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Fidelity of preservation of the insects from the Crato Formation (Lower Cretaceous), Brazil. View
project
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removal, which has been shown to be the rate- Environmental Molecular Sciences Laboratory, which is University. Data described can be found in the main figures and
determining step on similar surfaces (12–14, 17). sponsored by the DOE Office of Biological and Environmental supplementary materials. The authors declare no conflict of
Research at the Pacific Northwest National Laboratory; Center interests.
Relative to their core-shell precursors, the nano- for Nanoscale Materials at Argonne National Laboratory,
cage models showed substantially enhanced ac- supported by DOE contract DE-AC02-06CH11357; and National SUPPLEMENTARY MATERIALS
tivity, which is attributed to the shortening of Pt-Pt Energy Research Scientific Computing Center, supported by www.sciencemag.org/content/349/6246/412/suppl/DC1
interatomic distances (table S2). DOE contract DE-AC02-05CH11231. Part of the electron Materials and Methods
microscopy work was performed through a user project Figs. S1 to S8
We evaluated the long-term stability of the supported by the Oak Ridge National Laboratory’s Center for Tables S1 to S3
catalysts through an accelerated durability test Nanophase Materials Sciences, which is a DOE Office of Science References (29–37)
(Fig. 4, C and D). The Pt octahedral nanocages User Facility. J.L. gratefully acknowledges the support by Arizona
showed the best performance, with the ORR mass State University and the use of facilities in the John M. Cowley 8 March 2015; accepted 15 June 2015
Center for High Resolution Electron Microscopy at Arizona State 10.1126/science.aab0801
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 EVOLUTION
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
A four-legged snake from the Early
excellent durability associated with the core-shell
Cretaceous of Gondwana
S
12. S. Xie et al., Nano Lett. 14, 3570–3576 (2014).
13. J. Park et al., ACS Nano 9, 2635–2647 (2015). nakes are among the most diverse groups carnivorous (1), Typhlopidae and Anomalepididae,
14. X. Wang et al., Nat. Commun. 6, 7594 (2015).
15. Y. Yin et al., Science 304, 711–714 (2004).
of tetrapods, with >3000 extant species ex- which are basal with respect to Alethinophidia
16. M. Jin et al., Nano Res. 4, 83–91 (2011). ploiting a remarkable range of niches (1). (7–9), are insectivorous (1). This suggests that
17. Materials and methods are available as supplementary Snakes inhabit deserts and rainforests, moun- early snakes were insectivores, although adap-
materials on Science Online. tains and oceans; and despite lacking limbs, tations for carnivory in stem snakes (2) suggest
18. X. Xia et al., Proc. Natl. Acad. Sci. U.S.A. 110, 6669–6673
(2013).
employ an extraordinary range of locomotor that carnivory may be primitive (2, 5).
19. M. Heggen, M. Oezaslan, L. Houben, P. Strasser, J. Phys. Chem. styles, including crawling, burrowing, climbing, Here we report a fossil snake from the Early
C 116, 19073–19083 (2012). swimming, and even gliding (1). All snakes are Cretaceous of Gondwana, which sheds light on
20. J. Erlebacher, M. J. Aziz, A. Karma, N. Dimitrov, K. Sieradzki, predators, but they consume a wide range of prey, these issues. Tetrapodophis amplectus gen. et sp.
Nature 410, 450–453 (2001).
21. V. A. Baheti, R. Ravi, A. Paul, J. Mater. Sci. Mater. Electron. 24,
from insects to large mammals (1). This diversity nov. (holotype BMMS BK 2-2) is distinguished
2833–2838 (2013). is made possible by a specialized body plan, in- from all other snakes by the following combina-
22. N. M. Markovic, P. N. Ross, Surf. Sci. Rep. 45, 117–229 cluding an elongate body with reduced limbs, a tion of characters: 160 precaudal and 112 caudal
(2002). flexible skull and ribs to swallow large prey (2), vertebrae, short neural spines, four limbs, meta-
23. J. Zhang, H. Yang, J. Fang, S. Zou, Nano Lett. 10, 638–644
(2010).
and a specialized forked tongue and vomero- podials short, penultimate phalanges hyperelon-
24. J. Wu, A. Gross, H. Yang, Nano Lett. 11, 798–802 nasal organ to detect chemical gradients (1). The gate and curved, phalangeal formula 2?-3-3-3-3?
(2011). origins of this body plan remain unclear, how- (manus) 2-3-3-3-3 (pes).
25. S.-I. Choi et al., Nano Lett. 13, 3420–3425 (2013). ever (1). One scenario holds that it originated in The fossil (Fig. 1) comes from the Nova Olinda
26. C. Cui, L. Gan, M. Heggen, S. Rudi, P. Strasser, Nat. Mater. 12,
765–771 (2013).
a marine environment, whereas others argue that Member of the Early Cretaceous (Aptian) Crato
27. L. Gan et al., Science 346, 1502–1506 (2014). it results from adaptation for a fossorial lifestyle. Formation, Ceará, Brazil (10). The specimen is pre-
28. B. Han et al., Energy Environ. Sci. 8, 258–266 (2015). New fossils (2–4), including snakes with hindlimbs served on laminated limestone as part and coun-
(5, 6), have shed light on the lizard-to-snake terpart. The matrix is typical of the Nova Olinda
ACKN OW LEDG MEN TS
transition, but no snake has been reported with Member in being composed of fine-grained lam-
The syntheses were supported by start-up funds from the
Georgia Institute of Technology (to Y.X.). As jointly supervised
four limbs. The ecology of early snakes is also un- inated micrite with elongated pellets on the surface
PhD students from Xiamen University, L.Z. and X.W. were also certain. Although alethinophidians are primarily of the slab representing coprolites of the fish Dastilbe.
partially supported by fellowships from the China Scholarship As is typical of Crato vertebrates, the skeleton is
1
Council. The theoretical modeling work at University of School of Earth and Environmental Sciences, University of articulated and the bones are a translucent orange-
Wisconsin–Madison was supported by the U.S. Department of Portsmouth, Portsmouth PO1 3QL, UK. 2Tannenweg 16,
Energy (DOE)–Basic Energy Sciences (BES), Office of Chemical 85134 Stammham, Germany. 3Department of Biology and
brown color; soft tissues are also preserved.
Sciences, grant DE-FG02-05ER15731. Calculations were Biochemistry and Milner Centre for Evolution, University of The snake affinities of Tetrapodophis are dem-
performed at supercomputing centers located at the Bath, Claverton Down, Bath BA2 7AY, UK. onstrated by derived features of the skull, axial
skeleton, limbs, integument, and even behavior are preserved, and the presence of a vertebrate Strikingly, Tetrapodophis retains reduced but ap-
(Figs. 2 to 4) (* = snake autapomorphy). Snake- in the gut suggests a snake-like feeding strategy parently functional forelimbs and hindlimbs.
like features of the skull include a short rostrum, in which proportionately large prey are ingested To test Tetrapodophis’ ophidian affinities, we
a long braincase, and a nasal descending lamina. whole. Although many of these features occur used a morphological matrix (13, 14) to conduct
The mandible is bowed, with a deep subdental in other long-bodied squamates, only snakes four phylogenetic analyses: with and without mo-
ridge and an intramandibular joint formed by a exhibit all of them, and many of these characters lecular backbone constraint (8) and with equal
concave splenial cotyle contacting the angular, as are uniquely ophidian. and implied weighting (15). In each analysis,
in Dinilysia (11). Teeth exhibit the ophidian con- Tetrapodophis exhibits a number of primitive Tetrapodophis emerges as a basal snake (Fig. 5)
dition, being unicuspid and hooked, with expanded characters, however. The nasal is L-shaped, as in but is closer to modern snakes than the putative
bases. Implantation is subacrodont, with teeth Dinilysia (11) and Simoliophiidae. The maxilla’s Jurassic-Cretaceous stem ophidians Parviraptor,
separated by interdental ridges; replacement facial process is reduced as compared to those of Diablophis, Portugalophis, and Eophis. When a
teeth are oriented subhorizontally.* Snake-like lizards but tall relative to those of crown snakes, molecular backbone is used (Fig. 5), Tetrapodophis
features of the axial skeleton include an elon- as in Coniophis (2). The subdental ridge is shal- emerges as sister to Coniophis, and snakes emerge
gate trunk with over 150 vertebrae,* zygosphene- low posteriorly, a primitive feature shared with as sister to the Mosasauria; i.e., Pythonomorpha,
zygantrum articulations, a vaulted neural arch Najash (5) and Coniophis (2). Unlike crown snakes, as in a recent combined analysis (7).
with posterolateral tuberosities,* short neural in which a convex splenial condyle articulates As the only known four-legged snake, Tetra-
spines, haemal keels, large subcentral fossae/ with the angular, the splenial exhibits a concave podophis sheds light on the evolution of snakes
foramina, tubercular processes of the ribs, and cotyle, as in Dinilysia (11). Prezygapophyseal from lizards. Tetrapodophis lacks aquatic adap-
lymphapophyses. The ilium is long and slender processes are absent as in other stem snakes; tations (such as pachyostosis or a long, laterally
as in other snakes; the fibula is bowed as in Najash synapophyses are kidney-shaped, lacking the dis- compressed tail) and instead exhibits features of
(5) and Simoliophiidae (12). Transverse belly scales* tinct condyle and planar cotyle of alethinophidians. 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 that snakes
evolved 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.
10 mm The structure of the spine may represent an-
other such adaptation for carnivory. Elongate
Fig. 1. T. amplectus, holotype part and counterpart. (A) Counterpart, showing skull and skeleton bodies and reduced limbs evolved many times
impression. (B) Main slab, showing skeleton and skull impression. among squamates (13, 17), occurring in burrowing
fr lm nas fp mt
pm dt
par
rep
idr ld
rm
sdr rd
ld mec rd
imj sp
sp sdr
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.
and terrestrial forms (17) as well as in aquatic spinal column, so that the entire body can coil creased number of trunk vertebrae may be an
mosasaurs. Yet snakes are unique among long- into tight loops. The fact that other long-bodied adaptation allowing the body to be used to con-
bodied squamates in having over 150 precaudal squamates lack this feature suggests that it is not strict prey. Tetrapodophis exhibits both an increased
vertebrae. This permits extreme flexibility of the related to locomotion. We propose that the in- number of precaudal vertebrae and a high degree
of flexibility, with the body forming a tight coil
Fig. 3. T. amplectus zga anteriorly and a series of sinuous curves poste-
zgs
axial column. (A) riorly, suggesting that constriction was developed
nsp poz
Cervicals and anterior even in the earliest snakes.
presacrals. (B) Mid- The structure of the limbs may represent an-
thorax, showing ventral other predatory adaptation. The snake-like spine
scales. (C) Posterior and reduced limbs of Tetrapodophis suggest that
thorax, showing gut syn the animal engaged in characteristic serpentine
contents. Abbrevia- locomotion, with the limbs playing little or no
tions: gc, gut contents; role in locomotion. However, the specialized struc-
nsp, neural spines; prz ture of the limbs suggests that they were func-
poz, postzygapophysis; tional. Given Tetrapodophis’ presumed fossorial
prz, prezygapophysis; 1 mm or semifossorial habits, digging is a plausible
syn, synapophyses vb, function, but the limbs lack fossorial specializa-
vertebrate bone; vs, tions. Instead, the manus and pes exhibit slender
ventral scales; zga, isodactyl digits with hyperelongate penultimate
zygantrum; zgs, phalanges and abbreviated proximal phalanges.
zygosphene. This suite of characters recalls the prehensile feet
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-
1mm vs tine locomotion, the limbs were repurposed for
another function.
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-
vb taceous of Laurasia (4) would support this hypoth-
esis. However, the most basal divergences within
gc crown Serpentes, including Anomalolepididae
1mm
and Typhlopidae, Aniliidae and Tropidophiidae,
cal
as
hu mc mt
fem
fem ph
ph I
I ph
ra II
fib fib
fb
ul III un
ph b IV V 1 mm
tib tib
mann
un
V pes
IV il sr
II pes lym
III
1 mm 1 mm iil
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.
are endemic to or originate in South America and South America, and now Tetrapodophis from the an endemic Gondwanan radiation that saw lim-
Africa, hinting at Gondwanan origins (1). Further- Aptian of South America. Snakes are far less diverse ited dispersal to Laurasia during the Cretaceous.
more, during the middle Cretaceous, Gondwana was in the Cretaceous of Laurasia, with a single lineage Snakes appear to have been part of a highly
home to a diverse fauna of basal snakes, including appearing in the Cenomanian (24) of North Amer- endemic herpetofauna that evolved in the Creta-
Coniophiidae, Russellophiidae, Madtsoiidae (21), ica; alethinophidians do not appear until the ceous in Gondwana. In this fauna, notosuchian
and Simoliophiidae (22) in the Cenomanian of Maastrichtian in North America (14) and Europe (25). crocodiles (26) and rhynchocephalians (27) played
Africa, the Cenomanian-Turonian Najash (18, 23) in These patterns suggest that the Serpentes represent a major role, whereas squamates appear to have
been less diverse and disparate than in Laurasia.
JURASSIC CRETACEOUS PALAEOGENE NEOGENE The exception is the snakes, which radiated to
produce small burrowers, large constrictors,
Kimmeridgian
Maastrichtian
Cenomanian
Valanginian
Campanian
Tithonian
Berriasian
Barremian
Coniacian
Paleocene
Oligocene
Aalenian
Oxfordian
Miocene
Turonian
Santonian
Eocene
Aptian
Pliocene
and aquatic forms (21, 22). Much of this herpeto-
Albian
Hauterivian
Pleistocene
Bathonian
Callovian
Bajocian
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