Middle Jurassic fossils document an early stage in salamander evolution

Salamanders are an important group of living amphibians and model organisms for understanding locomotion, development, regeneration, feeding, and toxicity in tetrapods. However, their origin and early radiation remain poorly understood, with early fossil stem-salamanders so far represented by larval or incompletely known taxa. This poor record also limits understanding of the origin of Lissamphibia (i.e., frogs, salamanders, and caecilians). We report fossils from the Middle Jurassic of Scotland representing almost the entire skeleton of the enigmatic stem-salamander Marmorerpeton. We use computed tomography to visualize high-resolution three-dimensional anatomy, describing morphologies that were poorly characterized in early salamanders, including the braincase, scapulocoracoid, and lower jaw. We use these data in the context of a phylogenetic analysis intended to resolve the relationships of early and stem-salamanders, including representation of important outgroups alongside data from high-resolution imaging of extant species. Marmorerpeton is united with Karaurus, Kokartus, and others from the Middle Jurassic–Lower Cretaceous of Asia, providing evidence for an early radiation of robustly built neotenous stem-salamanders. These taxa display morphological specializations similar to the extant cryptobranchid “giant” salamanders. Our analysis also demonstrates stem-group affinities for a larger sample of Jurassic species than previously recognized, highlighting an unappreciated diversity of stem-salamanders and cautioning against the use of single species (e.g., Karaurus) as exemplars for stem-salamander anatomy. These phylogenetic findings, combined with knowledge of the near-complete skeletal anatomy of Mamorerpeton, advance our understanding of evolutionary changes on the salamander stem-lineage and provide important data on early salamanders and the origins of Batrachia and Lissamphibia

A relict stem salamander: Evidence from the Early Cretaceous of Siberia

The early evolution of salamanders, which are one of the three living groups of lissamphibians, is not well known. Both stem- and crown-group salamanders first appeared in the Middle Jurassic (Bathonian), but subsequently had different evolutionary histories: stem salamanders were thought to have gone extinct in the Late Jurassic, while crown salamanders persist to the present day. Here, I report the discovery of an indeterminate stem salamander in the Lower Cretaceous (Aptian–Albian) Ilek Formation of Western Siberia. This is new evidence that the most basal salamanders survived beyond the Jurassic–Cretaceous boundary and co-existed with crown-group salamanders during approximately the first 40 million years of the known history of salamanders. The recognition of stem salamanders in the Early Cretaceous of Western Siberia adds to the inventory of taxa that suggest this area was a refugium for various groups of vertebrates with Jurassic affinities

Evolution and biogeography of frogs and salamanders, inferred from fossils, morphology and molecules

Classified in the Lissamphibia, modern amphibians are the only non-amniote tetrapods living today. They consist of three morphologically distinct groups: the tailless frogs and toads (Anura), the limbless caecilians (Gymnophiona), and the tailed salamanders and newts (Urodela). With 205 species, the caecilians are highly specialized worm-like forms that live a fossorial lifestyle, with a relatively narrow distribution in the tropic rainforests of South America, Africa and Asia (Duellman and Trueb, 1994; Amphibiaweb, 2015). Salamanders, with 683 species, are widely distributed in the North America, Asia and Europe, with a few plethodontids extending to Central and South America (Duellman and Trueb, 1994; Amphibiaweb, 2015). Frogs are the most diverse amphibian groups, with 6644 species distributed over all continents except Antarctica (Duellman and Trueb, 1994; Amphibiaweb, 2015). Both frogs and salamanders develop a wide array of lifestyles, ranging from terrestrial, aquatic, fossorial to aboreal lifestyles (Duellman and Trueb, 1994). During ontogeny, amphibian larvae usually undergo a drastic post-embryonic shift into an adult form, a term known as metamorphosis. In salamanders, another developmental pathway – neoteny – also occurs, in which the larval morphology is retained in sexually mature adults (Duellman and Trueb, 1994; Rose, 2003). Because of the diverse lifestyles and developmental pathways, frogs and salamanders are often used as model systems in many fields of biology (e.g., evo-devo). Over a century, but especially in the past two decades, a wealth of frog and salamander fossils has been discovered from the Mesozoic and Cenozoic of East Asia (e.g., Noble, 1924; Young, 1936; Borsuk-Bialynicka, 1978; Gao, 1986; Dong and Wang, 1998; Gao and Shubin, 2001, 2003, 2012; Gao and Wang, 2001; Gao and Chen, 2004; Wang and Rose, 2005; Wang and Evans, 2006b; Zhang et al., 2009; Chen et al., 2016; this study). Some of these fossils represent the earliest members of many crown clades, including the earliest crown salamanders from the Middle Jurassic (~165 Ma, Gao and Shubin, 2003), the earliest salamandroid from the Late Jurassic, the earliest sirenid from the Late Jurassic (this study), and the earliest spadefoot toads from the late Paleocence (Chen et al., 2016). Other fossils also bear important anatomical, temporal and geographical information in understanding their evolution. Unfortunately, the importance of many of these fossils remains obscure in a phylogenetic context. For example, an early-middle Oligocene Mongolian spadefoot toad Macropelobates osborni (Noble, 1924) was discovered outside the current distribution of spadefoot toads, yet its phylogenetic position and its implication on spadefoot toad biogeography remain not well understood. A major reason for the poor understanding of these fossils can be attributed to a trend of dichotomy between morphological and molecular phylogenies on amphibians. Whereas morphologists and paleontologists sometimes use a relatively small morphological dataset to reconstruct relationships (e.g., Gao and Shubin, 2012; Henrici, 2013), large-scale phylogenies are almost always conducted with molecular data with only living taxa (e.g., Roelants and Bossuyt, 2005; Pyron and Wiens, 2011). Very few studies on amphibian phylogeny have combined morphological and molecular data together, and even fewer also combined fossils. Because of this, the positions of many important fossils remains unclear, and the evolutionary scenarios inferred from only living species can sometimes be inconsistent with fossil evidence. In this thesis, I adopt a total-evidence approach to understand the evolution of amphibians, especially frogs and salamanders. I will incorporate information from fossils, morphology and molecules together to reconstruct the relationships. Compared with studies with each individual datasets, this approach incorporates all available data in a single analysis, with a goal to reach robust and congruent results that allow further discussions on character evolution and biogeographic reconstruction. The inclusion of fossils directly into the combined analysis provides the time dimension that is independent from molecular data (Norell, 1992). The anatomical combination of fossils can represent intermediate forms that help to solve the “long branch” problems caused by highly specialized modern taxa. The morphological dataset, despite its much smaller size with molecular data, is the only link between fossils and modern taxa. The inclusion of key morphological characters in both reconstructing phylogenetic hypotheses and examining character evolution provide consistent results that allow discussion on the homology/homoplasy of a certain character without ambiguity. The molecular sequence data provides overwhelmingly large data on modern taxa for phylogenetic reconstructions compared with morphological data, which helps to reach a robust hypothesis. Although fossils contain no molecular data, the inclusion of molecular sequence data into the combined analysis does have an effect on the positions of fossil taxa. By altering the relationship “framework” of modern taxa, the character optimization of fossils and other taxa of a combined analysis also varies compared with results of morphology-only analysis, thus changing the positions of fossils. In the following five chapters, I will describe a number of fossil amphibian species, reconstruct three combined phylogenies, and use the results for discussions on character evolution and biogeography. In Chapter 1 and Chapter 2, I focus on a frog clade called spadefoot toads (Anura: Pelobatoidea). In Chapter 1, I provide descriptions on three important fossil spadefoot toads from the Cenozoic of East Asia and North America: Macropelobates osborni from the early-middle Oligocene of Mongolia, Prospea holoserisca from the latest Paleocene of Mongolia, and Scaphiopus skinneri from the middle Oligocene of the United States. In Chapter 2, I conduct a combined phylogenetic analysis of archaeobatrachian frogs, and discuss the evolution of the bony spade and the historical biogeography of spadefoot toads based on the results of the phylogeny. In Chapter 3, I describe a new fossil frog from the Early Cretaceous of Inner Mongolia, China. The unique morphology of the new fossil is distinct from previous Early Cretaceous frogs from the Jehol Biota of China. Results of the combined analysis show that the new frog represents a basal member of the Pipanura. Comparisons between the Early Cretaceous frogs from China, Spain and Brazil show a high diversity of species coupled with a high degree of endemism during the Early Cretaceous. I discuss in the phylogenetic context how early frogs gradually reach their postcranial body plan with a shortened vertebral column, loss of ribs, and specialized pelvic regions. In Chapter 4, I provide a brief review of Mesozoic fossil salamanders from northern China, and describe a new fossil from the Late Jurassic of Liaoning Province, China. I conduct a combined phylogeny of higher-level relationships of salamanders. The new fossil, despite its general-looking appearance, represents a basal member of the highly specialized eel-like neotenic family Sirenidae on the cladogram. I discuss character evolutions in the Sirenidae, and how the neotenic developmental pathway evolved in early salamanders. In Chapter 5, I conduct a combined phylogenetic analysis of the salamander suborder Cryptobranchoidea, consisting of the neotenic giant salamanders (Cryptobranchidae) and the metamorphic Asiatic salamanders (Hynobiidae). The new morphological matrix includes new characters that were previously less sampled in the hynobranchial region. The monophyly of the Hynobiidae are confirmed by the new analysis, and four unequivocal synapomorphies are found for the clade. An S-DIVA biogeographic reconstruction is conducted to disscuss the distributional patterns of the Hynobiidae

Phalanx morphology in salamanders: A reflection of microhabitat use, life cycle or evolutionary constraints?

Morphological patterns are modeled by the interaction of functional, phylogenetic, ecological, and/or developmental constraints. In addition, the evolution of life cycle complexity can favor phenotypic diversity; however, the correlation between stages of development may constrain the evolution of some organs. Salamanders present microhabitat and life cycle diversity, providing an excellent framework for testing how these factors constrain phenotypic evolution. We reconstructed the morphological evolution of the terminal phalanx using a sample of 60 extinct and living species of salamanders. Using a geometric morphometric approach combined with comparative analyses, we further investigated the impact of phylogenetic, ecological, and/or life cycle factors on the shape of the terminal phalanx. We find that the phylogeny has some influence in determining the dorsal shape of the phalanges; whereas a relationship between microhabitat or life cycle and the dorsal and lateral shapes of the phalanx was not observed in the analyzed species. The allometric pattern found in the phalanx shape implies that small phalanges are more curved and with more truncated end than bigger phalanges. The evolutionary rate of phalanx shape was higher in the semiaquatic species, and the morphological disparity was significantly higher on biphasic groups. These results contradict the hypothesis that a complex life cycle constrains body shape. Finally, the phalanx shape of the salamander remains quite conserved from the Mesozoic. This configuration would allow them to occur in the different microhabitats occupied by the salamander lineages.Fil: Ponssa, María Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Fratani Da Silva, Jéssica. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico - Tucumán. Unidad Ejecutora Lillo; ArgentinaFil: Barrionuevo, J. Sebastián. Fundación Miguel Lillo; Argentin

A new Jurassic lizard from China

The Jurassic record of lizards in eastern Asia is poor by comparison with that of the Cretaceous. In China, to date, the only confirmed records from this period are an armoured lizard from Shishugou, Xinjiang Uygur Autonomous Region, of probable Oxfordian age, and two unnamed juvenile specimens from the slightly older, Callovian-Oxfordian, Daohugou locality of Nei Mongol. Here we describe the first lizard from the locality of Guancaishan, Jianping County, Liaoning Province. This locality is close to Daohugou, and is considered t o be of similar age. The new skeleton is articulated and well-preserved. It is distinguished from other Jurassic-Cretaceous lizards by a unique combination of derived characters, notably a long frontal with posterior processes that clasp the short parietal; cranial osteoderms limited to the lower temporal and supraocular regions; and an elongated manus and pes. Phylogenetic analysis using morphological data alone places the new taxon on the stem of a traditional ‘Scleroglossa’, but when the same data is run with a backbone constraint tree based on molecular data, the new taxon is placed on the stem of Squamata as a whole. Thus its position, and that of other Jurassic and Early Cretaceous taxa, seem to be influenced primarily by the position of Gekkota

Phylogeny and systematic history of early salamanders

Prevalent paedomorphy and convergence in salamander morphology has made it difficult to resolve relationships using purely morphological characters. However, many new fully articulated fossil salamanders have emerged, especially from China, and it is important to be able to place them within a phylogenetic framework to better understand the origin and radiation patterns of early salamanders. This study looks at the phylogeny of extant taxa using both molecular and morphological datasets. In deciphering the phylogeny of modern day taxa the limitations and caveats of the data were explored. The extent of the influence homoplasy and convergence have on the phylogenetic topology has been assessed using methods designed to identify and/or down-weight homoplasy in morphological characters. Once characters had been identified as potentially homoplasious and removed from the dataset, further analyses were performed on reduced datasets. Fossils were simulated by creating subsets of characters (those commonly found in the fossil record) for extant taxa. Analyses using parsimony and Bayesian inference were performed to test the robustness of the placements of these simulated fossils. The impact of missing data caused by poor preservation and incomplete specimens was tested by simulating reduced/limited character scores for living taxa, and then comparing the phylogenetic placement of these artificially degraded taxa with their ‘true’ position based on complete data. This paves the way for the inclusion of the fossils. While this study has not resolved the relationships between salamander families it has allowed a deeper understanding of the data, and assesses the confidence with which the placement of key fossils can be made in a new way. This novel method has further implications for the fitting of fossils within a phylogenetic framework in other problem clades. Biogeographic hypotheses can then be tested

Biogeographic history of Palearctic caudates revealed by a critical appraisal of their fossil record quality and spatio-temporal distribution

Altres ajuts: CERCA Programme/Generalitat de CatalunyaThe disjunct geographical range of many lineages of caudates points to a complex evolutionary and biogeographic history that cannot be disentangled by only considering the present-day distribution of salamander biodiversity. Here, we provide a critical reappraisal of the published fossil record of caudates from the Palearctic and quantitatively evaluate the quality of the group's fossil record. Stem-Urodela and Karauridae were widespread in the Palearctic in the Middle Jurassic, suggesting an earlier, unsampled diversification for this group. Cryptobranchidae reached Europe no later than the Oligocene, but this clade was subsequently extirpated from this continent, as well as from western and central Asia. The relatively recent appearance of hynobiids in the fossil record (Early Miocene) is most likely an artefact of a taphonomic bias against the preservation of high-mountain, stream-type environments which early members likely inhabited. Salamandroids first appear in Europe, expanding into Asia by the Miocene. The apparently enigmatic and disjunct distribution of extant caudate lineages is therefore explained by a wider past geographical range, as testified by the fossil record, which was fragmented during the late Cenozoic by a combination of tectonic (i.e. the uplift of the Tibetan Plateau) and climatic drivers, resulting in regional extirpations

Cranial biomechanics in basal urodeles: the Siberian salamander (Salamandrella keyserlingii) and its evolutionary and developmental implications

Developmental changes in salamander skulls, before and after metamorphosis, afect the feeding capabilities of these animals. How changes in cranial morphology and tissue properties afect the function of the skull are key to decipher the early evolutionary history of the crown-group of salamanders. Here, 3D cranial biomechanics of the adult Salamandrella keyserlingii were analyzed under diferent tissue properties and ossifcation sequences of the cranial skeleton. This helped unravel that: (a) Mechanical properties of tissues (as bone, cartilage or connective tissue) imply a consensus between the stifness required to perform a function versus the fxation (and displacement) required with the surrounding skeletal elements. (b) Changes on the ossifcation pattern, producing fontanelles as a result of bone loss or failure to ossify, represent a trend toward simplifcation potentially helping to distribute stress through the skull, but may also imply a major destabilization of the skull. (c) Bone loss may be originated due to biomechanical optimization and potential reduction of developmental costs. (d) Hynobiids are excellent models for biomechanical reconstruction of extinct early urodeles

Microvertebrates of the Lourinhã Formation (Late Jurassic, Portugal)

The Upper Jurassic of Portugal has been globally known for its microfossil vertebrate fauna thanks to the Konzentrat-Lagerstätte of the Guimarota mine, which provided thousands of bone fragments, isolated teeth, and even complete specimens. Other vertebrate microfossil assemblages have been studied around the world. Besides Guimarota, no other Portuguese Jurassic assemblage has been extensively studied. Hereby is presented a revision of the state of the art on Portuguese microvertebrate record, and the first microvertebrate studies on three localities from the Lourinhã Formation (Late Jurassic) hosted by a Portuguese institution; Porto das Barcas, Zimbral, and Valmitão has provided 2,497 microvertebrates skeletal remains and teeth, from which 824 specimens have been identified, described and assessed to the conservative-most taxa. The stratigraphy and sedimentology of the localities suggest that Porto das Barcas and Zimbral were floodplain mud deposits, and Valmitão was an oxbow lake mud deposit, with a slow rate of sedimentation. The remains have been attributed to fishes, amphibians, squamates, crocodylomorphs, and dinosaurs; but unfortunately, no mammaliaform material has been collected. Paleoecological analyses suggest Zimbral and Valmitão were dominated by a terrestrial fauna and more diverse than Porto das Barcas, dominated by an amphibious fauna. The Lourinhã Formation appears to have been closer to the shoreline than American localities in the Morrison and Cloverly Formations were, but more continental than Buenache and Las Hoyas localities (Spain) with swamp to lacustrine paleoenvironments. A detailed study on 125 crocodylomorph teeth from Valmitão support the presence of Goniopholididae, at least two Atoposauridae taxa, and Bernissartiidae in the Late Jurassic of Portugal, with a fauna either dominated by relative small individuals, either juveniles or adults or small taxa