The first Miocene fossils from coastal woodlands in the southern East African Rift.

The Miocene was a key time in the evolution of African ecosystems witnessing the origin of the African apes and the isolation of eastern coastal forests through an expanding arid corridor. Until recently, however, Miocene sites from the southeastern regions of the continent were unknown. Here, we report the first Miocene fossil teeth from the shoulders of the Urema Rift in Gorongosa National Park, Mozambique. We provide the first 1) radiometric ages of the Mazamba Formation, 2) reconstructions of paleovegetation in the region based on pedogenic carbonates and fossil wood, and 3) descriptions of fossil teeth. Gorongosa is unique in the East African Rift in combining marine invertebrates, marine vertebrates, reptiles, terrestrial mammals, and fossil woods in coastal paleoenvironments. The Gorongosa fossil sites offer the first evidence of woodlands and forests on the coastal margins of southeastern Africa during the Miocene, and an exceptional assemblage of fossils including new species.

Disruption of trait-environment relationships in African megafauna occurred in the middle Pleistocene.

Mammalian megafauna have been critical to the functioning of Earth's biosphere for millions of years. However, since the Plio-Pleistocene, their biodiversity has declined concurrently with dramatic environmental change and hominin evolution. While these biodiversity declines are well-documented, their implications for the ecological function of megafaunal communities remain uncertain. Here, we adapt ecometric methods to evaluate whether the functional link between communities of herbivorous, eastern African megafauna and their environments (i.e., functional trait-environment relationships) was disrupted as biodiversity losses occurred over the past 7.4 Ma. Herbivore taxonomic and functional diversity began to decline during the Pliocene as open grassland habitats emerged, persisted, and expanded. In the mid-Pleistocene, grassland expansion intensified, and climates became more variable and arid. It was then that phylogenetic diversity declined, and the trait-environment relationships of herbivore communities shifted significantly. Our results divulge the varying implications of different losses in megafaunal biodiversity. Only the losses that occurred since the mid-Pleistocene were coincident with a disturbance to community ecological function. Prior diversity losses, conversely, occurred as the megafaunal species and trait pool narrowed towards those adapted to grassland environments.

The utility of body size as a functional trait to link the past and present in a diverse reptile clade.

Understanding the relationships between functional traits and environment is increasingly important for assessing ecosystem health and forecasting biotic responses to future environmental change. Taxon-free analyses of functional traits (ecometrics) allow for testing the performance of such traits through time, utilizing both the fossil record and paleoenvironmental proxies. Here, we test the role of body size as a functional trait with respect to climate, using turtles as a model system. We examine the influence of mass-specific metabolic rate as a functional factor in the sorting of body size with environmental temperature and investigate the utility of community body size composition as an ecometric correlated to climate variables. We then apply our results to the fossil record of the Plio-Pleistocene Shungura Formation in Ethiopia. Results show that turtle body sizes scale with mass-specific metabolic rate for larger taxa, but not for the majority of species, indicating that metabolism is not a primary driver of size. Body size ecometrics have stronger predictive power at continental than at global scales, but without a single, dominant predictive functional relationship. Application of ecometrics to the Shungura fossil record suggests that turtle paleocommunity ecometrics coarsely track independent paleoclimate estimates at local scales. We hypothesize that both human disruption and biotic interactions limit the ecometric fit of size to climate in this clade. Nonetheless, examination of the consistency of trait-environment relationships through deep and shallow time provides a means for testing anthropogenic influences on ecosystems.

hox gene expression predicts tetrapod-like axial regionalization in the skate, Leucoraja erinacea.

The axial skeleton of tetrapods is organized into distinct anteroposterior regions of the vertebral column (cervical, trunk, sacral, and caudal), and transitions between these regions are determined by colinear anterior expression boundaries of Hox5/6, -9, -10, and -11 paralogy group genes within embryonic paraxial mesoderm. Fishes, conversely, exhibit little in the way of discrete axial regionalization, and this has led to scenarios of an origin of Hox-mediated axial skeletal complexity with the evolutionary transition to land in tetrapods. Here, combining geometric morphometric analysis of vertebral column morphology with cell lineage tracing of hox gene expression boundaries in developing embryos, we recover evidence of at least five distinct regions in the vertebral skeleton of a cartilaginous fish, the little skate (Leucoraja erinacea). We find that skate embryos exhibit tetrapod-like anteroposterior nesting of hox gene expression in their paraxial mesoderm, and we show that anterior expression boundaries of hox5/6, hox9, hox10, and hox11 paralogy group genes predict regional transitions in the differentiated skate axial skeleton. Our findings suggest that hox-based axial skeletal regionalization did not originate with tetrapods but rather has a much deeper evolutionary history than was previously appreciated.

Squamate reptiles from Kanapoi: Faunal evidence for hominin paleoenvironments.

The squamate fossil record from Kanapoi reveals generic to higher-order similarities with modern East African herpetofaunas. The record is derived from surface collection and screen washing, and consists primarily of isolated vertebrae with a few maxillary and mandibular elements. The most abundant remains are vertebrae of large-bodied Python that are morphologically similar to extant Python sebae, and vertebrae of Varanus cf. (Varanus niloticus + Varanus exanthematicus). Additional cranial and vertebral remains indicate the presence of lygosomine skinks, indeterminate Varanus, Viperidae, cf. Atractaspididae, and multiple colubrine morphotypes in the Kanapoi ecosystem. Despite similarities with modern herpetofaunas, the Kanapoi record lacks taxa common to other East African records, including agamids, chamaeleonids, amphisbaenians, the elapid Naja, and typhlopids. The overall composition of the Kanapoi squamate record is consistent with paleoenvironments similar to modern shrub savanna habitats. There are no indicators of canopied forest environments in squamate faunal composition. The fossil record of Kanapoi suggests that assembly of squamate faunas of modern East Africa was well underway by the late Neogene.

Pectoral myology of limb-reduced worm lizards (Squamata, Amphisbaenia) suggests decoupling of the musculoskeletal system during the evolution of body elongation.

BACKGROUND: The evolution of elongated body forms in tetrapods has a strong influence on the musculoskeletal system, including the reduction of pelvic and pectoral girdles, as well as the limbs. However, despite extensive research in this area it still remains unknown how muscles within and around bony girdles are affected by these reductions. Here we investigate this issue using fossorial amphisbaenian reptiles, or worm lizards, as a model system, which show substantial variation in the degree of reductions of girdles and limbs. Using iodine-based contrast-enhanced computed tomography (diceCT), we analyze the composition of the shoulder muscles of the main clades of Amphisbaenia and their outgroups relative to the pectoral skeleton. RESULTS: All investigated amphisbaenian taxa retain the full set of 17 shoulder muscles, independent of the degree of limb and girdle reductions, whereas in some cases muscles are fused to complexes or changed in morphology relative to the ancestral condition. Bipes is the only taxon that retains forelimbs and an almost complete pectoral girdle. All other amphisbaenian families show more variation concerning the completeness of the pectoral girdle having reduced or absent girdle elements. Rhineura, which undergoes the most severe bone reductions, differs from all other taxa in possessing elongated muscle strands instead of discrete shoulder muscles. In all investigated amphisbaenians, the shoulder muscle agglomerate is shortened and shifted anteriorly relative to the ancestral position as seen in the outgroups. CONCLUSIONS: Our results show that pectoral muscle anatomy does not necessarily correspond to the loss or reduction of bones, indicating a decoupling of the musculoskeletal system. Muscle attachment sites change from bones to non-skeletal areas, such as surrounding muscles, skin or connective tissue, whereas muscle origins themselves remain in the same region where the pectoral bones were ancestrally located. Our findings indicate a high degree of developmental autonomy within the musculoskeletal system, we predict that the observed evolutionary rearrangements of amphisbaenian shoulder muscles were driven by functional demands rather than by developmental constraints. Nevertheless, worm lizards display a spatial offset of both pectoral bones and muscles relative to the ancestral position, indicating severe developmental modifications of the amphisbaenian body axis.

Merging paleobiology with conservation biology to guide the future of terrestrial ecosystems.

Conservation of species and ecosystems is increasingly difficult because anthropogenic impacts are pervasive and accelerating. Under this rapid global change, maximizing conservation success requires a paradigm shift from maintaining ecosystems in idealized past states toward facilitating their adaptive and functional capacities, even as species ebb and flow individually. Developing effective strategies under this new paradigm will require deeper understanding of the long-term dynamics that govern ecosystem persistence and reconciliation of conflicts among approaches to conserving historical versus novel ecosystems. Integrating emerging information from conservation biology, paleobiology, and the Earth sciences is an important step forward on the path to success. Maintaining nature in all its aspects will also entail immediately addressing the overarching threats of growing human population, overconsumption, pollution, and climate change.

A new Late Cretaceous iguanomorph from North America and the origin of New World Pleurodonta (Squamata, Iguania).

Iguanomorpha (stem + crown Iguania) is a diverse squamate clade with members that predominate many modern American lizard ecosystems. However, the temporal and palaeobiogeographic origins of its constituent crown clades (e.g. Pleurodonta (basilisks, iguanas, and their relatives)) are poorly constrained, mainly due to a meagre Mesozoic-age fossil record. Here, we report on two nearly complete skeletons from the Late Cretaceous (Campanian) of North America that represent a new and relatively large-bodied and possibly herbivorous iguanomorph that inhabited a semi-arid environment. The new taxon exhibits a mosaic of anatomical features traditionally used in diagnosing Iguania and non-iguanian squamates (i.e. Scleroglossa; e.g. parietal foramen at the frontoparietal suture, astragalocalcaneal notch in the tibia, respectively). Our cladistic analysis of Squamata revealed a phylogenetic link between Campanian-age North American and East Asian stem iguanomorphs (i.e. the new taxon + Temujiniidae). These results and our evaluation of the squamate fossil record suggest that crown pleurodontans were restricted to the low-latitude Neotropics prior to their early Palaeogene first appearances in the mid-latitudes of North America.

The Fossil Calibration Database-A New Resource for Divergence Dating.

Fossils provide the principal basis for temporal calibrations, which are critical to the accuracy of divergence dating analyses. Translating fossil data into minimum and maximum bounds for calibrations is the most important-often least appreciated-step of divergence dating. Properly justified calibrations require the synthesis of phylogenetic, paleontological, and geological evidence and can be difficult for nonspecialists to formulate. The dynamic nature of the fossil record (e.g., new discoveries, taxonomic revisions, updates of global or local stratigraphy) requires that calibration data be updated continually lest they become obsolete. Here, we announce the Fossil Calibration Database (http://fossilcalibrations.org), a new open-access resource providing vetted fossil calibrations to the scientific community. Calibrations accessioned into this database are based on individual fossil specimens and follow best practices for phylogenetic justification and geochronological constraint. The associated Fossil Calibration Series, a calibration-themed publication series at Palaeontologia Electronica, will serve as a key pipeline for peer-reviewed calibrations to enter the database.

Evolution of the snake body form reveals homoplasy in amniote Hox gene function.

Hox genes regulate regionalization of the axial skeleton in vertebrates, and changes in their expression have been proposed to be a fundamental mechanism driving the evolution of new body forms. The origin of the snake-like body form, with its deregionalized pre-cloacal axial skeleton, has been explained as either homogenization of Hox gene expression domains, or retention of standard vertebrate Hox domains with alteration of downstream expression that suppresses development of distinct regions. Both models assume a highly regionalized ancestor, but the extent of deregionalization of the primaxial domain (vertebrae, dorsal ribs) of the skeleton in snake-like body forms has never been analysed. Here we combine geometric morphometrics and maximum-likelihood analysis to show that the pre-cloacal primaxial domain of elongate, limb-reduced lizards and snakes is not deregionalized compared with limbed taxa, and that the phylogenetic structure of primaxial morphology in reptiles does not support a loss of regionalization in the evolution of snakes. We demonstrate that morphometric regional boundaries correspond to mapped gene expression domains in snakes, suggesting that their primaxial domain is patterned by a normally functional Hox code. Comparison of primaxial osteology in fossil and modern amniotes with Hox gene distributions within Amniota indicates that a functional, sequentially expressed Hox code patterned a subtle morphological gradient along the anterior-posterior axis in stem members of amniote clades and extant lizards, including snakes. The highly regionalized skeletons of extant archosaurs and mammals result from independent evolution in the Hox code and do not represent ancestral conditions for clades with snake-like body forms. The developmental origin of snakes is best explained by decoupling of the primaxial and abaxial domains and by increases in somite number, not by changes in the function of primaxial Hox genes.

Unusual soft-tissue preservation of a crocodile lizard (Squamata, Shinisauria) from the green river formation (Eocene) and shinisaur relationships.

We describe an unusual squamate fossil from the Green River Formation (Uintan, Eocene) from the Piceance Creek Basin, Colorado, USA. The new specimen, USNM PAL 540708, is a small fossil squamate skin lacking skeletal elements. It is preserved as a part and counterpart in fine-grained limestone. Recovery of a fossil organism's skin (not a shed, but a true skin) is unusual and is most often accompanied by bone preservation. Phylogenetic analysis of a combined morphology (phenotype) and genetic data set reveals that USNM PAL 540708 is a shinisaur and reaffirms that shinisaurs are more closely related to varanids than to Xenosaurus. Shinisaur fossils are very rare, with only three species having been described (Dalinghosaurus longidigitus, Bahndwivici ammoskius, and Merkurosaurus ornatus). Despite differences in the relative size of scales, the new fossil demonstrates that shinisaurs have remained unchanged in the distribution of scales and patterns of scale size during the Cenozoic. This, paired with the osteological similarity between another Green River fossil (Bahndwivici ammoskius) demonstrates considerable overall conservatism within shinisaurs over the past 50 million years.

Giant lizards occupied herbivorous mammalian ecospace during the Paleogene greenhouse in Southeast Asia.

Mammals dominate modern terrestrial herbivore ecosystems, whereas extant herbivorous reptiles are limited in diversity and body size. The evolution of reptile herbivory and its relationship to mammalian diversification is poorly understood with respect to climate and the roles of predation pressure and competition for food resources. Here, we describe a giant fossil acrodontan lizard recovered with a diverse mammal assemblage from the late middle Eocene Pondaung Formation of Myanmar, which provides a historical test of factors controlling body size in herbivorous squamates. We infer a predominately herbivorous feeding ecology for the new acrodontan based on dental anatomy, phylogenetic relationships and body size. Ranking body masses for Pondaung Formation vertebrates indicates that the lizard occupied a size niche among the larger herbivores and was larger than most carnivorous mammals. Paleotemperature estimates of Pondaung Formation environments based on the body size of the new lizard are approximately 2-5°C higher than modern. These results indicate that competitive exclusion and predation by mammals did not restrict body size evolution in these herbivorous squamates, and elevated temperatures relative to modern climates during the Paleogene greenhouse may have resulted in the evolution of gigantism through elevated poikilothermic metabolic rates and in response to increases in floral productivity.

Synthesizing and databasing fossilcalibrations: divergencedating and beyond

Divergence dating studies, which combine temporal data from the fossil record with branch length data from molecular phylogenetic trees, represent a rapidly expanding approach to understanding the history of life. National Evolutionary Synthesis Center hosted the first Fossil Calibrations Working Group (3–6 March, 2011, Durham, NC, USA), bringing together palaeontologists, molecular evolutionists and bioinformatics experts to present perspectives from disciplines that generate, model and use fossil calibration data. Presentations and discussions focused on channels for interdisciplinary collaboration, best practices for justifying, reporting and using fossil calibrations and roadblocks to synthesis of palaeontological and molecular data. Bioinformatics solutions were proposed, with the primary objective being a new database for vetted fossil calibrations with linkages to existing resources, targeted for a 2012 launch.

Eocene lizard from Germany reveals amphisbaenian origins.

Amphisbaenia is a speciose clade of fossorial lizards characterized by a snake-like body and a strongly reinforced skull adapted for head-first burrowing. The evolutionary origins of amphisbaenians are controversial, with molecular data uniting them with lacertids, a clade of Old World terrestrial lizards, whereas morphology supports a grouping with snakes and other limbless squamates. Reports of fossil stem amphisbaenians have been falsified, and no fossils have previously tested these competing phylogenetic hypotheses or shed light on ancestral amphisbaenian ecology. Here we report the discovery of a new lacertid-like lizard from the Eocene Messel locality of Germany that provides the first morphological evidence for lacertid-amphisbaenian monophyly on the basis of a reinforced, akinetic skull roof and braincase, supporting the view that body elongation and limblessness in amphisbaenians and snakes evolved independently. Morphometric analysis of body shape and ecology in squamates indicates that the postcranial anatomy of the new taxon is most consistent with opportunistically burrowing habits, which in combination with cranial reinforcement indicates that head-first burrowing evolved before body elongation and may have been a crucial first step in the evolution of amphisbaenian fossoriality.

Synthesizing and databasing fossil calibrations: divergence dating and beyond.

Divergence dating studies, which combine temporal data from the fossil record with branch length data from molecular phylogenetic trees, represent a rapidly expanding approach to understanding the history of life. National Evolutionary Synthesis Center hosted the first Fossil Calibrations Working Group (3-6 March, 2011, Durham, NC, USA), bringing together palaeontologists, molecular evolutionists and bioinformatics experts to present perspectives from disciplines that generate, model and use fossil calibration data. Presentations and discussions focused on channels for interdisciplinary collaboration, best practices for justifying, reporting and using fossil calibrations and roadblocks to synthesis of palaeontological and molecular data. Bioinformatics solutions were proposed, with the primary objective being a new database for vetted fossil calibrations with linkages to existing resources, targeted for a 2012 launch.

Phylogeny and divergence times of filesnakes (Acrochordus): inferences from morphology, fossils and three molecular loci.

Acrochordus is a species-poor but highly distinctive aquatic snake genus currently distributed from India to the western edge of the Pacific. We provide the first phylogeny for the three extant species using Bayesian and parsimony analyses of one mitochondrial and two nuclear gene sequences. Acrochordus javanicus is strongly recovered as sister to A. arafurae+A. granulatus, counter to expectations from superficial ecology, external phenotype and former taxonomy. We review and revise key fossil calibrations for dating snake divergences. Bayesian relaxed-clock analysis of the two nuclear loci yields deep interspecific divergences among extant species that occurred during the Miocene approximately 16 and approximately 20Mya (million years ago), pre-dating at least two of the three other living marine snake lineages. New morphological data for A. arafurae, and our molecular timescale, provide support for the placement of fossil taxon A. dehmi within the Acrochordus crown group, as sister to A. javanicus among nominate species. Finally, Acrochordus phylogeny provides an improved basis for taxon selection and character polarization in higher snake phylogenetics. Our study highlights the three Acrochordus species as old and highly distinct lineages that comprise an important component of the threatened Indo-Australian biodiversity.

Predation upon hatchling dinosaurs by a new snake from the late Cretaceous of India.

Derived large-mouthed snakes (macrostomatans) possess numerous specializations in their skull and lower jaws that allow them to consume large vertebrate prey. In contrast, basal snakes lack these adaptations and feed primarily on small prey items. The sequence of osteological and behavioral modifications involved in the evolution of the macrostomatan condition has remained an open question because of disagreement about the origin and interrelationships of snakes, the paucity of well-preserved early snake fossils on many continental landmasses, and the lack of information about the feeding ecology of early snakes. We report on a partial skeleton of a new 3.5-m-long snake, Sanajeh indicus gen. et sp. nov., recovered from Upper Cretaceous rocks of western India. S. indicus was fossilized in association with a sauropod dinosaur egg clutch, coiled around an egg and adjacent to the remains of a ca. 0.5-m-long hatchling. Multiple snake-egg associations at the site strongly suggest that S. indicus frequented nesting grounds and preyed on hatchling sauropods. We interpret this pattern as "ethofossil" preservation of feeding behavior. S. indicus lacks specializations of modern egg-eaters and of macrostomatans, and skull and vertebral synapomorphies place it in an intermediate position in snake phylogeny. Sanajeh and its large-bodied madtsoiid sister taxa Yurlunggur camfieldensis and Wonambi naracoortensis from the Neogene of Australia show specializations for intraoral prey transport but lack the adaptations for wide gape that characterize living macrostomatan snakes. The Dholi Dungri fossils are the second definitive association between sauropod eggs and embryonic or hatchling remains. New fossils from western India provide direct evidence of feeding ecology in a Mesozoic snake and demonstrate predation risks for hatchling sauropod dinosaurs. Our results suggest that large body size and jaw mobility afforded some non-macrostomatan snakes a greater diversity of prey items than previously suspected on the basis of extant basal snakes.

Homeotic effects, somitogenesis and the evolution of vertebral numbers in recent and fossil amniotes.

The development of distinct regions in the amniote vertebral column results from somite formation and Hox gene expression, with the adult morphology displaying remarkable variation among lineages. Mammalian regionalization is reportedly very conservative or even constrained, but there has been no study investigating vertebral count variation across Amniota as a whole, undermining attempts to understand the phylogenetic, ecological, and developmental factors affecting vertebral column variation. Here, we show that the mammalian (synapsid) and reptilian lineages show early in their evolutionary histories clear divergences in axial developmental plasticity, in terms of both regionalization and meristic change, with basal synapsids sharing the conserved axial configuration of crown mammals, and basal reptiles demonstrating the plasticity of extant taxa. We conducted a comprehensive survey of presacral vertebral counts across 436 recent and extinct amniote taxa. Vertebral counts were mapped onto a generalized amniote phylogeny as well as individual ingroup trees, and ancestral states were reconstructed by using squared-change parsimony. We also calculated the relationship between presacral and cervical numbers to infer the relative influence of homeotic effects and meristic changes and found no correlation between somitogenesis and Hox-mediated regionalization. Although conservatism in presacral numbers characterized early synapsid lineages, in some cases reptiles and synapsids exhibit the same developmental innovations in response to similar selective pressures. Conversely, increases in body mass are not coupled with meristic or homeotic changes, but mostly occur in concert with postembryonic somatic growth. Our study highlights the importance of fossils in large-scale investigations of evolutionary developmental processes.

Giant boid snake from the Palaeocene neotropics reveals hotter past equatorial temperatures.

The largest extant snakes live in the tropics of South America and southeast Asia where high temperatures facilitate the evolution of large body sizes among air-breathing animals whose body temperatures are dependant on ambient environmental temperatures (poikilothermy). Very little is known about ancient tropical terrestrial ecosystems, limiting our understanding of the evolution of giant snakes and their relationship to climate in the past. Here we describe a boid snake from the oldest known neotropical rainforest fauna from the Cerrejón Formation (58-60 Myr ago) in northeastern Colombia. We estimate a body length of 13 m and a mass of 1,135 kg, making it the largest known snake. The maximum size of poikilothermic animals at a given temperature is limited by metabolic rate, and a snake of this size would require a minimum mean annual temperature of 30-34 degrees C to survive. This estimate is consistent with hypotheses of hot Palaeocene neotropics with high concentrations of atmospheric CO(2) based on climate models. Comparison of palaeotemperature estimates from the equator to those from South American mid-latitudes indicates a relatively steep temperature gradient during the early Palaeogene greenhouse, similar to that of today. Depositional environments and faunal composition of the Cerrejón Formation indicate an anaconda-like ecology for the giant snake, and an earliest Cenozoic origin of neotropical vertebrate faunas.