauthier et al., 1988). It is true that 



turtles appear to have a single row of discrete 
ossifications, whereas Archosauriformes 
have two, but despite this difference, they 
share the presence of a longitudinal series of 
dermal bone elements in the mid-dorsal 
region. 

In addition to the synapomorphies includ- 
ed in the matrix, P. quenstedti has what 
appears to be a typical diapsid infraorbital 
foramen, despite the lack of a separate 
ectopterygoid. This infraorbital foramen 
becomes progressively smaller along the 
lineage to extant turtles and is given the 
name "foramen palatinum posterius" (Joyce, 
2007). This terminology implies homology to 
a very small vascular foramen present in 
stem reptiles (Gaffney, 1990), despite the 
greater resemblance of the large foramen of 
plesiomorphic stem turtles to the diapsid 
infraorbital foramen. Only more crown-ward 
turtles have a very small foramen. 

The first, unconstrained parsimony analy- 
sis yielded a single most parsimonious tree of 
397 steps and recovered P. quenstedti as 
sister to Archosauromorpha (Fig. 2), sug- 
gesting archosaurian affinities for turtles, but 
a dual origin of the laterosphenoid. Synapo- 
morphies supporting this placement are: 
36(1), quadrate exposed laterally; 47(1), 
crista prootica present; 107(1), entepicondy- 
lar foramen absent; 122(1), fifth metatarsal 
hooked without deflection. Unambiguous 
synapomorphies along the lineage leading 
to Archosauriformes, but lacking in Proga- 
nochelys (requiring reversal if Proganochelys 
is allied to Archosauriformes), are: 2(1), 
snout greater than or equal to 50% of skull 
length; 5(1), antorbital fenestra present; 8(1), 
maxillary ramus of premaxilla extends as 
posterodorsal process to form caudal border 
of naris; 18(1), ratio of lengths of nasal and 
frontal greater than 1.0; 29(0), postparietal 
present; 37(1), quadrate emargination pre- 
sent with conch; 43(1), orientation of basip- 
terygoid processes lateral; 45(1), internal 



2009 



ARCHOSAUR-LIKE LATEROSPHENOID IN EARLY TURTLES 



Archosauromorpha 






Prolacerta 

Euparkeria 

Proterosuchus 

Mesosuchus 

Howesia 

Rhynchosaurus 

Scaphonyx 

Hyperodapedon 

Stenaulorhynchus 

Trilophosaurus 

Macrocnemus 

Langobardisaurus 

Tanystropheus 

Megalancosaurus 

Drepanosaurus 

Protorosaurus 

Proganochelys 

Squamata 

Gephyrosaurus 

Cteniogenys 

Champsosaurus 

Lazurussuchus 

Youngina 

Petrolacosaurus 



Figure 2. Single most parsimonious tree resulting from unconstrained phylogenetic analysis with the use of 
modified matrix from Dilkes (1998). 



carotid foramina on ventral surface of 
parasphenoid; 53(1), post-temporal fenestra 
small; 75(1), upturned retroarticular process; 
76(1), lateral mandibular fenestra; 79(0), 
postaxial cervical intercentra present; 87(2), 
second sacral rib bifurcate with caudal 
process truncated sharply; 88(2), proximal 
caudal neural spies very tall; 96(0), inter- 
clavicle broad diamond; 97(1), notch in 
interclavicle between clavicles; 104(1), ante- 
rior apron of pubis present; 109(1), medial 
centrale of carpus absent; 116(1), lateral 
tuber of calcaneum; 126(1), pterygoids re- 
main separate cranially. 

For the second analysis, we constrained P. 
quenstedti to be sister to Archosauriformes to 



determine potential synapomorphies in the 
case of a single origin of the laterosphenoid. 
A single most parsimonious tree of 413 steps 
was recovered (Fig. 3). In this tree, the 
ProganochelyslKrchos&unfovmQS clade was 
sister to the remaining archosauromorphs. 
Synapomorphies supporting a sister-group 
relationship between P. quenstedti and Arch- 
osauriformes are: 14(1), septomaxilla absent; 
50(1), laterosphenoid present; 74(2), retro- 
articular process present, large, and formed 
by articular; 77(1), slender and tapering 
cervical ribs at low angle to vetebrae present; 
83(1), notochordal canal absent in adult; 
89(1), ratio of lengths of caudal transverse 
processes and centra greater than 1.0; 102(1), 



BREVIORA 



No. 518 



Archosauromorpha 



Proganochelys 

Euparkeria 

Proterosuchus 

Macrocnemus 

Langobardisaurus 

Tanystropheus 

Megalancosaurus 

Drepanosaurus 

Protorosaurus 

Prolacerta 

Trilophosaurus 

Mesosuchus 

Howesia 

Rhynchosaurus 

Scaphonyx 

Hyperodapedon 

Stenaulorhynchus 

Cteniogenys 

Champsosaurus 

Lazurussuchus 

Squamata 

Gephyrosaurus 

Youngina 

Petrolacosaurus 

Figure 3. Single most parsimonious tree resulting from phylogenetic analysis with Proganochelys quenstedti 
constrained as sister to Archosauriformes with the use of modified matrix from Dilkes (1998). 




dorsal margin of ilium with large posterior 
process and smaller anterior process; 143(1), 
distal ends of cervical neural spines expanded 
in form of flat table; 147(1), mid-dorsal 
region dermal ossifications present. 

DISCUSSION 

The tree recovered by our first (uncon- 
strained) analysis agrees in its general topol- 
ogy with the preferred tree discussed by 
Dilkes (1998). This topology suggests a dual 
origin of the laterosphenoid; note, however, 
the caveats below about the overall topology 
of the tree. Nevertheless, Proganochelys does 



emerge on the basis of this dataset both as a 
diapsid and as part of the archosaur stem 
lineage. Constraining Proganochelys as sister 
to Archosauriformes (and therefore forcing a 
single origin of the laterosphenoid) pulls that 
clade into a sister-taxon relationship with the 
remaining archosauromorphs. That Proga- 
nochelys would exert a pull toward the 
archosauromorph base is unsurprising given 
that the apparently primitive reptilian char- 
acters of turtles generally place them as the 
sister taxon to the remaining reptiles in 
morphological phylogenetic analyses (Gau- 
thier et al., 1988). Additionally, the positions 
of Trilophosaurus and Prolacerta are labile, 



2009 



ARCHOSAUR-LIKE LATEROSPHENOID IN EARLY TURTLES 



with Prolacerta jumping from an affinity 
with Archosauriformes in the unconstrained 
tree to a more traditional position allied with 
other "primitive" archosauromorphs in the 
constrained tree. Trilophosaurus is highly 
autapomorphic and jumps from a sister- 
taxon relationship to a "higher" archosaur- 
omorph clade, including Archosauriformes, 
in the unconstrained analysis to a position 
sister to the "primitive" archosauromorph 
clade in the constrained analysis. Note that 
the new characters we added did not affect 
the broad-scale topology of the tree exclusive 
of Proganochelys. 

Because of the lability of the trees recov- 
ered using the matrix from Dilkes (1998) and 
the incongruence among various hypotheses 
of diapsid relationships, we consider that a 
good deal of additional work is required to 
create a truly comprehensive character list 
allowing a robust placement of turtles among 
fossil and extant taxa. The exercise described 
above is directed only at examining, in a 
preliminary way, the distribution of poten- 
tially interesting characters within Archo- 
sauromorpha if turtles have archosaur affin- 
ities. The continued lack of consensus about 
relationships within archosauromorphs is 
why we are careful to distinguish between 
physical identity between the laterosphenoids 
of turtles and archosauriforms, which we 
have shown, and homology between the 
structures. We subscribe to the "historical" 
homology concept, elegantly stated by Van 
Valen (1982) as "continuity of information" 
from ancestor to descendant. Thus, a con- 
clusive homology statement depends on a 
robust phylogenetic tree. 

The laterosphenoids in turtles and arch- 
osauriforms fulfill the requirements for a 
hypothesis of homology as set forth by 
Patterson (1982), including topology and 
ontogeny. Ontogeny, however, has since 
been discredited as a separate, special crite- 
rion for homology or character polarity 



determination (de Queiroz, 1985). Rather, 
characters from different times in an organ- 
ism's existence simply represent additional 
points of identity between putatively homol- 
ogous structures. The total existence of every 
organism in time consists of a series of 
"frames" or semaphoronts (sensu Hennig, 
1966), and points of identity that might be 
homology relations can be sought between 
any semaphoronts, no matter their relative 
sequence. Interestingly, Owen (1848) already 
understood, as stated explicitly in the intro- 
duction to the cited work, that different 
modes of development (early semaphoronts) 
do not preclude homology of later struc- 
tures. 

Although the debate on turtle origins and 
the evolution of their unique anatomy 
remains unresolved, molecular studies over- 
whelmingly indicate archosaurian affinities 
for turtles. The preliminary analyses we ran 
identified a number of interesting characters 
that might represent synapomorphies of 
turtles and various archosauromorph clades. 
Yet, the laterosphenoid alone is a character 
shared between turtles and a monophyletic 
group within archosauromorphs that does 
not appear elsewhere among vertebrates. It 
represents potential morphological support 
for the hypothesis that turtles are part of a 
major stem archosaur radiation and another 
example of the immense variety of the 
archosaur lineage. 



ACKNOWLEDGMENTS 

We thank Jacques Gauthier, Tyler Lyson, 
and Farish Jenkins for discussion of the 
structure in question. Jonathan Losos, Jose 
Rosado, Farish Jenkins, and Bill Amaral 
permitted access to comparative specimens. 
Reviews by Chris Brochu, Michael Lee, and 
Randy Irmis were uniformly insightful and 
constructive. 



10 



BREVIORA 



No. 518 



APPENDIX 1: 
ADDITIONS TO DILKES (1998) CHAR- 
ACTER MATRIX 

For new characters, order is: Pe, Y, G, Sq, 
Pr, Ma, Ta, Tr, Ho, Me, R, Sc, St, Hy, Ph, E, 
Ch, Ct, L, Po, Mg, Ln, D. See Dilkes (1998) 
for key to abbreviations. 
Character 145: ?????????????? 1 1 ??????? 
Character 146: 0000000000000001000000? 
Character 147: 00000000000000710000000 
Proganochelys quenstedti: 1077000010 
1111 200000 00070? 1011 0000? 121?? 
7701011101 2100?????? ????0002?0 
0012001011 0117770110 1???010021 
0100111101 007010???? 1112000000 
000007000? 0710001 

LITERATURE CITED 

Bellairs, A. D'A., and A. M. Kamal. 1981. The 
chondrocranium and the development of the 
skull in Recent reptiles, pp. 1-262. In C. Gans 
and T. S. Parsons (eds.), Biology of the Reptilia, 
Volume 11: Morphology F. London, Academic 
Press. 

Brochu, C. A. 2001. Progress and future directions in 
archosaur phylogenetics. Journal of Paleontology, 
75: 1185-1201. 

Clark, J. M., J. A. Welman, J. Gauthier, and M. 
Parrish. 1993. The laterosphenoid bone of early 
archosauriforms. Journal of Vertebrate Paleontol- 
ogy, 13: 48-57. 

Cao, Y., M. D. Sorensen, Y. Kumazawa, D. P. Mindell, 
and M. Hasegawa. 2000. Phylogenetic position of 
turtles among amniotes: evidence from mitochondrial 
and nuclear genes. Gene, 259: 139-148. 

De Queiroz, K. 1985. The ontogenetic method for 
determining character polarity and its relevance to 
phylogenetic systematics. Systematic Zoology, 34: 
280-299. 

Debraga, M., and O. Rieppel. 1997. Reptile phylogeny 
and the interrelationships of turtles. Zoological 
Journal of the Linnean Society, 120: 281— 
354. 

Dilk.es, D. W. 1998. The Early Triassic rhynchosaur 
Mesosuchus browni and the interrelationships of 
basal archosauromorph reptiles. Philosophical 
Transactions of the Royal Society of London B, 
353: 501-541. 



Gaffney, E. S. 1990. The comparative osteology of the 
Triassic turtle Proganochelys. Bulletin of the Amer- 
ican Museum of Natural History, 194: 1-263. 

Gauthier, J., A. G. Kluge, and T. Rowe. 1988. 
Amniote phylogeny and the importance of fossils. 
Cladistics, 4: 105-209. 

Hennig, W. 1966. Phylogenetic Systematics. Urbana, 
University of Illinois Press. 

Iwabe, N., Y. Hara, Y. Kumazawa, K. Shibamoto, Y. 
Saito, T. Miyata, and K. Katoh. 2005. Sister 
group relationship of turtles to the bird-crocodilian 
clade revealed by nuclear DNA-coded proteins. 
Molecular Biology and Evolution, 22: 810-813. 

Joyce, W. G. 2007. Phylogenetic relationships of 
Mesozoic turtles. Bulletin of the Peabody Museum 
of Natural History, 48: 3-102. 

, J. F. Parham, and J. A. Gauthier. 2004. 

Developing a protocol for the conversion of rank- 
based taxon names to phylogenetically defined 
clade names, as exemplified by turtles. Journal of 
Paleontology, 78: 989-1013. 

Kumazawa, Y., and M. Nishida. 1999. Complete 
mitochondrial DNA sequences of the green turtle 
and blue-tailed mole skink: statistical evidence for 
archosaurian affinities of turtles. Molecular Biology 
and Evolution, 16: 784-792. 

Laurin, M., and R. R. Reisz. 1995. A reevaluation of 
early amniote phylogeny. Zoological Journal of the 
Linnean Society, 113: 165-223. 

Lee, M. S. Y. 1993. The origin of the turtle body plan: 
bridging a famous morphological gap. Science, 261: 
1716-1720. 

. 1995. Historical burden in systematics and the 

interrelationships of "parareptiles." Proceedings of 
the Royal Society B, 263: 111-117. 

. 1997. Pareiasaur phylogeny and the origin of 



turtles. Zoological Journal of the Linnean Society, 
120: 197-280. 

Li, C, X. Wu, O. Rieppel, L. Wang, and L. Zhao. 2008. 
An ancestral turtle from the Late Triassic of 
southwestern China. Nature, 456: 497-501. 

Merck, J. W. 1997. A phylogenetic analysis of the 
Euryapsid reptiles. Ph.D. Dissertation. The Univer- 
sity of Texas at Austin. 785 pp. 

Modesto, S. P., and H.-D. Sues. 2004. The skull of the 
Early Triassic archosauromorph reptile Prolacerta 
broomi and its phylogenetic significance. Zoolo- 
gical Journal of the Linnean Society, 140: 335- 
351. 

MUller, J., and R. R. Reisz. 2006. The phylogeny of 
early eureptiles: comparing parsimony and Bayes- 
ian approaches in the investigation of a basal fossil 
clade. Systematic Biology, 55: 503-511. 



2009 



ARCHOSAUR-LIKE LATEROSPHENOID IN EARLY TURTLES 



II 



Organ, C. L., R. G. Moreno, and S. V. Edwards. 2008. 
Three tiers of genome evolution in reptiles. Inte- 
grative and Comparative Biology, 48: 494-504. 

Owen, R. 1848. On the Archetype and Homologies of 
the Vertebrate Skeleton. London, John van Voorst. 

Patterson, C. 1982. Morphological characters and 
homology, pp. 21-74. In K. A. Joysey and A. E. 
Friday (eds.), Problems of Phylogenetic Recon- 
struction. London and New York, Academic Press. 

Rieppel, O. 2000. Turtles as diapsid reptiles. Zoologica 
Scripta, 29: 199-212. 

— , and R. R. Reisz. 1999. The origin and early 
evolution of turtles. Annual Review of Ecology and 
Systematics, 30: 1-22. 



Sterli, J., and W. G. Joyce. 2007. The cranial ana- 
tomy of the Early Jurassic turtle Kayentachelys 
aprix. Acta Palaeontologca Polonica, 52: 675- 
694. 

Sues, H.-D. 2003. An unusual new archosauromorph 
reptile from the Upper Triassic Wolfville Forma- 
tion of Nova Scotia. Canadian Journal of Earth 
Sciences, 40: 635-649. 

Swofford, D. L. 2001. PAUP*: Phylogenetic Analysis 
Using Parsimony (*and Other Methods), Version 
4.0b 10. Sunderland, Massachusetts, Sinauer Associ- 
ates. 

Van Valen, L. 1982. Homology and causes. Journal of 
Morphology, 173: 305-312.