removal, which has been shown to be the rate-
determining step on similar surfaces (12–14,17).
Relative to their core-shell precursors, the nano-
cage models showed substantially enhanced ac-
tivity, which is attributed to the shortening of Pt-Pt
interatomic distances (table S2).
We evaluated the long-term stability of the
catalysts through an accelerated durability test
(Fig. 4, C and D). The Pt octahedral nanocages
showed the best performance, with the ORR mass
activity only reduced by 36% after 10,000 cycles,
still showing 3.4-fold enhancement relative to the
pristine Pt/C. The ECSAs of the cubic and octa-
hedral nanocages only dropped by 13 and 6% after
5000 cycles and by 32 and 23% after 10,000 cycles,
respectively. During the durability test, the holes
in the walls of the nanocages were slightly en-
larged (fig. S7). These results demonstrate that the
excellent durability associated with the core-shell
catalysts was not affected by the selective removal
of Pd cores.
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28. B. Han et al., Energy Environ. Sci. 8, 258–266 (2015).
The syntheses were supported by start-up funds from the
Georgia Institute of Technology (to Y.X.). As jointly supervised
PhD students from Xiamen University, L.Z. and X.W. were also
partially supported by fellowships from the China Scholarship
Council. The theoretical modeling work at University of
Wisconsin–Madison was supported by the U.S. Department of
Energy (DOE)–Basic Energy Sciences (BES), Office of Chemical
Sciences, grant DE-FG02-05ER15731. Calculations were
performed at supercomputing centers located at the
Environmental Molecular Sciences Laboratory, which is
sponsored by the DOE Office of Biological and Environmental
Research at the Pacific Northwest National Laboratory; Center
for Nanoscale Materials at Argonne National Laboratory,
supported by DOE contract DE-AC02-06CH11357; and National
Energy Research Scientific Computing Center, supported by
DOE contract DE-AC02-05CH11231. Part of the electron
microscopy work was performed through a user project
supported by the Oak Ridge National Laboratory’s Center for
Nanophase Materials Sciences, which is a DOE Office of Science
User Facility. J.L. gratefully acknowledges the support by Arizona
State University and the use of facilities in the John M. Cowley
Center for High Resolution Electron Microscopy at Arizona State
University. Data described can be found in the main figures and
supplementary materials. The authors declare no conflict of
Materials and Methods
Figs. S1 to S8
Tables S1 to S3
8 March 2015; accepted 15 June 2015
A four-legged snake from the Early
Cretaceous of Gondwana
David M. Martill,
Nicholas R. Longrich
Snakes are a remarkably diverse and successful group today, but their evolutionary origins are
obscure. The discovery of snakes with two legs has shed light on the transition from lizards to
snakes, but no snake has been described with four limbs, and the ecology of early snakes is
poorly known. We describe a four-limbed snake from the Early Cretaceous (Aptian) Crato
Formation of Brazil.The snake has a serpentiform body plan with an elongate trunk, short tail,
and large ventral scales suggesting characteristic serpentine locomotion, yet retains small
prehensile limbs. Skull and body proportions as well as reduced neural spines indicate fossorial
adaptation, suggesting that snakes evolved from burrowing rather than marine ancestors.
Hooked teeth, an intramandibular joint, a flexible spine capable of constricting prey, and the
presence of vertebrate remains in the guts indicate that this species preyed on vertebrates and
that snakes made the transition to carnivory early in their history.The structure of the limbs
suggests that they were adapted for grasping, either to seize prey or as claspers during mating.
Together with a diverse fauna of basal snakes from the Cretaceous of South America, Africa, and
India, this snake suggests that crown Serpentes originated in Gondwana.
Snakes are among the most diverse groups
of tetrapods, with >3000 extant species ex-
ploiting a remarkable range of niches (1).
Snakes inhabit deserts and rainforests, moun-
tains and oceans; and despite lacking limbs,
employ an extraordinary range of locomotor
styles, including crawling, burrowing, climbing,
swimming, and even gliding (1). All snakes are
predators, but they consume a wide range of prey,
from insects to large mammals (1). This diversity
is made possible by a specialized body plan, in-
cluding an elongate body with reduced limbs, a
flexible skull and ribs to swallow large prey (2),
and a specialized forked tongue and vomero-
nasal organ to detect chemical gradients (1). The
origins of this body plan remain unclear, how-
ever (1). One scenario holds that it originated in
a marine environment, whereas others argue that
it results from adaptation for a fossorial lifestyle.
New fossils (2–4), including snakes with hindlimbs
(5,6), have shed light on the lizard-to-snake
transition, but no snake has been reported with
four limbs. The ecology of early snakes is also un-
certain. Although alethinophidians are primarily
carnivorous (1), Typhlopidae and Anomal epididae,
which are basal with respect to Alethinophidia
(7–9), are insectivorous (1). This suggests that
early snakes were insectivores, although adap-
tations for carnivory in stem snakes (2) suggest
that carnivory may be primitive (2,5).
Here we report a fossil snake from the Early
Cretaceous of Gondwana, which sheds light on
these issues. Tetrapodophis amplectus gen. et sp.
nov. (holotype BMMS BK 2-2) is distinguished
from all other snakes by the following combina-
tion of characters: 160 precaudal and 112 caudal
vertebrae, short neural spines, four limbs, meta-
podials short, penultimate phalanges hyperelon-
gate and curved, phalangeal formula 2?-3-3-3-3?
(manus) 2-3-3-3-3 (pes).
The fossil (Fig. 1) comes from the Nova Olinda
Member of the Early Cretaceous (Aptian) Crato
Formation, Ceará, Brazil (10). The specimen is pre-
served on laminated limestone as part and coun-
terpart. The matrix is typical of the Nova Olinda
Member in being composed of fine-grained lam-
inated micrite with elongated pellets on the surface
of the slab representing coprolites of the fish Dastilbe.
As is typical of Crato vertebrates, the skeleton is
articulated and the bones are a translucent orange-
brown color; soft tissues are also preserved.
The snake affinities of Tetrapodophis are dem-
onstrated by derived features of the skull, axial
416 24 JULY 2015 •VOL 349 ISSUE 6246 sciencemag.org SCIENCE
School of Earth and Environmental Sciences, University of
Portsmouth, Portsmouth PO1 3QL, UK.
85134 Stammham, Germany.
Department of Biology and
Biochemistry and Milner Centre for Evolution, University of
Bath, Claverton Down, Bath BA2 7AY, UK.
on July 23, 2015www.sciencemag.orgDownloaded from on July 23, 2015www.sciencemag.orgDownloaded from on July 23, 2015www.sciencemag.orgDownloaded from on July 23, 2015www.sciencemag.orgDownloaded from
skeleton, limbs, integument, and even behavior
(Figs. 2 to 4) (* = snake autapomorphy). Snake-
like features of the skull include a short rostrum,
The mandible is bowed, with a deep subdental
ridge and an intramandibular joint formed by a
concave splenial cotyle contacting the angular, as
in Dinilysia (11). Teeth exhibit the ophidian con-
dition, being unicuspid and hooked, with expanded
bases. Implantation is subacrodont, with teeth
separated by interdental ridges; replacement
teeth are oriented subhorizontally.* Snake-like
features of the axial skeleton include an elon-
gate trunk with over 150 vertebrae,* zygosphene-
zygantrum articulations, a vaulted neural arch
with posterolateral tuberosities,* short neural
spines, haemal keels, large subcentral fossae/
foramina, tubercular processes of the ribs, and
lymphapophyses. The ilium is long and slender
as in other snakes; the fibula is bowed as in Najash
(5) and Simoliophiidae (12). Transverse belly scales*
are preserved, and the presence of a vertebrate
in the gut suggests a snake-like feeding strategy
in which proportionately large prey are ingested
whole. Although many of these features occur
in other long-bodied squamates, only snakes
exhibit all of them, and many of these characters
are uniquely ophidian.
Tetrapodophis exhibits a number of primitive
characters, however. The nasal is L-shaped, as in
Dinilysia (11) and Simoliophiidae. The maxilla’s
facial process is reduced as compared to those of
lizards but tall relative to those of crown snakes,
as in Coniophis (2). The subdental ridge is shal-
low posteriorly, a primitive feature shared with
Najash (5)andConiophis (2). Unlike crown snakes,
in which a convex splenial condyle articulates
with the angular, the splenial exhibits a concave
cotyle, as in Dinilysia (11). Prezygapophyseal
processes are absent as in other stem snakes;
synapophyses are kidney-shaped, lacking the dis-
tinct condyle and planar cotyle of alethinophidians.
Strikingly, Tetrapodophis retains reduced but ap-
parently functional forelimbs and hindlimbs.
To test Tetrapodophis’ophidian affinities, we
used a morphological matrix (13,14)toconduct
four phylogenetic analyses: with and without mo-
lecular backbone constraint (8) and with equal
and implied weighting (15). In each analysis,
Tetrapodophis emerges as a basal snake (Fig. 5)
Jurassic-Cretaceous stem ophidians Parviraptor,
molecular backbone is used (Fig. 5), Tetrapodophis
emerges as sister to Coniophis, and snakes emerge
as sister to the Mosasauria; i.e., Pythonomorpha,
as in a recent combined analysis (7).
As the only known four-legged snake, Tetra-
podophis sheds light on the evolution of snakes
from lizards. Tetrapodophis lacks aquatic adap-
tations (such as pachyostosis or a long, laterally
compressed tail) and instead exhibits features of
fossorial snakes and lizards: a short rostrum and
elongation of the postorbital skull, a long trunk
and short tail (16,17), short neural spines (18),
and highly reduced limbs (16,17). Tetrapodophis
therefore supports the hypothesis tha t snakes
ev olved from burrowing (2,5,6) rather than ma-
rine (19) ancestors. Although the current anal-
ysis suggests a sister-group relationship between
Mosasauria and Serpentes, Cretaceous aquatic
snakes (Simoliophiidae) are recovered nested
within crown Serpentes, and aquatic habits are
therefore derived (2,7).
Tetrapodophis also sheds light on the evolu-
tion of snake feeding. Tetrapodophis exhibits adap-
tations for carnivory, including recurved claw-like
teeth to seize large prey and an intramandibular
joint allowing the gape to expand to swallow
large prey. Along with the presence of a vertebrate
in the gut, these feature show that Tetrapodophis
preyed on vertebrates. Similar adaptations oc-
cur in other early snakes (2,11), suggesting that
snakes made the transition to carnivory early in
their history and that the insectivorous lifestyle
of typhlopids and anomalolepidids is derived.
The structure of the spine may represent an-
other such adaptation for carnivory. Elongate
bodies and reduced limbs evolved many times
among squamates (13,17), occurring in burrowing
SCIENCE sciencemag.org 24 JULY 2015 •VOL 349 ISSUE 6246 417
sdr ld rd
1 mm 1 mm
Fig. 2. T. amplectus, skull and jaws. (A) Skull. (B) Left mandible in medial view. Abbreviations: dt, dentary tooth; fp, facial process of maxilla, fr, frontal; idr,
interdental ridges; imj, intramandibular joint lm, left maxilla, ld, left dentary; mt, maxillary teeth; nas, nasal, par, parietal; pm, premaxilla; rd, right dentary; rd,
right dentary; rep, replacement teeth; sdr, subdental ridge; sp, splenial.
Fig. 1. T. amplectus, holotype part and counterpart. (A) Counterpart, showing skull and skeleton
impression. (B) Main slab, showing skeleton and skull impression.
and terrestrial forms (17)aswellasinaquatic
mosasaurs. Yet snakes are unique among long-
bodied squamates in having over 150 precaudal
vertebrae. This permits extreme flexibility of the
spinal column, so that the entire body can coil
into tight loops. The fact that other long-bodied
related to locomotion. We propose that the in-
creased number of trunk vertebrae may be an
adaptation allowing the body to be used to con-
strict prey. Tetrapodophis exhibits both an increased
number of precaudal vertebrae and a high degree
of flexibility, with the body forming a tight coil
anteriorly and a series of sinuous curves poste-
riorly, suggesting that constriction was developed
even in the earliest snakes.
The structure of the limbs may represent an-
other predatory adaptation. The snake-like spine
and reduced limbs of Tetrapodophis suggest that
the animal engaged in characteristic serpentine
locomotion, with the limbs playing little or no
role in locomotion. However, the specialized struc-
ture of the limbs suggests that they were func-
tional. Given Tetrapodophis’presumed fossorial
or semifossorial habits, digging is a plausible
function, but the limbs lack fossorial specializa-
tions. Instead, the manus and pes exhibit slender
isodactyl digits with hyperelongate penultimate
phalanges and abbreviated proximal phalanges.
of scansorial birds, sloths (20), and bats, suggest-
ing a grasping or hooking function. The limbs
may have functioned for grasping prey, or per-
haps mates. Climbing is another possibility, al-
though the low neural spines seem inconsistent
with this function. Regardless, Tetrapodophis
shows that after the initial evolution of serpen-
tine locomotion, the limbs were repurposed for
Finally, Tetrapodophis sheds light on the geo-
graphic origin of snakes. The Serpentes, Iguania,
and Anguimorpha form the Toxicofera (7–9), with
the oldest iguanian and anguimorph fossils com-
ing from Laurasia (13). These patterns suggest
that the center of toxicoferan diversification is
Laurasia and that the ancestors of snakes probably
originated there. The identification of possible
stem ophidians from the Jurassic and Early Cre-
taceous of Laurasia (4) would support this hypoth-
esis. However, the most basal divergences within
crown Serpentes, including Anomalolepididae
and Typhlopidae, Aniliidae and Tropidophiidae,
418 24 JULY 2015 •VOL 349 ISSUE 6246 sciencemag.org SCIENCE
1 mm 1 mm 1 mm
Fig. 4. T. amplectus appendicular morphology. (A) Forelimb. (B) Manus. (C) Hindlimbs and pelvis. (D)Pes.(E) Pelvis. Abbreviations: fem, femur; fib, fibula;
hu, humerus; il, ilium; lym, lymphapophysis; man, manus; mc, metacarpal; mt, metatarsals; ph, phalanges; ra, radius; sr, sacral rib; tib, tibia; ul, ulna; un, ungual.
Fig. 3. T. amplectus
axial column. (A)
Cervicals and anterior
presacrals. (B) Mid-
thorax, showing ventral
thorax, showing gut
tions: gc, gut contents;
nsp, neural spines;
syn, synapophyses vb,
vertebrate bone; vs,
ventral scales; zga,
are endemic to or originate in South America and
Africa, hinting at Gondwanan origins (1). Further-
more, during the middle Cretaceous, Gondwana was
home to a diverse fauna of basal snakes, including
Coniophiidae, Russellophiidae, Madtsoiidae (21),
and Simoliophiidae (22) in the Cenomanian of
Africa, the Cenomanian-Turonian Najash (18,23)in
South America, and now Tetrapodophis from the
Aptian of South America. Snakes are far less diverse
in the Cretaceous of Laurasia, with a single lineage
appearing in the Cenomanian (24)ofNorthAmer-
ica; alethinophidians do not appear until the
Maastrichtian in North America (14)andEurope(25).
These patterns suggest that the Serpentes r epr ese nt
an endemic Gondwanan radiation that saw lim-
ited dispersal to Laurasia during the Cretaceous.
Snakes appear to have been part of a highly
endemic herpetofauna that evolved in the Creta-
ceous in Gondwana. In this fauna, notosuchian
crocodiles (26) and rhynchocephalians (27) played
a major role, whereas squamates appear to have
been less diverse and disparate than in Laurasia.
The exception is the snakes, which radiated to
produce small burrowers, large constrictors,
and aquatic forms (21,22). Much of this herpeto-
fauna appears to have become extinct during
the Cretaceous-Paleogene extinction (Notosuchia)
or was greatly reduced in diversity in the Ceno-
zoic (Rhynchocephalia). Snakes, meanwhile, not
only survived but became diverse and widespread
in the Paleogene (14), perhaps in response to ecol-
ogical release provided by the end-Cretaceous
mass extinction (14).
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26. P. M. O’Connor et al., Nature 466, 748–751 (2010).
Thanks to B. A. S. Bhullar, J. A. Gauthier, and J. C. Rage for
discussions and to the anonymous reviewers whose comments
improved this paper. The holotype (BMMS BK 2-2) is housed at
the Bürgermeister-Müller-Museum, Solnhofen, Germany.
Figs. S1 to S7
23 February 2015; accepted 16 June 2015
SCIENCE sciencemag.org 24 JULY 2015 •VOL 349 ISSUE 6246 419
OPHIDIA Tetrapodophis amplectus
Fig. 5. Phylogenetic position of T. amplectus.
A strict consensus of 85 most parsimonious
trees found using implied weights and molec-
ular constraint is shown (see the supplemen-
tary materials) for a matrix of 632 characters
and 205 taxa.
, 416 (2015);349 Science et al.David M. Martill
A four-legged snake from the Early Cretaceous of Gondwana
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