Locomotion and the early Mesozoic success of Archosauromorpha.

The Triassic was a time of ecological upheaval as life recovered from the Permian-Triassic mass extinction. Archosauromorphs were a key component of the recovery, diversifying substantially during the Triassic and encompassing the origins of dinosaurs, pterosaurs and crocodylomorphs. Here, we explore the evolution of locomotion in Archosauromorpha to test whether dinosaurs show any distinctive locomotory features that might explain their success. We implement geometric morphometrics on limb bone shapes and use limb ratios to calculate bipedality and cursoriality metrics. We find that the Avemetatarsalia (dinosaurs, pterosaurs and relatives) exhibit more variable limb form and limb ratios than any other group, indicating a wider range of locomotory modes. The earliest avemetatarsalians were bipedal and cursorial, and their range of form increased through the Triassic with notable diversification shifts following extinction events. This is especially true of dinosaurs, even though these changes cannot be discriminated from a stochastic process. By contrast, the Pseudosuchia (crocodilians and relatives) were more restricted in limb form and locomotor mode with disparity decreasing through time, suggesting more limited locomotor adaptation and vulnerability to extinction. Perhaps the greater locomotor plasticity of dinosaurs gave them a competitive advantage in the changing climates of the Late Triassic.

Predatory synapsid ecomorphology signals growing dynamism of late Palaeozoic terrestrial ecosystems.

Terrestrial ecosystems evolved substantially through the Palaeozoic, especially the Permian, gaining much new complexity, especially among predators. Key among these predators were non-mammalian synapsids. Predator ecomorphology reflect interactions with prey and competitors, which are key controls on carnivore diversity and ecology. Therefore, carnivorous synapsids may offer insight on wider ecological evolution as the first complex, tetrapod-dominated, terrestrial ecosystems formed through the late Palaeozoic. Using morphometric and phylogenetic comparative methods, we chart carnivorous synapsid trophic morphology from the latest Carboniferous to the earliest Triassic (307-251.2 Ma). We find a major morphofunctional shift in synapsid carnivory between the early and middle Permian, via the addition of new feeding modes increasingly specialised for greater biting power or speed that captures the growing antagonism and dynamism of terrestrial tetrapod predator-prey interactions. The further evolution of new hypo- and hypercarnivorous synapsids highlight the nascent intrinsic pressures and complexification of terrestrial ecosystems across the mid-late Permian.

High phenotypic plasticity at the dawn of the eosauropterygian radiation.

The initial radiation of Eosauropterygia during the Triassic biotic recovery represents a key event in the dominance of reptiles secondarily adapted to marine environments. Recent studies on Mesozoic marine reptile disparity highlighted that eosauropterygians had their greatest morphological diversity during the Middle Triassic, with the co-occurrence of Pachypleurosauroidea, Nothosauroidea and Pistosauroidea, mostly along the margins of the Tethys Ocean. However, these previous studies quantitatively analysed the disparity of Eosauropterygia as a whole without focussing on Triassic taxa, thus limiting our understanding of their diversification and morphospace occupation during the Middle Triassic. Our multivariate morphometric analyses highlight a clearly distinct colonization of the ecomorphospace by the three clades, with no evidence of whole-body convergent evolution with the exception of the peculiar pistosauroid Wangosaurus brevirostris, which appears phenotypically much more similar to nothosauroids. This global pattern is mostly driven by craniodental differences and inferred feeding specializations. We also reveal noticeable regional differences among nothosauroids and pachypleurosauroids of which the latter likely experienced a remarkable diversification in the eastern Tethys during the Pelsonian. Our results demonstrate that the high phenotypic plasticity characterizing the evolution of the pelagic plesiosaurians was already present in their Triassic ancestors, casting eosauropterygians as particularly adaptable animals.

Rapid neck elongation in Sauropterygia (Reptilia: Diapsida) revealed by a new basal pachypleurosaur from the Lower Triassic of China.

Neck elongation has appeared independently in several tetrapod groups, including giraffes and sauropod dinosaurs on land, birds and pterosaurs in the air, and sauropterygians (plesiosaurs and relatives) in the oceans. Long necks arose in Early Triassic sauropterygians, but the nature and rate of that elongation has not been documented. Here, we report a new species of pachypleurosaurid sauropterygian, Chusaurus xiangensis gen. et sp. nov., based on two new specimens from the Early Triassic Nanzhang-Yuan'an Fauna in the South China Block. The new species shows key features of its Middle Triassic relatives, but has a relatively short neck, measuring 0.48 of the trunk length, compared to > 0.8 from the Middle Triassic onwards. Comparative phylogenetic analysis shows that neck elongation occurred rapidly in all Triassic eosauropterygian lineages, probably driven by feeding pressure in a time of rapid re-establishment of new kinds of marine ecosystems.

A Highly Diverse Olenekian Brachiopod Fauna from the Nanpanjiang Basin, South China, and Its Implications for the Early Triassic Biotic Recovery.

As one of the predominant benthic organisms in the Palaeozoic, brachiopod was largely eliminated in the Permian-Triassic boundary mass extinction, and then highly diversified in the Middle Triassic. Since fossil data from the Early Triassic are rarely reported, the recovery patterns of Early Triassic brachiopods remain unclear. This study documents a well-preserved fauna that is the most diverse Olenekian brachiopod fauna so far (age constrained by conodont biostratigraphy) from the Datuguan section of ramp facies in South China. This fauna is composed of 14 species within nine genera, including six genera (Hirsutella, Sulcatinella, Paradoxothyris, Dioristella, Neoretzia and Isocrania) found in the Early Triassic for the first time and three new species, including Paradoxothyris flatus sp. nov., Hirsutella sulcata sp. nov. and Sulcatinella elongata sp. nov. The Datuguan fauna indicates that the diversity of Olenekian brachiopod fauna has been underestimated, which can be caused by a combination of reduced habitats (in geographic size and sedimentary type) compared with the end-Permian, great bed thickness making it difficult to find fossils and most species in the fauna having low abundance. Based on the faunal change in the Datuguan section and environmental changes in South China, it can be inferred that brachiopod recovery in the studied section occurred in the latest Spathian rather than the Smithian when the environment started to ameliorate. Global brachiopod data also indicates that the initial recovery of brachiopods happened in the Spathian, and many genera that widely occurred in the Middle or Late Triassic had originated in the Olenekian.

The Jurassic rise of squamates as supported by lepidosaur disparity and evolutionary rates.

The squamates (lizards, snakes, and relatives) today comprise more than 10,000 species, and yet their sister group, the Rhynchocephalia, is represented by a single species today, the tuatara. The explosion in squamate diversity has been tracked back to the Cretaceous Terrestrial Revolution, 100 million years ago (Ma), the time when flowering plants began their takeover of terrestrial ecosystems, associated with diversification of coevolving insects and insect-eating predators such as lizards, birds, and mammals. Squamates arose much earlier, but their long pre-Cretaceous history of some 150 million years (Myr) is documented by sparse fossils. Here, we provide evidence for an initial radiation of squamate morphology in the Middle and Late Jurassic (174-145 Ma), and show that they established their key ecological roles much earlier than had been assumed, and they have not changed them much since.

Large size in aquatic tetrapods compensates for high drag caused by extreme body proportions.

Various Mesozoic marine reptile lineages evolved streamlined bodies and efficient lift-based swimming, as seen in modern aquatic mammals. Ichthyosaurs had low-drag bodies, akin to modern dolphins, but plesiosaurs were strikingly different, with long hydrofoil-like limbs and greatly variable neck and trunk proportions. Using computational fluid dynamics, we explore the effect of this extreme morphological variation. We find that, independently of their body fineness ratio, plesiosaurs produced more drag than ichthyosaurs and modern cetaceans of equal mass due to their large limbs, but these differences were not significant when body size was accounted for. Additionally, necks longer than twice the trunk length can substantially increase the cost of forward swimming, but this effect was cancelled out by the evolution of big trunks. Moreover, fast rates in the evolution of neck proportions in the long-necked elasmosaurs suggest that large trunks might have released the hydrodynamic constraints on necks thus allowing their extreme enlargement.

Niche partitioning shaped herbivore macroevolution through the early Mesozoic.

The Triassic (252-201 Ma) marks a major punctuation in Earth history, when ecosystems rebuilt themselves following the devastating Permian-Triassic mass extinction. Herbivory evolved independently several times as ecosystems comprising diverse assemblages of therapsids, parareptiles and archosauromorphs rose and fell, leading to a world dominated by dinosaurs. It was assumed that dinosaurs prevailed either through long-term competitive replacement of the incumbent clades or rapidly and opportunistically following one or more extinction events. Here we use functional morphology and ecology to explore herbivore morphospace through the Triassic and Early Jurassic. We identify five main herbivore guilds (ingestion generalists, prehension specialists, durophagous specialists, shearing pulpers, and heavy oral processors), and find that herbivore clades generally avoided competition by almost exclusively occupying different guilds. Major ecosystem remodelling was triggered multiple times by external environmental challenges, and previously dominant herbivores were marginalised by newly emerging forms. Dinosaur dominance was a mix of opportunity following disaster, combined with competitive advantage in their new world.

Ecomorphological diversification of squamates in the Cretaceous.

Squamates (lizards and snakes) are highly successful modern vertebrates, with over 10 000 species. Squamates have a long history, dating back to at least 240 million years ago (Ma), and showing increasing species richness in the Late Cretaceous (84 Ma) and Early Palaeogene (66-55 Ma). We confirm that the major expansion of dietary functional morphology happened before these diversifications, in the mid-Cretaceous, 110-90 Ma. Until that time, squamates had relatively uniform tooth types, which then diversified substantially and ecomorphospace expanded to modern levels. This coincides with the Cretaceous Terrestrial Revolution, when angiosperms began to take over terrestrial ecosystems, providing new roles for plant-eating and pollinating insects, which were, in turn, new sources of food for herbivorous and insectivorous squamates. There was also an early Late Cretaceous (95-90 Ma) rise in jaw size disparity, driven by the diversification of marine squamates, particularly early mosasaurs. These events established modern levels of squamate feeding ecomorphology before the major steps in species diversification, confirming decoupling of diversity and disparity. In fact, squamate feeding ecomorphospace had been partially explored in the Late Jurassic and Early Cretaceous, and jaw innovation in Late Cretaceous squamates involved expansions at the extremes of morphospace.

Ecological opportunity and the rise and fall of crocodylomorph evolutionary innovation.

Understanding the origin, expansion and loss of biodiversity is fundamental to evolutionary biology. The approximately 26 living species of crocodylomorphs (crocodiles, caimans, alligators and gharials) represent just a snapshot of the group's rich 230-million-year history, whereas the fossil record reveals a hidden past of great diversity and innovation, including ocean and land-dwelling forms, herbivores, omnivores and apex predators. In this macroevolutionary study of skull and jaw shape disparity, we show that crocodylomorph ecomorphological variation peaked in the Cretaceous, before declining in the Cenozoic, and the rise and fall of disparity was associated with great heterogeneity in evolutionary rates. Taxonomically diverse and ecologically divergent Mesozoic crocodylomorphs, like marine thalattosuchians and terrestrial notosuchians, rapidly evolved novel skull and jaw morphologies to fill specialized adaptive zones. Disparity in semi-aquatic predatory crocodylians, the only living crocodylomorph representatives, accumulated steadily, and they evolved more slowly for most of the last 80 million years, but despite their conservatism there is no evidence for long-term evolutionary stagnation. These complex evolutionary dynamics reflect ecological opportunities, that were readily exploited by some Mesozoic crocodylomorphs but more limited in Cenozoic crocodylians.

Ontogenetic endocranial shape change in alligators and ostriches and implications for the development of the non-avian dinosaur endocranium.

Birds and crocodiles show radically different patterns of brain development, and it is of interest to compare these to determine the pattern of brain growth expected in dinosaurs. Here we provide atlases of 3D brain (endocast) reconstructions for Alligator mississippiensis (alligator) and Struthio camelus (ostrich) through ontogeny, prepared as digital restorations from CT scans of stained head and dry skull specimens. Our morphometric analysis confirms that ostrich brains do not change significantly in shape during postnatal growth, whereas alligator brains unfold from a cramped bird-like shape in the hatchling to an elongate, straight structure in the adult. We confirm that birds exhibit paedomorphic dinosaur endocranial traits such as retaining an enlarged and compact brain shape in the adult, whereas crocodiles show peramorphic traits where the brain elongates with growth as the skull elongates. These atlases of ontogenetic stages of modern bird and crocodilian endocrania provide a basis for comparison of non-avian dinosaur endocasts and consideration of the divergence of the "avian" and "crocodilian" modes of brain development and heterochronic change on phylogenies.

Morphological convergence obscures functional diversity in sabre-toothed carnivores.

The acquisition of elongated, sabre-like canines in multiple vertebrate clades during the last 265 Myr represents a remarkable example for convergent evolution. Due to striking superficial similarities in the cranial skeleton, the same or similar skull and jaw functions have been inferred for sabre-toothed species and interpreted as an adaptation to subdue large-bodied prey. However, although some sabre-tooth lineages have been classified into different ecomorphs (dirk-tooths and scimitar-tooths) the functional diversity within and between groups and the evolutionary paths leading to these specializations are unknown. Here, we use a suite of biomechanical simulations to analyse key functional parameters (mandibular gape angle, bending strength, bite force) to compare the functional performance of different groups and to quantify evolutionary rates across sabre-tooth vertebrates. Our results demonstrate a remarkably high functional diversity between sabre-tooth lineages and that different cranial function and prey killing strategies evolved within clades. Moreover, different biomechanical adaptations in coexisting sabre-tooth species further suggest that this functional diversity was at least partially driven by niche partitioning.

Early high rates and disparity in the evolution of ichthyosaurs.

How clades diversify early in their history is integral to understanding the origins of biodiversity and ecosystem recovery following mass extinctions. Moreover, diversification can represent evolutionary opportunities and pressures following ecosystem changes. Ichthyosaurs, Mesozoic marine reptiles, appeared after the end-Permian mass extinction and provide opportunities to assess clade diversification in a changed world. Using recent cladistic data, skull length data, and the most complete phylogenetic trees to date for the group, we present a combined disparity, morphospace, and evolutionary rates analysis that reveals the tempo and mode of ichthyosaur morphological evolution through 160 million years. Ichthyosaur evolution shows an archetypal early burst trend, driven by ecological opportunity in Triassic seas, and an evolutionary bottleneck leading to a long-term reduction in evolutionary rates and disparity. This is represented consistently across all analytical methods by a Triassic peak in ichthyosaur disparity and evolutionary rates, and morphospace separation between Triassic and post-Triassic taxa.

Does exceptional preservation distort our view of disparity in the fossil record?

How much of evolutionary history is lost because of the unevenness of the fossil record? Lagerstätten, sites which have historically yielded exceptionally preserved fossils, provide remarkable, yet distorting insights into past life. When examining macroevolutionary trends in the fossil record, they can generate an uneven sampling signal for taxonomic diversity; by comparison, their effect on morphological variety (disparity) is poorly understood. We show here that lagerstätten impact the disparity of ichthyosaurs, Mesozoic marine reptiles, by preserving higher diversity and more complete specimens. Elsewhere in the fossil record, undersampled diversity and more fragmentary specimens produce spurious results. We identify a novel effect, that a taxon moves towards the centroid of a Generalized Euclidean dataset as its proportion of missing data increases. We term this effect 'centroid slippage', as a disparity-based analogue of phylogenetic stemward slippage. Our results suggest that uneven sampling presents issues for our view of disparity in the fossil record, but that this is also dependent on the methodology used, especially true with widely used Generalized Euclidean distances. Mitigation of missing cladistic data is possible by phylogenetic gap filling, and heterogeneous effects of lagerstätten on disparity may be accounted for by understanding the factors affecting their spatio-temporal distribution.

Melanosome diversity and convergence in the evolution of iridescent avian feathers-Implications for paleocolor reconstruction.

Some of the most varied colors in the natural world are created by iridescent nanostructures in bird feathers, formed by layers of melanin-containing melanosomes. The morphology of melanosomes in iridescent feathers is known to vary, but the extent of this diversity, and when it evolved, is unknown. We use scanning electron microscopy to quantify the diversity of melanosome morphology in iridescent feathers from 97 extant bird species, covering 11 orders. In addition, we assess melanosome morphology in two Eocene birds, which are the stem lineages of groups that respectively exhibit hollow and flat melanosomes today. We find that iridescent feathers contain the most varied melanosome morphologies of all types of bird coloration sampled to date. Using our extended dataset, we predict iridescence in an early Eocene trogon (cf. Primotrogon) but not in the early Eocene swift Scaniacypselus, and neither exhibit the derived melanosome morphologies seen in their modern relatives. Our findings confirm that iridescence is a labile trait that has evolved convergently in several lineages extending down to paravian theropods. The dataset provides a framework to detect iridescence with more confidence in fossil taxa based on melanosome morphology.

The long-term ecology and evolution of marine reptiles in a Jurassic seaway.

Marine reptiles flourished in the Mesozoic oceans, filling ecological roles today dominated by crocodylians, large fish, sharks and cetaceans. Many groups of these reptiles coexisted for over 50 million years (Myr), through major environmental changes. However, little is known about how the structure of their ecosystems or their ecologies changed over millions of years. We use the most common marine reptile fossils-teeth-to establish a quantitative system that assigns species to dietary guilds and then track the evolution of these guilds over the roughly 18-million-year history of a single seaway, the Jurassic Sub-Boreal Seaway of the United Kingdom. Groups did not significantly overlap in guild space, indicating that dietary niche partitioning enabled many species to live together. Although a highly diverse fauna was present throughout the history of the seaway, fish and squid eaters with piercing teeth declined over time while hard-object and large-prey specialists diversified, in concert with rising sea levels. High niche partitioning and spatial variation in dietary ecology related to sea depth also characterize modern marine tetrapod faunas, indicating a conserved ecological structure of the world's oceans that has persisted for over 150 Myr.

Morphometric assessment of pterosaur jaw disparity.

Pterosaurs were a successful group of Mesozoic flying reptiles. They were the first vertebrate group to achieve powered flight and varied enormously in morphology and ecology, occupying a variety of niches and developing specialized feeding strategies. Ecomorphological principles suggest this variation should be reflected by great morphological diversity in the lower jaw, given that the mandible served as the primary apparatus for prey acquisition. Here we present the first study of mandibular shape disparity in pterosaurs and aim to characterize major aspects of variation. We use a combination of geometric morphometric approaches, incorporating both outline analysis using elliptical Fourier analysis and semi-landmark approaches. Our results show that morphological convergence is prevalent and many pterosaurs, belonging to diverse dietary groups and subclades, overlap in morphospace and possessed relatively simple 'rod-shaped' jaws. There is no clear trend of size distributions in pterosaur mandibular morphospace, and larger forms are widely distributed. Additionally, there is limited functional signal within pterosaur lower jaw morphospace. Instead, the development of a large anterior ventral crest represents the major component of disparity. This suggests that a socio-sexual trait was a key driver for innovation in pterosaur lower jaw shape.

Phanerozoic survivors: Actinopterygian evolution through the Permo-Triassic and Triassic-Jurassic mass extinction events.

Actinopterygians (ray-finned fishes) successfully passed through four of the big five mass extinction events of the Phanerozoic, but the effects of these crises on the group are poorly understood. Many researchers have assumed that the Permo-Triassic mass extinction (PTME) and end-Triassic extinction (ETE) had little impact on actinopterygians, despite devastating many other groups. Here, two morphometric techniques, geometric (body shape) and functional (jaw morphology), are used to assess the effects of these two extinction events on the group. The PTME elicits no significant shifts in functional disparity while body shape disparity increases. An expansion of body shape and functional disparity coincides with the neopterygian radiation and evolution of novel feeding adaptations in the Middle-Late Triassic. Through the ETE, small decreases are seen in shape and functional disparity, but are unlikely to represent major changes brought about by the extinction event. In the Early Jurassic, further expansions into novel areas of ecospace indicative of durophagy occur, potentially linked to losses in the ETE. As no evidence is found for major perturbations in actinopterygian evolution through either extinction event, the group appears to have been immune to two major environmental crises that were disastrous to most other organisms.