Molecular evidence for a terrestrial origin of snakes

Biologists have debated the origin of snakes since the nineteenth century. One hypothesis suggests that snakes are most closely related to terrestrial lizards, and reduced their limbs on land. An alternative hypothesis proposes that snakes are most closely related to Cretaceous marine lizards, such as mosasaurs, and reduced their limbs in water. A presumed close relationship between living monitor lizards, believed to be close relatives of the extinct mosasaurs, and snakes has bolstered the marine origin hypothesis. Here, we show that DNA sequence evidence does not support a close relationship between snakes and monitor lizards, and thus supports a terrestrial origin of snakes.     

The First Freshwater Mosasauroid (Upper Cretaceous,Hungary) and a New Clade of Basal Mosasauroids

Mosasauroids are conventionally conceived of as gigantic, obligatorily aquatic marine lizards (1000s of specimens from marine deposited rocks) with a cosmopolitan distribution in the Late Cretaceous (90–65 million years ago [mya]) oceans and seas of the world. Here we report on the fossilized remains of numerous individuals (small juveniles to large adults) of a new taxon, Pannoniasaurus inexpectatus gen. et sp. nov. from the Csehbánya Formation, Hungary (Santonian, Upper Cretaceous, 85.3–83.5 mya) that represent the first known mosasauroid that lived in freshwater environments. Previous to this find, only one specimen of a marine mosasauroid, cf. Plioplatecarpus sp., is known from non-marine rocks in Western Canada. Pannoniasaurus inexpectatus gen. et sp. nov. uniquely possesses a plesiomorphic pelvic anatomy, a non-mosasauroid but pontosaur-like tail osteology, possibly limbs like a terrestrial lizard, and a flattened, crocodile-like skull. Cladistic analysis reconstructs P. inexpectatus in a new clade of mosasauroids: (Pannoniasaurus (Tethysaurus (Yaguarasaurus, Russellosaurus))). P. inexpectatus is part of a mixed terrestrial and freshwater faunal assemblage that includes fishes, amphibians turtles, terrestrial lizards, crocodiles, pterosaurs, dinosaurs and birds.     

Live birth in Cretaceous marine lizards (mosasauroids).

Although live-bearing (viviparity) has evolved around 100 times within reptiles, evidence of it is almost never preserved in the fossil record. Here, we report viviparity in mosasauroids, a group of Cretaceous marine lizards. This is the only known fossil record of live-bearing in squamates (lizards and snakes), and might represent the oldest occurrence of the trait in this diverse group; it is also the only known fossil record of viviparity in reptiles other than ichthyosaurs. An exceptionally preserved gravid female of the aigialosaur Carsosaurus (a primitive mosasauroid) contains at least four advanced embryos distributed along the posterior two-thirds of the long trunk region (dorsal vertebrae 9-21). Their orientation suggests that they were born tail-first (the nostrils emerging last) to reduce the possibility of drowning, an adaptation shared with other highly aquatic amniotes such as cetaceans, sirenians and ichthyosaurs; the orientation of the embryos also suggests that they were not gut contents because swallowed prey are usually consumed head-first. One embryo is located within the pelvis, raising the possibility that the adult died during parturition. Viviparity in early medium-sized amphibious aigialosaurs may have freed them from the need to return to land to deposit eggs, and permitted the subsequent evolution of gigantic totally marine mosasaurs.     

Earliest example of a giant monitor lizard (varanus, varanidae, squamata)

Background

Varanidae is a clade of tiny (<20 mm pre-caudal length [PCL]) to giant (>600 mm PCL) lizards first appearing in the Cretaceous. True monitor lizards (Varanus) are known from diagnostic remains beginning in the early Miocene (Varanus rusingensis), although extremely fragmentary remains have been suggested as indicating earlier Varanus. The paleobiogeographic history of Varanus and timing for origin of its gigantism remain uncertain.

Methodology/Principal Findings

A new Varanus from the Mytilini Formation (Turolian, Miocene) of Samos, Greece is described. The holotype consists of a partial skull roof, right side of a braincase, partial posterior mandible, fragment of clavicle, and parts of six vertebrae. A cladistic analysis including 83 taxa coded for 5733 molecular and 489 morphological characters (71 previously unincluded) demonstrates that the new fossil is a nested member of an otherwise exclusively East Asian Varanus clade. The new species is the earliest-known giant (>600 mm PCL) terrestrial lizard. Importantly, this species co-existed with a diverse continental mammalian fauna.

Conclusions/Significance

The new monitor is larger (longer) than 99% of known fossil and living lizards. Varanus includes, by far, the largest limbed squamates today. The only extant non-snake squamates that approach monitors in maximum size are the glass-snake Pseudopus and the worm-lizard Amphisbaena. Mosasauroids were larger, but exclusively marine, and occurred only during the Late Cretaceous. Large, extant, non-Varanus, lizards are limbless and/or largely isolated from mammalian competitors. By contrast, our new Varanus achieved gigantism in a continental environment populated by diverse eutherian mammal competitors.     

New dyrosaurid crocodylomorph and evidences for faunal turnover at the K-P transition in Brazil

The discovery of a new dyrosaurid crocodylomorph from the well-dated Palaeocene deposits of northeastern Brazil sheds new light on the evolutionary history of this extinct group of marine crocodylomorphs that have survived the Cretaceous-Palaeogene (K-P) extinction crisis. Guarinisuchus munizi, the most complete member of this group collected in South America so far, is closely related to the African forms, and this fact suggests that dyrosaurids had crossed the Atlantic Ocean before the K-P boundary and dispersed from there to North America and other parts of South America. This discovery also suggests that on the coast of northeastern Brazil, dyrosaurids replaced the pre-existing Late Cretaceous fauna of diversified mosasaurs, a group of marine lizards, after the K-P extinction event, becoming the main predators, together with sharks, in shallow marine Palaeocene environments. More detailed stratigraphic records and detailed dating of the deposits with dyrosaurids are necessary to correlate this particular pattern found in the ancient northeastern Brazilian coast within the evolution of the group, especially in Africa.     

The Asian grass lizard (Takydromus sexlineatus) does not respond to the scent of a native mammalian predator

Lacertid lizards use chemical cues emitted by saurophagous snakes to evade predation. Whether these lizards can detect and respond to the chemical cues of predatory mammals has not been studied. As many mammals carry distinct body odours and/or use chemical cues for intraspecific communication, lizards can be expected to use these chemicals as early warning cues. To test this idea, we observed the behaviour of Asian grass lizards (Takydromus sexlineatus) that had been transferred to an unfamiliar test arena containing one of four scent treatments. No particular scent was applied to the arena in the control situation. Diluted aftershave served as a pungency control. In the snake treatment, scent of the Oriental whip snake (Ahaetulla prasina) was applied. We included this treatment to learn how Asian grass lizards react to predator chemical cues. Finally, in the mongoose treatment, the lizards were confronted with scent cues of several small Indian mongooses (Herpestes auropunctatus). Snake scent elicited foot shakes, startles and tail vibrations. These are behaviours that in lacertid lizards are associated with stressful situations such as predatory encounters. Surprisingly, lizards confronted with mongoose scent exhibited none of these stress-indicating behaviours. In fact, their behaviour did not differ from that of lizards subjected to an odourless control treatment. These results raise concern. Mongooses are rapidly invading ecosystems worldwide. If lizards that have co-evolved with mongooses are unable to detect these predators’ presence through chemical cues, it seems highly unlikely that evolutionary naïve lizards will develop this ability rapidly.     

AN EARLY HERBIVOROUS LIZARD FROM THE LOWER CRETACEOUS OF JAPAN

Abstract:  The Lower Cretaceous Tetori Group of Japan has yielded diverse freshwater and terrestrial vertebrate assemblages. The most productive small vertebrate locality is the 'Kaseki-Kabe' or 'fossil-bluff' at Kuwajima, Hakusan City, Ishikawa Prefecture. These deposits have produced at least six distinct lizard taxa of which one, described and named here as Kuwajimalla kagaensis , has lanceolate denticulate teeth convergent on those of the living Iguana . This type of dentition is rare among living lizards and is usually considered indicative of herbivory and, more specifically, folivory. Kuwajimalla kagaensis provides the earliest unambiguous record of squamate herbivory. Comparisons with modern and fossil lizards suggest that Kuwajimalla may be an early relative of the macrocephalosaurines, a group of large herbivores well represented in the Upper Cretaceous of Mongolia.     

Convergent Evolution in Aquatic Tetrapods: Insights from an Exceptional Fossil Mosasaur

Mosasaurs (family Mosasauridae) are a diverse group of secondarily aquatic lizards that radiated into marine environments during the Late Cretaceous (98–65 million years ago). For the most part, they have been considered to be simple anguilliform swimmers – i.e., their propulsive force was generated by means of lateral undulations incorporating the greater part of the body – with unremarkable, dorsoventrally narrow tails and long, lizard-like bodies. Convergence with the specialized fusiform body shape and inferred carangiform locomotory style (in which only a portion of the posterior body participates in the thrust-producing flexure) of ichthyosaurs and metriorhynchid crocodyliform reptiles, along with cetaceans, has so far only been recognized in Plotosaurus, the most highly derived member of the Mosasauridae. Here we report on an exceptionally complete specimen (LACM 128319) of the moderately derived genus Platecarpus that preserves soft tissues and anatomical details (e.g., large portions of integument, a partial body outline, putative skin color markings, a downturned tail, branching bronchial tubes, and probable visceral traces) to an extent that has never been seen previously in any mosasaur. Our study demonstrates that a streamlined body plan and crescent-shaped caudal fin were already well established in Platecarpus, a taxon that preceded Plotosaurus by 20 million years. These new data expand our understanding of convergent evolution among marine reptiles, and provide insights into their evolution''s tempo and mode.     

中国化石两栖类和有鳞类研究进展:过去15年回顾

过去15年中,我国的化石两柄类和有鳞类研究取得了加速进展。共报道了16种两栖类和22种有鳞类,其中15种两栖类和11种有鳞类为新种,包括我国最古老的四足动物宁夏晚泥盆世的潘氏中国螈,湖北中三叠世的大型全椎两栖类宽头远安鲵,东北晚侏罗世/早白垩世的多种滑体两栖类(如无尾类三燕丽蟾和北票中蟾,有尾类奇异热河螈和东方塘螈),华北占近纪的蜥蜴类(如淅川短齿蜥和垣曲响蜥),以及内蒙古晚白垩世的多种蜥蜴类等。部分旧属种被修订,多与热河生物群的种类有关,如细小矢部龙过去依据幼年个体被认为是一种小型细弱的蜥蜴,新材料显示它实为大型强壮的种类。一批新的两栖类和有鳞类重要化石点被发现,如辽宁北票市四合屯、陆家屯和葫芦岛市水口子,河北丰宁县炮仗沟以及内蒙古宁城县道虎沟和乌拉特后旗巴彦满达呼。我国晚侏罗世/早白垩世两栖类和有鳞类对研究滑体两栖类和有鳞类相关类群的起源和早期演化提供了重要信息,但系统发育研究工作尚处于初级阶段。     

A tiny lizard (Lepidosauria,Squamata) from the Lower Cretaceous of Spain

Abstract: The smallest living amniotes are all lizards, but the fossil history of this size trait in Squamata is difficult to follow because small skeletons have low preservation potential and are often hard to detect in the field. A new squamate taxon, Jucaraseps grandipes gen. et sp. nov., is here described on the basis of an articulated skeleton from the Early Cretaceous Spanish lagerstätten of Las Hoyas. It differs from other known Mesozoic lizards in combining very small body size with a short rostrum, low maxillary tooth count, a relatively slender and elongated body, and short limbs with large hind feet. Phylogenetic analysis using TNT places it on the stem of a clade encompassing scincomorphs, gekkotans, snakes, amphisbaenians and anguimorphs. Comparison with modern lizards suggests it was probably a cryptic surface or subsurface ground dweller but not a burrower.     

The evolution of the lepidosaurian lower temporal bar: new perspectives from the Late Cretaceous of South China

Until recently, it was considered axiomatic that the skull of lizards and snakes arose from that of a diapsid ancestor by loss of the lower temporal bar. The presence of the bar in the living New Zealand Tuatara, Sphenodon, was thus considered primitive, corroborating its status as a ‘living fossil’. A combination of new fossils and rigorous phylogeny has demonstrated unequivocally that the absence of the bar is the primitive lepidosaurian condition, prompting questions as to its function. Here we describe new material of Tianyusaurus, a remarkable lizard from the Late Cretaceous of China that is paradoxical in having a complete lower temporal bar and a fixed quadrate. New material from Jiangxi Province is more complete and less distorted than the original holotype. Tianyusaurus is shown to be a member of the Boreoteiioidea, a successful clade of large herbivorous lizards that were dispersed through eastern Asia, Europe and North America in the Late Cretaceous, but disappeared in the end-Cretaceous extinction. A unique combination of characters suggests that Tianyusaurus took food items requiring a large gape.     

Seventy-five-million-year-old tropical tetra-like fish from Canada tracks Cretaceous global warming

Newly discovered fossil fish material from the Cretaceous Dinosaur Park Formation of Alberta, Canada, documents the presence of a tropical fish in this northern area about 75 million years ago (Ma). The living relatives of this fossil fish, members of the Characiformes including the piranha and neon tetras, are restricted to tropical and subtropical regions, being limited in their distribution by colder temperatures. Although characiform fossils are known from Cretaceous through to Cenozoic deposits, none has been reported previously from North America. The modern distribution of characiforms in Mexico and southern Texas in the southernmost United States is believed to have been the result of a relatively recent colonization less than 12 Ma. The new Canadian fossils document the presence of these fish in North America in the Late Cretaceous, a time of significantly warmer global temperatures than now. Global cooling after this time apparently extirpated them from the northern areas and these fishes only survived in more southern climes. The lack of early Cenozoic characiform fossils in North America suggests that marine barriers prevented recolonization during warmer times, unlike in Europe where Eocene characiform fossils occur during times of global warmth.     

Paleobiota from the Deccan volcano-sedimentary sequences of India: paleoenvironments,age and paleobiogeographic implications

Paleobiotic assemblages from the Deccan infra- and intertrappean beds are reviewed in great detail. Three distinct paleoenvironments (fluvio-lacustrine/terrestrial, brackish water and marine) have been identified within the infra- and intertrappean biotic assemblages of peninsular India. Recently, marine incursions have been recorded in a few of the Deccan intertrappean beds exposed in central and south-eastern India. The intertrappean beds have yielded marine planktic foraminiferans and freshwater/brackish water ostracods. The affinities of the paleobiotas are commonly considered to show a mixed pattern resulting from the addition of Gondwanan and Laurasian elements to endemic Indian taxa. During the last four decades, various biogeographic models (southern and northern connections) have been proposed to explain the presence of anomalous biogeographic biota in the Late Cretaceous of India. Based on the recovered fauna and flora assemblages, the Cretaceous–Paleogene boundary has been marked and a Late Cretaceous to Early Paleocene age has been assigned to these Deccan volcano-sedimentary sequences.     

Parataxonomy and palaeobiogeographic significance of dinosaur eggshell fragments from the Upper Cretaceous strata of the Cauvery Basin,South India

Abstract

In the past, fossilised dinosaur eggshells have been extensively documented from the Upper Cretaceous Lameta Formation of Central India and as many as nine oospecies are known at present from this formation. Compared to this, only one dinosaur oospecies has been described from the Cretaceous succession of the Cauvery Basin. However, the first fossil egg from India, identified as a chelonian egg, was documented from the Aptian – Albian Karai Formation of the Cauvery Basin in 1957. Following this, a solitary titanosaurid dinosaur egg was described from the Upper Cretaceous (Lower Maastrichtian) Kallankuruchhi Formation, Cauvery Basin in 1996. More recently, we have recovered isolated eggshell fragments from the marine part of the Upper Cretaceous (Late Maastrichtian) Kallamedu Formation. Based on eggshell morphology, microstructure and ultrastructure, these eggshell fragments are assigned to the oospecies Fusioolithus baghensis. The new find from the Cauvery Basin is important from palaeobiogeographic point of view as the oofamily Fusioolithidae is found in the Upper Cretaceous strata of India, France, Argentina and Morocco. Based on the common occurrence of similar oospecies in South America, Africa, Europe and India, a Late Cretaceous palaeobiogeographic connection between India and South America as well as Europe via Africa is suggested.     

Habitat avoidance of an introduced weed by native lizards

Abstract: Rubber vine (Cryptostegia grandiflora) is an environmental weed that frequently invades riparian habitats in northern Australia. I examined the habitat use of lizards in riparian and woodland environments comprised of native and rubber vine vegetation. Rubber vine was a major component of vegetation in the riparian habitat (approximately 40%), but only a minor component of woodland habitat (approximately 5%). Of 132 lizards, none were observed using rubber vine vegetation in riparian habitats, significantly less than expected, and only one lizard was observed in rubber vine vegetation in the woodland habitat. As rubber vine vegetation contains features that superficially resemble native habitat used by lizards, such as leaf litter, the avoidance of rubber vine by lizards suggests that rubber vine has underlying characteristics that create a suboptimal environment for lizards.     

Huehuecuetzpalli mixtecus gen. et sp. nov: a basal squamate (Reptilia) from the Early Cretaceous of Tepexi de Rodríguez,Central México

Huehuecuetzpalli mixtecus gen. et sp. nov. is characterized by a combination of characters unlike those of any of the previously described Late Jurassic or Early Cretaceous lizards. It has most of the synapomorphies common to modern squamates, but still retains primitive features rare in living taxa. Autapomorphic characters include an anteroposteriorly elongated premaxilla that results in the elongation of the snout and the apparent retraction of the external nares. A small rounded postfrontal and a parietal foramen on the frontoparietal suture suggest affinities with iguanians, but the retention of divided premaxillae, amphicoelous vertebrae, thoracolumbar intercentra, entepicondylar foramen, and a second distal tarsal supports the hypothesis that Huehuecuetzpalli has a more basal position relative to the extant squamates. Although its appearance is late in the fossil record of lizards, Huehuecuetzpalli is the first report of a basal squamate. It provides important information on early transformation of characters in lizard evolution. Many primitive characters present in some modern squamates are usually explained by paedomorphosis; however, these characters are common in early lizards suggesting that derived states may have been fixed later in lizard evolution. If Huehuecuetzpalli is an iguanian, then it would be the earliest known representative of this lineage and extends their fossil record into the Albian. This paper presents an extensive review of the characters and character states used in previously published cladistic analyses of the Squamata.     

Biochemical and microbiological evidence for fermentative digestion in free-living land iguanas (Conolophus pallidus) and marine iguanas (Amblyrhynchus cristatus) on the Galápagos archipelago

Herbivorous lizards are potentially capable of high digestive efficiency, but the presence of an indigenous microbial population has been implied from measurements of activity rather than directly studied. This study is the first to provide direct biochemical and microbiological evidence for fermentative digestion in free-living land iguanas (Conolophus pallidus) and marine iguanas (Amblyrhynchus cristatus) from the Galapagos archipelago. In marine iguanas, the stomach and large capacious colon contained ca. 32% and 60%, respectively, of the weight of total gut content. Total volatile fatty acid concentration was ca. 150 and 180 mM, respectively, for marine and land iguanas. Molar proportions of acetate, propionate, and butyrate (80.3%, 9.5%, and 3.5%) in land iguana fecal samples were similar to those for marine iguanas. Examination of fecal samples using confocal and transmission electron microscopy, as well as cultivable counts, revealed a dense and diverse population of bacteria, with spores prominent. Total culturable counts of anaerobes (2.22x10(8) g(-1) wet weight of fecal material) outnumbered aerobes on average by a factor of ca. 700. Combined, these results strongly support the contention that these unique herbivorous lizards are largely dependent on the presence and metabolic activities of a resident bacterial population in order to hydrolyze and ferment plant polymers that are indigestible to the host.     

Anatomy and relationships of Pachyrhachis problematicus,a primitive snake with hindlimbs

The anatomy of Pachyrhachis problematicus, an elongate, limb-reduced squamate from the Upper Cretaceous of Israel, is described and evaluated in detail. Previously considered a snake-like ''lizard'' of uncertain affinities, it is here shown to be the most primitive snake, and the sister-group to all other snakes. Pachyrhachis exhibits numerous derived characters uniting it with modern snakes (scolecophidians and alethinophidians): e.g. mobile premaxilla-maxilla articulation, braincase enclosed by frontals and parietals, sagittal parietal crest, absence of tympanic recess, single postdentary bone, over 140 presacral vertebrae, and complete loss of shoulder girdle and forelimb. However, it is more primitive than all modern snakes in retaining some strikingly primitive (lizard-like) features: presence of a jugal, squamosal, normal sacral attachment, and well-developed hindlimb composed of femur, tibia, fibula, and tarsals. Pachyrhachis provides additional support for the hypothesis that snakes are most closely related to Cretaceous marine lizards (mosasauroids). Almost all of the derived characters proposed to unite snakes and mosasauroids are highly developed in Pachyrhachis: the mobile mandibular symphysis, intramandibular joint, long and recurved pterygoid teeth, quadrate suspended by the supratemporal, loosely united pelvic elements (ilium, ischium, and pubis), and separate astragalus and calcaneum.