Post-extinction recovery of the Phanerozoic oceans and biodiversity hotspots.

The fossil record of marine invertebrates has long fuelled the debate as to whether or not there are limits to global diversity in the sea1-5. Ecological theory states that, as diversity grows and ecological niches are filled, the strengthening of biological interactions imposes limits on diversity6,7. However, the extent to which biological interactions have constrained the growth of diversity over evolutionary time remains an open question1-5,8-11. Here we present a regional diversification model that reproduces the main Phanerozoic eon trends in the global diversity of marine invertebrates after imposing mass extinctions. We find that the dynamics of global diversity are best described by a diversification model that operates widely within the exponential growth regime of a logistic function. A spatially resolved analysis of the ratio of diversity to carrying capacity reveals that less than 2% of the global flooded continental area throughout the Phanerozoic exhibits diversity levels approaching ecological saturation. We attribute the overall increase in global diversity during the Late Mesozoic and Cenozoic eras to the development of diversity hotspots under prolonged conditions of Earth system stability and maximum continental fragmentation. We call this the 'diversity hotspots hypothesis', which we propose as a non-mutually exclusive alternative to the hypothesis that the Mesozoic marine revolution led this macroevolutionary trend12,13.

150 million years of sustained increase in pterosaur flight efficiency.

The long-term accumulation of biodiversity has been punctuated by remarkable evolutionary transitions that allowed organisms to exploit new ecological opportunities. Mesozoic flying reptiles (the pterosaurs), which dominated the skies for more than 150 million years, were the product of one such transition. The ancestors of pterosaurs were small and probably bipedal early archosaurs1, which were certainly well-adapted to terrestrial locomotion. Pterosaurs diverged from dinosaur ancestors in the Early Triassic epoch (around 245 million years ago); however, the first fossils of pterosaurs are dated to 25 million years later, in the Late Triassic epoch. Therefore, in the absence of proto-pterosaur fossils, it is difficult to study how flight first evolved in this group. Here we describe the evolutionary dynamics of the adaptation of pterosaurs to a new method of locomotion. The earliest known pterosaurs took flight and subsequently appear to have become capable and efficient flyers. However, it seems clear that transitioning between forms of locomotion2,3-from terrestrial to volant-challenged early pterosaurs by imposing a high energetic burden, thus requiring flight to provide some offsetting fitness benefits. Using phylogenetic statistical methods and biophysical models combined with information from the fossil record, we detect an evolutionary signal of natural selection that acted to increase flight efficiency over millions of years. Our results show that there was still considerable room for improvement in terms of efficiency after the appearance of flight. However, in the Azhdarchoidea4, a clade that exhibits gigantism, we test the hypothesis that there was a decreased reliance on flight5-7 and find evidence for reduced selection on flight efficiency in this clade. Our approach offers a blueprint to objectively study functional and energetic changes through geological time at a more nuanced level than has previously been possible.

Allometric wing growth links parental care to pterosaur giantism.

Pterosaurs evolved a broad range of body sizes, from small-bodied early forms with wingspans of mostly 1-2 m to the last-surviving giants with sizes of small airplanes. Since all pterosaurs began life as small hatchlings, giant forms must have attained large adult sizes through new growth strategies, which remain largely unknown. Here we assess wing ontogeny and performance in the giant Pteranodon and the smaller-bodied anurognathids Rhamphorhynchus, Pterodactylus and Sinopterus. We show that most smaller-bodied pterosaurs shared negative allometry or isometry in the proximal elements of the fore- and hindlimbs, which were critical elements for powering both flight and terrestrial locomotion, whereas these show positive allometry in Pteranodon. Such divergent growth allometry typically signals different strategies in the precocial-altricial spectrum, suggesting more altricial development in Pteranodon. Using a biophysical model of powered and gliding flight, we test and reject the hypothesis that an aerodynamically superior wing planform could have enabled Pteranodon to attain its larger body size. We therefore propose that a shift from a plesiomorphic precocial state towards a derived state of enhanced parental care may have relaxed the constraints of small body sizes and allowed the evolution of derived flight anatomies critical for the flying giants.

The Angiosperm Terrestrial Revolution and the origins of modern biodiversity.

Biodiversity today has the unusual property that 85% of plant and animal species live on land rather than in the sea, and half of these live in tropical rainforests. An explosive boost to terrestrial diversity occurred from c. 100-50 million years ago, the Late Cretaceous and early Palaeogene. During this interval, the Earth-life system on land was reset, and the biosphere expanded to a new level of productivity, enhancing the capacity and species diversity of terrestrial environments. This boost in terrestrial biodiversity coincided with innovations in flowering plant biology and evolutionary ecology, including their flowers and efficiencies in reproduction; coevolution with animals, especially pollinators and herbivores; photosynthetic capacities; adaptability; and ability to modify habitats. The rise of angiosperms triggered a macroecological revolution on land and drove modern biodiversity in a secular, prolonged shift to new, high levels, a series of processes we name here the Angiosperm Terrestrial Revolution.

Dietary niche partitioning in Early Jurassic ichthyosaurs from Strawberry Bank.

Jurassic ichthyosaurs dominated upper trophic levels of marine ecosystems. Many species coexisted alongside each another, and it is uncertain whether they competed for the same array of food or divided dietary resources, each specializing in different kinds of prey. Here, we test whether feeding differences existed between species, applying finite element analysis to ichthyosaurs for the first time. We examine two juvenile ichthyosaur specimens, referred to Hauffiopteryx typicus and Stenopterygius triscissus, from the Strawberry Bank Lagerstätte, a shallow marine environment from the Early Jurassic of southern England (Toarcian, ~183 Ma). Snout and cranial robusticity differ between the species, with S. triscissus having a more robust snout and cranium and specializing in slow biting of hard prey, and H. typicus with its slender snout specializing in fast, but weaker bites on fast-moving, but soft prey. The two species did not differ in muscle forces, but stress distributions varied in the nasal area, reflecting differences when biting at different points along the tooth row: the more robustly snouted Stenopterygius resisted increases or shifts in stress distribution when the bite point was shifted from the posterior to the mid-point of the tooth row, but the slender-snouted Hauffiopteryx showed shifts and increases in stress distributions between these two bite points. The differences in cranial morphology, dentition and inferred stresses between the two species suggest adaptations for dietary niche partitioning.

Ecological dynamics of terrestrial and freshwater ecosystems across three mid-Phanerozoic mass extinctions from northwest China.

The Earth has been beset by many crises during its history, and yet comparing the ecological impacts of these mass extinctions has been difficult. Key questions concern the kinds of species that go extinct and survive, how communities rebuild in the post-extinction recovery phase, and especially how the scaling of events affects these processes. Here, we explore ecological impacts of terrestrial and freshwater ecosystems in three mass extinctions through the mid-Phanerozoic, a span of 121 million years (295-174 Ma). This critical duration encompasses the largest mass extinction of all time, the Permian-Triassic (P-Tr) and is flanked by two smaller crises, the Guadalupian-Lopingian (G-L) and Triassic-Jurassic (T-J) mass extinctions. Palaeocommunity dynamics modelling of 14 terrestrial and freshwater communities through a long sedimentary succession from the lower Permian to the lower Jurassic in northern Xinjiang, northwest China, shows that the P-Tr mass extinction differed from the other two in two ways: (i) ecological recovery from this extinction was prolonged and the three post-extinction communities in the Early Triassic showed low stability and highly variable and unpredictable responses to perturbation primarily following the huge losses of species, guilds and trophic space; and (ii) the G-L and T-J extinctions were each preceded by low-stability communities, but post-extinction recovery was rapid. Our results confirm the uniqueness of the P-Tr mass extinction and shed light on the trophic structure and ecological dynamics of terrestrial and freshwater ecosystems across the three mid-Phanerozoic extinctions, and how complex communities respond to environmental stress and how communities recovered after the crisis. Comparisons with the coeval communities from the Karoo Basin, South Africa show that geographically and compositionally different communities of terrestrial ecosystems were affected in much the same way by the P-Tr extinction.

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.

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.

Effects of body plan evolution on the hydrodynamic drag and energy requirements of swimming in ichthyosaurs.

Ichthyosaurs are an extinct group of fully marine tetrapods that were well adapted to aquatic locomotion. During their approximately 160 Myr existence, they evolved from elongate and serpentine forms into stockier, fish-like animals, convergent with sharks and dolphins. Here, we use computational fluid dynamics (CFD) to quantify the impact of this transition on the energy demands of ichthyosaur swimming for the first time. We run computational simulations of water flow using three-dimensional digital models of nine ichthyosaurs and an extant functional analogue, a bottlenose dolphin, providing the first quantitative evaluation of ichthyosaur hydrodynamics across phylogeny. Our results show that morphology did not have a major effect on the drag coefficient or the energy cost of steady swimming through geological time. We show that even the early ichthyosaurs produced low levels of drag for a given volume, comparable to those of a modern dolphin, and that deep 'torpedo-shaped' bodies did not reduce the cost of locomotion. Our analysis also provides important insight into the choice of scaling parameters for CFD applied to swimming mechanics, and underlines the great influence of body size evolution on ichthyosaur locomotion. A combination of large bodies and efficient swimming modes lowered the cost of steady swimming as ichthyosaurs became increasingly adapted to a pelagic existence.

Origins of Biodiversity.

Biodiversity today is huge, and it has a long history. Identifying rules for the heterogeneity of modern biodiversity-the high to low species richness of different clades-has been hard. There are measurable biodiversity differences between land and sea and between the tropics and temperate-polar regions. Some analyses suggest that the net age of a clade can determine its extinction risk, but this is equivocal. New work shows that, through geological time, clades pass through different diversification regimes, and those regimes constrain the balance of tree size and the nature of branching events.

Dinosaurs in decline tens of millions of years before their final extinction.

Whether dinosaurs were in a long-term decline or whether they were reigning strong right up to their final disappearance at the Cretaceous-Paleogene (K-Pg) mass extinction event 66 Mya has been debated for decades with no clear resolution. The dispute has continued unresolved because of a lack of statistical rigor and appropriate evolutionary framework. Here, for the first time to our knowledge, we apply a Bayesian phylogenetic approach to model the evolutionary dynamics of speciation and extinction through time in Mesozoic dinosaurs, properly taking account of previously ignored statistical violations. We find overwhelming support for a long-term decline across all dinosaurs and within all three dinosaurian subclades (Ornithischia, Sauropodomorpha, and Theropoda), where speciation rate slowed down through time and was ultimately exceeded by extinction rate tens of millions of years before the K-Pg boundary. The only exceptions to this general pattern are the morphologically specialized herbivores, the Hadrosauriformes and Ceratopsidae, which show rapid species proliferations throughout the Late Cretaceous instead. Our results highlight that, despite some heterogeneity in speciation dynamics, dinosaurs showed a marked reduction in their ability to replace extinct species with new ones, making them vulnerable to extinction and unable to respond quickly to and recover from the final catastrophic event.

Belowground rhizomes in paleosols: The hidden half of an Early Devonian vascular plant.

The colonization of terrestrial environments by rooted vascular plants had far-reaching impacts on the Earth system. However, the belowground structures of early vascular plants are rarely documented, and thus the plant-soil interactions in early terrestrial ecosystems are poorly understood. Here we report the earliest rooted paleosols (fossil soils) in Asia from Early Devonian deposits of Yunnan, China. Plant traces are extensive within the soil and occur as complex network-like structures, which are interpreted as representing long-lived, belowground rhizomes of the basal lycopsid Drepanophycus The rhizomes produced large clones and helped the plant survive frequent sediment burial in well-drained soils within a seasonal wet-dry climate zone. Rhizome networks contributed to the accumulation and pedogenesis of floodplain sediments and increased the soil stabilizing effects of early plants. Predating the appearance of trees with deep roots in the Middle Devonian, plant rhizomes have long functioned in the belowground soil ecosystem. This study presents strong, direct evidence for plant-soil interactions at an early stage of vascular plant radiation. Soil stabilization by complex rhizome systems was apparently widespread, and contributed to landscape modification at an earlier time than had been appreciated.

Tetrapod distribution and temperature rise during the Permian-Triassic mass extinction.

The Permian-Triassic mass extinction (PTME) had an enormous impact on life in three ways: by substantially reducing diversity, by reshuffling the composition of ecosystems and by expelling life from the tropics following episodes of intense global warming. But was there really an 'equatorial tetrapod gap', and how long did it last? Here, we consider both skeletal and footprint data, and find a more complex pattern: (i) tetrapods were distributed both at high and low latitudes during this time; (ii) there was a clear geographic disjunction through the PTME, with tetrapod distribution shifting 10-15° poleward; and (iii) there was a rapid expansion phase across the whole of Pangea following the PTME. These changes are consistent with a model of generalized migration of tetrapods to higher latitudinal, cooler regions, to escape from the superhot equatorial climate in the earliest Triassic, but the effect was shorter in time scale, and not as pronounced as had been proposed. In the recovery phase following the PTME, this episode of forced range expansion also appears to have promoted the emergence and radiation of entirely new groups, such as the archosaurs, including the dinosaurs.

Hyperthermal-driven mass extinctions: killing models during the Permian-Triassic mass extinction.

Many mass extinctions of life in the sea and on land have been attributed to geologically rapid heating, and in the case of the Permian-Triassic and others, driven by large igneous province volcanism. The Siberian Traps eruptions raised ambient temperatures to 35-40°C. A key question is how massive eruptions during these events, and others, could have killed life in the sea and on land; proposed killers are reviewed here. In the oceans, benthos and plankton were killed by anoxia-euxinia and lethal heating, respectively, and the habitable depth zone was massively reduced. On land, the combination of extreme heating and drought reduced the habitable land area, and acid rain stripped forests and soils. Physiological experiments show that some animals can adapt to temperature rises of a few degrees, and that some can survive short episodes of increases of 10°C. However, most plants and animals suffer major physiological damage at temperatures of 35-40°C. Studies of the effects of extreme physical conditions on modern organisms, as well as assumptions about rates of environmental change, give direct evidence of likely killing effects deriving from hyperthermals of the past.This article is part of a discussion meeting issue 'Hyperthermals: rapid and extreme global warming in our geological past'.

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.

Fossilized melanosomes and the colour of Cretaceous dinosaurs and birds.

Spectacular fossils from the Early Cretaceous Jehol Group of northeastern China have greatly expanded our knowledge of the diversity and palaeobiology of dinosaurs and early birds, and contributed to our understanding of the origin of birds, of flight, and of feathers. Pennaceous (vaned) feathers and integumentary filaments are preserved in birds and non-avian theropod dinosaurs, but little is known of their microstructure. Here we report that melanosomes (colour-bearing organelles) are not only preserved in the pennaceous feathers of early birds, but also in an identical manner in integumentary filaments of non-avian dinosaurs, thus refuting recent claims that the filaments are partially decayed dermal collagen fibres. Examples of both eumelanosomes and phaeomelanosomes have been identified, and they are often preserved in life position within the structure of partially degraded feathers and filaments. Furthermore, the data here provide empirical evidence for reconstructing the colours and colour patterning of these extinct birds and theropod dinosaurs: for example, the dark-coloured stripes on the tail of the theropod dinosaur Sinosauropteryx can reasonably be inferred to have exhibited chestnut to reddish-brown tones.

Exploring macroevolution using modern and fossil data.

Macroevolution, encompassing the deep-time patterns of the origins of modern biodiversity, has been discussed in many contexts. Non-Darwinian models such as macromutations have been proposed as a means of bridging seemingly large gaps in knowledge, or as a means to explain the origin of exquisitely adapted body plans. However, such gaps can be spanned by new fossil finds, and complex, integrated organisms can be shown to have evolved piecemeal. For example, the fossil record between dinosaurs and Archaeopteryx has now filled up with astonishing fossil intermediates that show how the unique plexus of avian adaptations emerged step by step over 60 Myr. New numerical approaches to morphometrics and phylogenetic comparative methods allow palaeontologists and biologists to work together on deep-time questions of evolution, to explore how diversity, morphology and function have changed through time. Patterns are more complex than sometimes expected, with frequent decoupling of species diversity and morphological diversity, pointing to the need for some new generalizations about the processes that lie behind such patterns.

Functional anatomy and feeding biomechanics of a giant Upper Jurassic pliosaur (Reptilia: Sauropterygia) from Weymouth Bay, Dorset, UK.

Pliosaurs were among the largest predators in Mesozoic seas, and yet their functional anatomy and feeding biomechanics are poorly understood. A new, well-preserved pliosaur from the Kimmeridgian of Weymouth Bay (UK) revealed cranial adaptations related to feeding. Digital modelling of computed tomography scans allowed reconstruction of missing, distorted regions of the skull and of the adductor musculature, which indicated high bite forces. Size-corrected beam theory modelling showed that the snout was poorly optimised against bending and torsional stresses compared with other aquatic and terrestrial predators, suggesting that pliosaurs did not twist or shake their prey during feeding and that seizing was better performed with post-symphyseal bites. Finite element analysis identified biting-induced stress patterns in both the rostrum and lower jaws, highlighting weak areas in the rostral maxillary-premaxillary contact and the caudal mandibular symphysis. A comparatively weak skull coupled with musculature that was able to produce high forces, is explained as a trade-off between agility, hydrodynamics and strength. In the Kimmeridgian ecosystem, we conclude that Late Jurassic pliosaurs were generalist predators at the top of the food chain, able to prey on reptiles and fishes up to half their own length.