Publications by authors named "Mark A Norell"

67 Publications

Decelerated dinosaur skull evolution with the origin of birds.

PLoS Biol 2020 08 18;18(8):e3000801. Epub 2020 Aug 18.

Life Sciences Department, Vertebrates Division, Natural History Museum, London, United Kingdom.

The evolutionary radiation of birds has produced incredible morphological variation, including a huge range of skull form and function. Investigating how this variation arose with respect to non-avian dinosaurs is key to understanding how birds achieved their remarkable success after the Cretaceous-Paleogene extinction event. Using a high-dimensional geometric morphometric approach, we quantified the shape of the skull in unprecedented detail across 354 extant and 37 extinct avian and non-avian dinosaurs. Comparative analyses reveal fundamental differences in how skull shape evolved in birds and non-avian dinosaurs. We find that the overall skull shape evolved faster in non-avian dinosaurs than in birds across all regions of the cranium. In birds, the anterior rostrum is the most rapidly evolving skull region, whereas more posterior regions-such as the parietal, squamosal, and quadrate-exhibited high rates in non-avian dinosaurs. These fast-evolving elements in dinosaurs are strongly associated with feeding biomechanics, forming the jaw joint and supporting the jaw adductor muscles. Rapid pulses of skull evolution coincide with changes to food acquisition strategies and diets, as well as the proliferation of bony skull ornaments. In contrast to the appendicular skeleton, which has been shown to evolve more rapidly in birds, avian cranial morphology is characterised by a striking deceleration in morphological evolution relative to non-avian dinosaurs. These results may be due to the reorganisation of skull structure in birds-including loss of a separate postorbital bone in adults and the emergence of new trade-offs with development and neurosensory demands. Taken together, the remarkable cranial shape diversity in birds was not a product of accelerated evolution from their non-avian relatives, despite their frequent portrayal as an icon of adaptive radiations.
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http://dx.doi.org/10.1371/journal.pbio.3000801DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7437466PMC
August 2020

Potential for Powered Flight Neared by Most Close Avialan Relatives, but Few Crossed Its Thresholds.

Curr Biol 2020 Oct 6;30(20):4033-4046.e8. Epub 2020 Aug 6.

Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology & Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China.

Uncertainties in the phylogeny of birds (Avialae) and their closest relatives have impeded deeper understanding of early theropod flight. To help address this, we produced an updated evolutionary hypothesis through an automated analysis of the Theropod Working Group (TWiG) coelurosaurian phylogenetic data matrix. Our larger, more resolved, and better-evaluated TWiG-based hypothesis supports the grouping of dromaeosaurids + troodontids (Deinonychosauria) as the sister taxon to birds (Paraves) and the recovery of Anchiornithinae as the earliest diverging birds. Although the phylogeny will continue developing, our current results provide a pertinent opportunity to evaluate what we know about early theropod flight. With our results and available data for vaned feathered pennaraptorans, we estimate the potential for powered flight among early birds and their closest relatives. We did this by using an ancestral state reconstruction analysis calculating maximum and minimum estimates of two proxies of powered flight potential-wing loading and specific lift. These results confirm powered flight potential in early birds but its rarity among the ancestors of the closest avialan relatives (select unenlagiine and microraptorine dromaeosaurids). For the first time, we find a broad range of these ancestors neared the wing loading and specific lift thresholds indicative of powered flight potential. This suggests there was greater experimentation with wing-assisted locomotion before theropod flight evolved than previously appreciated. This study adds invaluable support for multiple origins of powered flight potential in theropods (≥3 times), which we now know was from ancestors already nearing associated thresholds, and provides a framework for its further study. VIDEO ABSTRACT.
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http://dx.doi.org/10.1016/j.cub.2020.06.105DOI Listing
October 2020

Modularity and heterochrony in the evolution of the ceratopsian dinosaur frill.

Ecol Evol 2020 Jul 22;10(13):6288-6309. Epub 2020 May 22.

Integrative Research Center Field Museum of Natural History Chicago IL USA.

The fossil record provides compelling examples of heterochrony at macroevolutionary scales such as the peramorphic giant antlers of the Irish elk. Heterochrony has also been invoked in the evolution of the distinctive cranial frill of ceratopsian dinosaurs such as . Although ceratopsian frills vary in size, shape, and ornamentation, quantitative analyses that would allow for testing hypotheses of heterochrony are lacking. Here, we use geometric morphometrics to examine frill shape variation across ceratopsian diversity and within four species preserving growth series. We then test whether the frill constitutes an evolvable module both across and within species, and compare growth trajectories of taxa with ontogenetic growth series to identify heterochronic processes. Evolution of the ceratopsian frill consisted primarily of progressive expansion of its caudal and caudolateral margins, with morphospace occupation following taxonomic groups. Although taphonomic distortion represents a complicating factor, our data support modularity both across and within species. Peramorphosis played an important role in frill evolution, with acceleration operating early in neoceratopsian evolution followed by progenesis in later diverging cornosaurian ceratopsians. Peramorphic evolution of the ceratopsian frill may have been facilitated by the decoupling of this structure from the jaw musculature, an inference that predicts an expansion of morphospace occupation and higher evolutionary rates among ceratopsids as indeed borne out by our data. However, denser sampling of the meager record of early-diverging taxa is required to test this further.
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http://dx.doi.org/10.1002/ece3.6361DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7381594PMC
July 2020

The first dinosaur egg was soft.

Nature 2020 07 17;583(7816):406-410. Epub 2020 Jun 17.

Department of Geoscience, University of Calgary, Calgary, Alberta, Canada.

Calcified eggshells protect developing embryos against environmental stress and contribute to reproductive success. As modern crocodilians and birds lay hard-shelled eggs, this eggshell type has been inferred for non-avian dinosaurs. Known dinosaur eggshells are characterized by an innermost membrane, an overlying protein matrix containing calcite, and an outermost waxy cuticle. The calcitic eggshell consists of one or more ultrastructural layers that differ markedly among the three major dinosaur clades, as do the configurations of respiratory pores. So far, only hadrosaurid, a few sauropodomorph and tetanuran eggshells have been discovered; the paucity of the fossil record and the lack of intermediate eggshell types challenge efforts to homologize eggshell structures across all dinosaurs. Here we present mineralogical, organochemical and ultrastructural evidence for an originally non-biomineralized, soft-shelled nature of exceptionally preserved ornithischian Protoceratops and basal sauropodomorph Mussaurus eggs. Statistical evaluation of in situ Raman spectra obtained for a representative set of hard- and soft-shelled, fossil and extant diapsid eggshells clusters the originally organic but secondarily phosphatized Protoceratops and the organic Mussaurus eggshells with soft, non-biomineralized eggshells. Histology corroborates the organic composition of these soft-shelled dinosaur eggs, revealing a stratified arrangement resembling turtle soft eggshell. Through an ancestral-state reconstruction of composition and ultrastructure, we compare eggshells from Protoceratops and Mussaurus with those from other diapsids, revealing that the first dinosaur egg was soft-shelled. The calcified, hard-shelled dinosaur egg evolved independently at least three times throughout the Mesozoic era, explaining the bias towards eggshells of derived dinosaurs in the fossil record.
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http://dx.doi.org/10.1038/s41586-020-2412-8DOI Listing
July 2020

Tempo and Pattern of Avian Brain Size Evolution.

Curr Biol 2020 Jun 23;30(11):2026-2036.e3. Epub 2020 Apr 23.

Department of Anthropology, Stony Brook University, Stony Brook, NY 11794, USA; Division of Anthropology, American Museum of Natural History, New York, NY 10024, USA.

Relative brain sizes in birds can rival those of primates, but large-scale patterns and drivers of avian brain evolution remain elusive. Here, we explore the evolution of the fundamental brain-body scaling relationship across the origin and evolution of birds. Using a comprehensive dataset sampling> 2,000 modern birds, fossil birds, and theropod dinosaurs, we infer patterns of brain-body co-variation in deep time. Our study confirms that no significant increase in relative brain size accompanied the trend toward miniaturization or evolution of flight during the theropod-bird transition. Critically, however, theropods and basal birds show weaker integration between brain size and body size, allowing for rapid changes in the brain-body relationship that set the stage for dramatic shifts in early crown birds. We infer that major shifts occurred rapidly in the aftermath of the Cretaceous-Paleogene mass extinction within Neoaves, in which multiple clades achieved higher relative brain sizes because of a reduction in body size. Parrots and corvids achieved the largest brains observed in birds via markedly different patterns. Parrots primarily reduced their body size, whereas corvids increased body and brain size simultaneously (with rates of brain size evolution outpacing rates of body size evolution). Collectively, these patterns suggest that an early adaptive radiation in brain size laid the foundation for subsequent selection and stabilization.
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http://dx.doi.org/10.1016/j.cub.2020.03.060DOI Listing
June 2020

Estimating Flight Style of Early Eocene Stem Palaeognath Bird Calciavis grandei (Lithornithidae).

Anat Rec (Hoboken) 2020 04 16;303(4):1035-1042. Epub 2019 Jul 16.

Department of Integrative Biology, University of Texas at Austin, Austin, Texas.

Lithornithids are volant stem palaeognaths from the Paleocene-Eocene. Except for these taxa and the extant neotropical tinamous, all other known extinct and extant palaeognaths are flightless. Investigation of properties of the lithornithid wing and its implications for inference of flight style informs understood locomotor diversity within Palaeognathae and may have implications for estimation of ancestral traits in the clade. Qualitative comparisons with their closest extant volant relatives, the burst-flying tinamous, previously revealed skeletal differences suggesting lithornithids were capable of sustained flight, but quantitative work on wing morphology have been lacking. Until comparatively recently, specimens of lithornithids preserving wing feather remains have been limited. Here, we reconstruct the wing of an exceptionally preserved specimen of the Early Eocene lithornithid Calciavis grandei and estimate body mass, wing surface area, and wing span. We then estimate flight parameters and compare our estimates with representatives from across Aves in a statistical framework. We predict that flight in C. grandei was likely marked by continuous flapping, and that lithornithids were capable of sustained flight and migratory behavior. Our results are consistent with previous hypotheses that the ancestor of extant Palaeognathae may also have been capable of sustained flight. Anat Rec, 303:1035-1042, 2020. © 2019 Wiley Periodicals, Inc.
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http://dx.doi.org/10.1002/ar.24207DOI Listing
April 2020

Reply to: Egg pigmentation probably has an Archosaurian origin.

Nature 2019 06 19;570(7761):E46-E50. Epub 2019 Jun 19.

Division of Paleontology, American Museum of Natural History, New York, NY, USA.

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http://dx.doi.org/10.1038/s41586-019-1283-3DOI Listing
June 2019

Cretaceous dinosaur bone contains recent organic material and provides an environment conducive to microbial communities.

Elife 2019 06 18;8. Epub 2019 Jun 18.

Department of Geosciences, Princeton University, Princeton, United States.

Fossils were thought to lack original organic molecules, but chemical analyses show that some can survive. Dinosaur bone has been proposed to preserve collagen, osteocytes, and blood vessels. However, proteins and labile lipids are diagenetically unstable, and bone is a porous open system, allowing microbial/molecular flux. These 'soft tissues' have been reinterpreted as biofilms. Organic preservation versus contamination of dinosaur bone was examined by freshly excavating, with aseptic protocols, fossils and sedimentary matrix, and chemically/biologically analyzing them. Fossil 'soft tissues' differed from collagen chemically and structurally; while degradation would be expected, the patterns observed did not support this. 16S rRNA amplicon sequencing revealed that dinosaur bone hosted an abundant microbial community different from lesser abundant communities of surrounding sediment. Subsurface dinosaur bone is a relatively fertile habitat, attracting microbes that likely utilize inorganic nutrients and complicate identification of original organic material. There exists potential post-burial taphonomic roles for subsurface microorganisms.
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http://dx.doi.org/10.7554/eLife.46205DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6581507PMC
June 2019

Evolutionary Integration and Modularity in the Archosaur Cranium.

Integr Comp Biol 2019 08;59(2):371-382

Life Sciences Department, Vertebrates Division, Natural History Museum, London, SW7 5BD, UK.

Complex structures, like the vertebrate skull, are composed of numerous elements or traits that must develop and evolve in a coordinated manner to achieve multiple functions. The strength of association among phenotypic traits (i.e., integration), and their organization into highly-correlated, semi-independent subunits termed modules, is a result of the pleiotropic and genetic correlations that generate traits. As such, patterns of integration and modularity are thought to be key factors constraining or facilitating the evolution of phenotypic disparity by influencing the patterns of variation upon which selection can act. It is often hypothesized that selection can reshape patterns of integration, parceling single structures into multiple modules or merging ancestrally semi-independent traits into a strongly correlated unit. However, evolutionary shifts in patterns of trait integration are seldom assessed in a unified quantitative framework. Here, we quantify patterns of evolutionary integration among regions of the archosaur skull to investigate whether patterns of cranial integration are conserved or variable across this diverse group. Using high-dimensional geometric morphometric data from 3D surface scans and computed tomography scans of modern birds (n = 352), fossil non-avian dinosaurs (n = 27), and modern and fossil mesoeucrocodylians (n = 38), we demonstrate that some aspects of cranial integration are conserved across these taxonomic groups, despite their major differences in cranial form, function, and development. All three groups are highly modular and consistently exhibit high integration within the occipital region. However, there are also substantial divergences in correlation patterns. Birds uniquely exhibit high correlation between the pterygoid and quadrate, components of the cranial kinesis apparatus, whereas the non-avian dinosaur quadrate is more closely associated with the jugal and quadratojugal. Mesoeucrocodylians exhibit a slightly more integrated facial skeleton overall than the other grades. Overall, patterns of trait integration are shown to be stable among archosaurs, which is surprising given the cranial diversity exhibited by the clade. At the same time, evolutionary innovations such as cranial kinesis that reorganize the structure and function of complex traits can result in modifications of trait correlations and modularity.
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http://dx.doi.org/10.1093/icb/icz052DOI Listing
August 2019

Are endocasts good proxies for brain size and shape in archosaurs throughout ontogeny?

J Anat 2019 03 3;234(3):291-305. Epub 2018 Dec 3.

Division of Paleontology, American Museum of Natural History, New York, NY, USA.

Cranial endocasts, or the internal molds of the braincase, are a crucial correlate for investigating the neuroanatomy of extinct vertebrates and tracking brain evolution through deep time. Nevertheless, the validity of such studies pivots on the reliability of endocasts as a proxy for brain morphology. Here, we employ micro-computed tomography imaging, including diffusible iodine-based contrast-enhanced CT, and a three-dimensional geometric morphometric framework to examine both size and shape differences between brains and endocasts of two exemplar archosaur taxa - the American alligator (Alligator mississippiensis) and the domestic chicken (Gallus gallus). With ontogenetic sampling, we quantitatively evaluate how endocasts differ from brains and whether this deviation changes during development. We find strong size and shape correlations between brains and endocasts, divergent ontogenetic trends in the brain-to-endocast correspondence between alligators and chickens, and a comparable magnitude between brain-endocast shape differences and intraspecific neuroanatomical variation. The results have important implications for paleoneurological studies in archosaurs. Notably, we demonstrate that the pattern of endocranial shape variation closely reflects brain shape variation. Therefore, analyses of endocranial morphology are unlikely to generate spurious conclusions about large-scale trends in brain size and shape. To mitigate any artifacts, however, paleoneurological studies should consider the lower brain-endocast correspondence in the hindbrain relative to the forebrain; higher size and shape correspondences in chickens than alligators throughout postnatal ontogeny; artificially 'pedomorphic' shape of endocasts relative to their corresponding brains; and potential biases in both size and shape data due to the lack of control for ontogenetic stages in endocranial sampling.
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http://dx.doi.org/10.1111/joa.12918DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6365484PMC
March 2019

Dinosaur egg colour had a single evolutionary origin.

Nature 2018 11 31;563(7732):555-558. Epub 2018 Oct 31.

Division of Vertebrate Paleontology, American Museum of Natural History, New York, NY, USA.

Birds are the only living amniotes with coloured eggs, which have long been considered to be an avian innovation. A recent study has demonstrated the presence of both red-brown protoporphyrin IX and blue-green biliverdin-the pigments responsible for all the variation in avian egg colour-in fossilized eggshell of a nonavian dinosaur. This raises the fundamental question of whether modern birds inherited egg colour from their nonavian dinosaur ancestors, or whether egg colour evolved independently multiple times. Here we present a phylogenetic assessment of egg colour in nonavian dinosaurs. We applied high-resolution Raman microspectroscopy to eggshells that represent all of the major clades of dinosaurs, and found that egg colour pigments were preserved in all eumaniraptorans: egg colour had a single evolutionary origin in nonavian theropod dinosaurs. The absence of colour in ornithischian and sauropod eggs represents a true signal rather than a taphonomic artefact. Pigment surface maps revealed that nonavian eumaniraptoran eggs were spotted and speckled, and colour pattern diversity in these eggs approaches that in extant birds, which indicates that reproductive behaviours in nonavian dinosaurs were far more complex than previously known. Depth profiles demonstrated identical mechanisms of pigment deposition in nonavian and avian dinosaur eggs. Birds were not the first amniotes to produce coloured eggs: as with many other characteristics this is an attribute that evolved deep within the dinosaur tree and long before the spectacular radiation of modern birds.
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http://dx.doi.org/10.1038/s41586-018-0646-5DOI Listing
November 2018

Fossilization transforms vertebrate hard tissue proteins into N-heterocyclic polymers.

Nat Commun 2018 11 9;9(1):4741. Epub 2018 Nov 9.

Department of Geology & Geophysics, Yale University, 210 Whitney Avenue, New Haven, CT, 06511, USA.

Vertebrate hard tissues consist of mineral crystallites within a proteinaceous scaffold that normally degrades post-mortem. Here we show, however, that decalcification of Mesozoic hard tissues preserved in oxidative settings releases brownish stained extracellular matrix, cells, blood vessels, and nerve projections. Raman Microspectroscopy shows that these fossil soft tissues are a product of diagenetic transformation to Advanced Glycoxidation and Lipoxidation End Products, a class of N-heterocyclic polymers generated via oxidative crosslinking of proteinaceous scaffolds. Hard tissues in reducing environments, in contrast, lack soft tissue preservation. Comparison of fossil soft tissues with modern and experimentally matured samples reveals how proteinaceous tissues undergo diagenesis and explains biases in their preservation in the rock record. This provides a target, focused on oxidative depositional environments, for finding cellular-to-subcellular soft tissue morphology in fossils and validates its use in phylogenetic and other evolutionary studies.
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http://dx.doi.org/10.1038/s41467-018-07013-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6226439PMC
November 2018

The Endocranial Cavity of Oviraptorosaur Dinosaurs and the Increasingly Complex, Deep History of the Avian Brain.

Brain Behav Evol 2018 10;91(3):125-135. Epub 2018 Aug 10.

Center for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

Unraveling the origins of the character complexes diagnosing major crown clades is one of the greatest challenges in evolutionary biology. These origination events tend to optimize along extraordinarily long stem lineages where the comparative biology of extant lineages is relatively weak in its heuristic power. Here we add to a growing paleontological literature on the evolutionary origins of the modern avi an brain by describing the endocranial casts of two oviraptorosaur dinosaurs, Citipati osmolskae and Khaan mckennai. These fossil data confirm the antiquity of several avian features, including the expanded cerebrum. They also extend our appreciation of both the inherent variability in the brain-skull relationship along the avian stem and the dynamic nature of these crown characters in the earliest history of their expression.
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http://dx.doi.org/10.1159/000488890DOI Listing
April 2019

Rapid F-FDG Uptake in Brain of Awake, Behaving Rat and Anesthetized Chicken has Implications for Behavioral PET Studies in Species With High Metabolisms.

Front Behav Neurosci 2018 5;12:115. Epub 2018 Jun 5.

Department of Psychology, Yeditepe University, Istanbul, Turkey.

Brain-behavior studies using F-FDG PET aim to reveal brain regions that become active during behavior. In standard protocols, F-FDG is injected, the behavior is executed during 30-60 min of tracer uptake, and then the animal is anesthetized and scanned. Hence, the uptake of F-FDG is not itself observed and could, in fact, be complete in very little time. This has implications for behavioral studies because uptake is assumed to reflect concurrent behavior. Here, we utilized a new, miniature PET scanner termed RatCAP to measure uptake simultaneously with behavior. We employed a novel injection protocol in which we administered F-FDG (i.v.) four times over two 2 h to allow for repeated measurements and the correlation of changes in uptake and behavioral activity. Furthermore, using standard PET methods, we explored the effects of injection route on uptake time in chickens, a model for avians, for which PET studies are just beginning. We found that in the awake, behaving rat most of the F-FDG uptake occurred within minutes and overlapped to a large extent with F-FDG data taken from longer uptake periods. By contrast, behavior which occurred within minutes of the F-FDG infusion differed markedly from the behavior that occurred during later uptake periods. Accordingly, we found that changes in F-FDG uptake in the striatum, motor cortex and cerebellum relative to different reference regions significantly predicted changes in behavioral activity during the scan, if the time bins used for correlation were near the injection times of F-FDG. However, when morphine was also injected during the scan, which completely abolished behavioral activity for over 50 min, a large proportion of the variance in behavioral activity was also explained by the uptake data from the entire scan. In anesthetized chickens, tracer uptake was complete in about 80 min with s.c. injection, but 8 min with i.v. injection. In conclusion, uptake time needs to be taken into account to more accurately correlate PET and behavioral data in mammals and avians. Additionally, RatCAP together with multiple, successive injections of F-FDG may be useful to explore changes in uptake over time in relation to changes in behavior.
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http://dx.doi.org/10.3389/fnbeh.2018.00115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5996747PMC
June 2018

Dome-headed, small-brained island mammal from the Late Cretaceous of Romania.

Proc Natl Acad Sci U S A 2018 05 23;115(19):4857-4862. Epub 2018 Apr 23.

Division of Paleontology, American Museum of Natural History, New York, NY 10024.

The island effect is a well-known evolutionary phenomenon, in which island-dwelling species isolated in a resource-limited environment often modify their size, anatomy, and behaviors compared with mainland relatives. This has been well documented in modern and Cenozoic mammals, but it remains unclear whether older, more primitive Mesozoic mammals responded in similar ways to island habitats. We describe a reasonably complete and well-preserved skeleton of a kogaionid, an enigmatic radiation of Cretaceous island-dwelling multituberculate mammals previously represented by fragmentary fossils. This skeleton, from the latest Cretaceous of Romania, belongs to a previously unreported genus and species that possesses several aberrant features, including an autapomorphically domed skull and one of the smallest brains relative to body size of any advanced mammaliaform, which nonetheless retains enlarged olfactory bulbs and paraflocculi for sensory processing. Drawing on parallels with more recent island mammals, we interpret these unusual neurosensory features as related to the island effect. This indicates that the ability to adapt to insular environments developed early in mammalian history, before the advent of therian mammals, and mammals with insular-related modifications were key components of well-known dwarfed dinosaur faunas. Furthermore, the specimen suggests that brain size reduction, in association with heightened sensory acuity but without marked body size change, is a novel expression of the island effect in mammals.
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http://dx.doi.org/10.1073/pnas.1801143115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5948999PMC
May 2018

A new rhynchocephalian (Reptilia: Lepidosauria) from the Late Jurassic of Solnhofen (Germany) and the origin of the marine Pleurosauridae.

R Soc Open Sci 2017 Nov 8;4(11):170570. Epub 2017 Nov 8.

Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA.

A new rhynchocephalian is described based on a recently discovered and well-preserved specimen from the Late Jurassic (Kimmeridgian) marine limestones of Solnhofen, Bavaria. Phylogenetic analysis recovers the new taxon as the sister group to Pleurosauridae, a small radiation of rhynchocephalians representing the oldest marine invasion of crown-clade Lepidosauria. The relatively strong evidence for this taxonomically exclusive lineage, within a generally volatile rhynchocephalian tree, places the new taxon in a position to inform the early history of the pleurosaur transition to the sea. The early steps in this transition are distributed throughout the skeleton and appear to increase hydrodynamic efficiency for both swimming and aquatic feeding. This early history may also have included a global truncation of plesiomorphic ontogenetic trajectories that left a number of skeletal features with reduced levels of ossification/fusion. The exact degree to which had adopted an aquatic ecology remains unclear, but the insight it provides into the origin of the enigmatic pleurosaurs exemplifies the potential of Rhynchocephalia for generating and informing broad-based questions regarding the interplay of development, morphology, ecology and macroevolutionary patterns.
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http://dx.doi.org/10.1098/rsos.170570DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5717629PMC
November 2017

The skull roof tracks the brain during the evolution and development of reptiles including birds.

Nat Ecol Evol 2017 Oct 11;1(10):1543-1550. Epub 2017 Sep 11.

Department of Geology and Geophysics and Peabody Museum of Natural History, Yale University, New Haven, CT, 06520, USA.

Major transformations in brain size and proportions, such as the enlargement of the brain during the evolution of birds, are accompanied by profound modifications to the skull roof. However, the hypothesis of concerted evolution of shape between brain and skull roof over major phylogenetic transitions, and in particular of an ontogenetic relationship between specific regions of the brain and the skull roof, has never been formally tested. We performed 3D morphometric analyses to examine the deep history of brain and skull-roof morphology in Reptilia, focusing on changes during the well-documented transition from early reptiles through archosauromorphs, including nonavian dinosaurs, to birds. Non-avialan taxa cluster tightly together in morphospace, whereas Archaeopteryx and crown birds occupy a separate region. There is a one-to-one correspondence between the forebrain and frontal bone and the midbrain and parietal bone. Furthermore, the position of the forebrain-midbrain boundary correlates significantly with the position of the frontoparietal suture across the phylogenetic breadth of Reptilia and during the ontogeny of individual taxa. Conservation of position and identity in the skull roof is apparent, and there is no support for previous hypotheses that the avian parietal is a transformed postparietal. The correlation and apparent developmental link between regions of the brain and bony skull elements are likely to be ancestral to Tetrapoda and may be fundamental to all of Osteichthyes, coeval with the origin of the dermatocranium.
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http://dx.doi.org/10.1038/s41559-017-0288-2DOI Listing
October 2017

The evolution of the manus of early theropod dinosaurs is characterized by high inter- and intraspecific variation.

J Anat 2018 Jan 8;232(1):80-104. Epub 2017 Nov 8.

Richard Gilder Graduate School, American Museum of Natural History, New York, NY, USA.

The origin of the avian hand, with its reduced and fused carpals and digits, from the five-fingered hands and complex wrists of early dinosaurs represents one of the major transformations of manus morphology among tetrapods. Much attention has been directed to the later part of this transition, from four- to three-fingered taxa. However, earlier anatomical changes may have influenced these later modifications, possibly paving the way for a later frameshift in digit identities. We investigate the five- to four-fingered transition among early dinosaurs, along with changes in carpus morphology. New three-dimensional reconstructions from computed tomography data of the manus of the Triassic and Early Jurassic theropod dinosaurs Coelophysis bauri and Megapnosaurus rhodesiensis are described and compared intra- and interspecifically. Several novel findings emerge from these reconstructions and comparisons, including the first evidence of an ossified centrale and a free intermedium in some C. bauri specimens, as well as confirmation of the presence of a vestigial fifth metacarpal in this taxon. Additionally, a specimen of C. bauri and an unnamed coelophysoid from the Upper Triassic Hayden Quarry, New Mexico, are to our knowledge the only theropods (other than alvarezsaurs and birds) in which all of the distal carpals are completely fused together into a single unit. Several differences between the manus of C. bauri and M. rhodesiensis are also identified. We review the evolution of the archosauromorph manus more broadly in light of these new data, and caution against incorporating carpal characters in phylogenetic analyses of fine-scale relationships of Archosauromorpha, in light of the high degree of observed polymorphism in taxa for which large sample sizes are available, such as the theropod Coelophysis and the sauropodomorph Plateosaurus. We also find that the reduction of the carpus and ultimate loss of the fourth and fifth digits among early dinosaurs did not proceed in a neat, stepwise fashion, but was characterized by multiple losses and possible gains of carpals, metacarpals and phalanges. Taken together, the high degree of intra- and interspecific variability in the number and identities of carpals, and the state of reduction of the fourth and fifth digits suggest the presence of a 'zone of developmental variability' in early dinosaur manus evolution, from which novel avian-like morphologies eventually emerged and became channelized among later theropod clades.
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http://dx.doi.org/10.1111/joa.12719DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5735062PMC
January 2018

Dinosaur incubation periods directly determined from growth-line counts in embryonic teeth show reptilian-grade development.

Proc Natl Acad Sci U S A 2017 01 3;114(3):540-545. Epub 2017 Jan 3.

Division of Paleontology, American Museum of Natural History, New York, NY 10024.

Birds stand out from other egg-laying amniotes by producing relatively small numbers of large eggs with very short incubation periods (average 11-85 d). This aspect promotes high survivorship by limiting exposure to predation and environmental perturbation, allows for larger more fit young, and facilitates rapid attainment of adult size. Birds are living dinosaurs; their rapid development has been considered to reflect the primitive dinosaurian condition. Here, nonavian dinosaurian incubation periods in both small and large ornithischian taxa are empirically determined through growth-line counts in embryonic teeth. Our results show unexpectedly slow incubation (2.8 and 5.8 mo) like those of outgroup reptiles. Developmental and physiological constraints would have rendered tooth formation and incubation inherently slow in other dinosaur lineages and basal birds. The capacity to determine incubation periods in extinct egg-laying amniotes has implications for dinosaurian embryology, life history strategies, and survivorship across the Cretaceous-Paleogene mass extinction event.
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http://dx.doi.org/10.1073/pnas.1613716114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5255600PMC
January 2017

Flying starlings, PET and the evolution of volant dinosaurs.

Curr Biol 2016 Apr;26(7):R265-7

Richard Gilder Graduate School, American Museum of Natural History, New York, NY 10024, USA; Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA.

Birds have evolved behavioral and morphological adaptations for powered flight. Many aspects of this transition are unknown, including the neuroanatomical changes that made flight possible [1]. To understand how the avian brain drives this complex behavior, we utilized positron emission tomography (PET) scanning and the tracer (18)F-fluorodeoxyglucose (FDG) to document regional metabolic activity in the brain associated with a variety of locomotor behaviors. FDG studies are typically employed in rats [2] though the technology has been applied to birds [3]. We examined whole-brain function in European Starlings (Sturnus vulgaris), trained to fly in a wind tunnel while metabolizing the tracer. Drawing on predictions from early anatomical studies [4], we hypothesized increased metabolic activity in the Wulst and functionally related visual brain regions during flight. We found that flight behaviors correlated positively with entopallia and Wulst activity, but negatively with thalamic activity.
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http://dx.doi.org/10.1016/j.cub.2016.02.025DOI Listing
April 2016

A burrowing frog from the late Paleocene of Mongolia uncovers a deep history of spadefoot toads (Pelobatoidea) in East Asia.

Sci Rep 2016 Jan 11;6:19209. Epub 2016 Jan 11.

Department of Earth and Environmental Sciences, Columbia University, New York 10025.

Fossils are indispensible in understanding the evolutionary origins of the modern fauna. Crown-group spadefoot toads (Anura: Pelobatoidea) are the best-known fossorial frog clade to inhabit arid environments, with species utilizing a characteristic bony spade on their foot for burrowing. Endemic to the Northern Hemisphere, they are distributed across the Holarctic except East Asia. Here we report a rare fossil of a crown-group spadefoot toad from the late Paleocene of Mongolia. The phylogenetic analysis using both morphological and molecular information recovered this Asian fossil inside the modern North American pelobatoid clade Scaphiopodidae. The presence of a spade and the phylogenetic position of the new fossil frog strongly support its burrowing behavior. The late Paleocene age and other information suggestive of a mild climate cast doubt on the conventional assertion that burrowing evolved as an adaptation to aridity in spadefoot toads. Temporally and geographically, the new fossil provides the earliest record of Scaphiopodidae worldwide, and the only member of the group in Asia. Quantitative biogeographic analysis suggests that Scaphiopodidae, despite originating in North America, dispersed into East Asia via Beringia in the Early Cenozoic. The absence of spadefoot toads in East Asia today is a result of extinction.
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http://dx.doi.org/10.1038/srep19209DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4707494PMC
January 2016

The burrowing origin of modern snakes.

Sci Adv 2015 Nov 27;1(10):e1500743. Epub 2015 Nov 27.

Division of Paleontology, American Museum of Natural History, Central Park West and 79th Street, New York, NY 10024, USA.

Modern snakes probably originated as habitat specialists, but it controversial unclear whether they were ancestrally terrestrial burrowers or marine swimmers. We used x-ray virtual models of the inner ear to predict the habit of Dinilysia patagonica, a stem snake closely related to the origin of modern snakes. Previous work has shown that modern snakes perceive substrate vibrations via their inner ear. Our data show that D. patagonica and modern burrowing squamates share a unique spherical vestibule in the inner ear, as compared with swimmers and habitat generalists. We built predictive models for snake habit based on their vestibular shape, which estimated D. patagonica and the hypothetical ancestor of crown snakes as burrowers with high probabilities. This study provides an extensive comparative data set to test fossoriality quantitatively in stem snakes, and it shows that burrowing was predominant in the lineages leading to modern crown snakes.
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http://dx.doi.org/10.1126/sciadv.1500743DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4681343PMC
November 2015

Vertebral Pneumaticity in the Ornithomimosaur Archaeornithomimus (Dinosauria: Theropoda) Revealed by Computed Tomography Imaging and Reappraisal of Axial Pneumaticity in Ornithomimosauria.

PLoS One 2015 18;10(12):e0145168. Epub 2015 Dec 18.

Division of Paleontology, American Museum of Natural History, New York, New York, United States of America.

Among extant vertebrates, pneumatization of postcranial bones is unique to birds, with few known exceptions in other groups. Through reduction in bone mass, this feature is thought to benefit flight capacity in modern birds, but its prevalence in non-avian dinosaurs of variable sizes has generated competing hypotheses on the initial adaptive significance of postcranial pneumaticity. To better understand the evolutionary history of postcranial pneumaticity, studies have surveyed its distribution among non-avian dinosaurs. Nevertheless, the degree of pneumaticity in the basal coelurosaurian group Ornithomimosauria remains poorly known, despite their potential to greatly enhance our understanding of the early evolution of pneumatic bones along the lineage leading to birds. Historically, the identification of postcranial pneumaticity in non-avian dinosaurs has been based on examination of external morphology, and few studies thus far have focused on the internal architecture of pneumatic structures inside the bones. Here, we describe the vertebral pneumaticity of the ornithomimosaur Archaeornithomimus with the aid of X-ray computed tomography (CT) imaging. Complementary examination of external and internal osteology reveals (1) highly pneumatized cervical vertebrae with an elaborate configuration of interconnected chambers within the neural arch and the centrum; (2) anterior dorsal vertebrae with pneumatic chambers inside the neural arch; (3) apneumatic sacral vertebrae; and (4) a subset of proximal caudal vertebrae with limited pneumatic invasion into the neural arch. Comparisons with other theropod dinosaurs suggest that ornithomimosaurs primitively exhibited a plesiomorphic theropod condition for axial pneumaticity that was extended among later taxa, such as Archaeornithomimus and large bodied Deinocheirus. This finding corroborates the notion that evolutionary increases in vertebral pneumaticity occurred in parallel among independent lineages of bird-line archosaurs. Beyond providing a comprehensive view of vertebral pneumaticity in a non-avian coelurosaur, this study demonstrates the utility and need of CT imaging for further clarifying the early evolutionary history of postcranial pneumaticity.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0145168PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4684312PMC
July 2016

Wear biomechanics in the slicing dentition of the giant horned dinosaur Triceratops.

Sci Adv 2015 Jun 5;1(5):e1500055. Epub 2015 Jun 5.

Department of Mechanical Engineering, Lehigh University, 19 Memorial Drive West, Bethlehem, PA 18015, USA.

Herbivorous reptiles rarely evolve occluding dentitions that allow for the mastication (chewing) of plant matter. Conversely, most herbivorous mammals have occluding teeth with complex tissue architectures that self-wear to complex morphologies for orally processing plants. Dinosaurs stand out among reptiles in that several lineages acquired the capacity to masticate. In particular, the horned ceratopsian dinosaurs, among the most successful Late Cretaceous dinosaurian lineages, evolved slicing dentitions for the exploitation of tough, bulky plant matter. We show how Triceratops, a 9-m-long ceratopsian, and its relatives evolved teeth that wore during feeding to create fullers (recessed central regions on cutting blades) on the chewing surfaces. This unique morphology served to reduce friction during feeding. It was achieved through the evolution of a complex suite of osseous dental tissues rivaling the complexity of mammalian dentitions. Tribological (wear) properties of the tissues are preserved in ~66-million-year-old teeth, allowing the creation of a sophisticated three-dimensional biomechanical wear model that reveals how the complexes synergistically wore to create these implements. These findings, along with similar discoveries in hadrosaurids (duck-billed dinosaurs), suggest that tissue-mediated changes in dental morphology may have played a major role in the remarkable ecological diversification of these clades and perhaps other dinosaurian clades capable of mastication.
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http://dx.doi.org/10.1126/sciadv.1500055DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4640618PMC
June 2015

Reidentification of avian embryonic remains from the cretaceous of mongolia.

PLoS One 2015 1;10(6):e0128458. Epub 2015 Jun 1.

Division of Paleontology, American Museum of Natural History, New York, NY, 10024, United States of America.

Embryonic remains within a small (4.75 by 2.23 cm) egg from the Late Cretaceous, Mongolia are here re-described. High-resolution X-ray computed tomography (HRCT) was used to digitally prepare and describe the enclosed embryonic bones. The egg, IGM (Mongolian Institute for Geology, Ulaanbaatar) 100/2010, with a three-part shell microstructure, was originally assigned to Neoceratopsia implying extensive homoplasy among eggshell characters across Dinosauria. Re-examination finds the forelimb significantly longer than the hindlimbs, proportions suggesting an avian identification. Additional, postcranial apomorphies (strut-like coracoid, cranially located humeral condyles, olecranon fossa, slender radius relative to the ulna, trochanteric crest on the femur, and ulna longer than the humerus) identify the embryo as avian. Presence of a dorsal coracoid fossa and a craniocaudally compressed distal humerus with a strongly angled distal margin support a diagnosis of IGM 100/2010 as an enantiornithine. Re-identification eliminates the implied homoplasy of this tri-laminate eggshell structure, and instead associates enantiornithine birds with eggshell microstructure composed of a mammillary, squamatic, and external zones. Posture of the embryo follows that of other theropods with fore- and hindlimbs folded parallel to the vertebral column and the elbow pointing caudally just dorsal to the knees. The size of the egg and embryo of IGM 100/2010 is similar to the two other Mongolian enantiornithine eggs. Well-ossified skeletons, as in this specimen, characterize all known enantiornithine embryos suggesting precocial hatchlings, comparing closely to late stage embryos of modern precocial birds that are both flight- and run-capable upon hatching. Extensive ossification in enantiornithine embryos may contribute to their relatively abundant representation in the fossil record. Neoceratopsian eggs remain unrecognized in the fossil record.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0128458PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4452496PMC
April 2016

A possible instance of sexual dimorphism in the tails of two oviraptorosaur dinosaurs.

Sci Rep 2015 Mar 31;5:9472. Epub 2015 Mar 31.

American Museum of Natural History, New York City, New York, USA.

The hypothesis that oviraptorosaurs used tail-feather displays in courtship behavior previously predicted that oviraptorosaurs would be found to display sexually dimorphic caudal osteology. MPC-D 100/1002 and MPC-D 100/1127 are two specimens of the oviraptorosaur Khaan mckennai. Although similar in absolute size and in virtually all other anatomical details, the anterior haemal spines of MPC-D 100/1002 exceed those of MPC-D 100/1127 in ventral depth and develop a hitherto unreported "spearhead" shape. This dissimilarity cannot be readily explained as pathologic and is too extreme to be reasonably attributed to the amount of individual variation expected among con-specifics. Instead, this discrepancy in haemal spine morphology may be attributable to sexual dimorphism. The haemal spine form of MPC-D 100/1002 offers greater surface area for caudal muscle insertions. On this basis, MPC-D 100/1002 is regarded as most probably male, and MPC-D 100/1127 is regarded as most probably female.
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http://dx.doi.org/10.1038/srep09472DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4379468PMC
March 2015

Reconsidering the Avian Nature of the Oviraptorosaur Brain (Dinosauria: Theropoda).

PLoS One 2014 10;9(12):e113559. Epub 2014 Dec 10.

American Museum of Natural History, Division of Paleontology, Central Park West at 79th Street, New York, New York, United States of America.

The high degree of encephalization characterizing modern birds is the product of a long evolutionary history, our understanding of which is still largely in its infancy. Here we provide a redescription of the endocranial space of the oviraptorosaurian dinosaur Conchoraptor gracilis with the goal of assessing the hypothesis that it shares uniquely derived endocranial characters with crown-group avians. The existence of such features has implications for the transformational history of avian neuroanatomy and suggests that the oviraptorosaur radiation is a product of the immediate stem lineage of birds-after the divergence of Archaeopteryx lithographica. Results derived from an expanded comparative sample indicate that the strong endocranial similarity between Conchoraptor and modern birds largely reflects shared conservation of plesiomorphic features. The few characters that are maintained as being uniquely expressed in these two taxa are more likely products of convergence than homology but still indicate that the oviraptorosaur endocranial cavity has much to teach us about the complex history of avian brain evolution.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0113559PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4262302PMC
October 2017

Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur-bird transition.

Curr Biol 2014 Oct 25;24(20):2386-92. Epub 2014 Sep 25.

Division of Paleontology, American Museum of Natural History, New York, NY 10024, USA.

The evolution of birds from theropod dinosaurs was one of the great evolutionary transitions in the history of life. The macroevolutionary tempo and mode of this transition is poorly studied, which is surprising because it may offer key insight into major questions in evolutionary biology, particularly whether the origins of evolutionary novelties or new ecological opportunities are associated with unusually elevated "bursts" of evolution. We present a comprehensive phylogeny placing birds within the context of theropod evolution and quantify rates of morphological evolution and changes in overall morphological disparity across the dinosaur-bird transition. Birds evolved significantly faster than other theropods, but they are indistinguishable from their closest relatives in morphospace. Our results demonstrate that the rise of birds was a complex process: birds are a continuum of millions of years of theropod evolution, and there was no great jump between nonbirds and birds in morphospace, but once the avian body plan was gradually assembled, birds experienced an early burst of rapid anatomical evolution. This suggests that high rates of morphological evolution after the development of a novel body plan may be a common feature of macroevolution, as first hypothesized by G.G. Simpson more than 60 years ago.
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http://dx.doi.org/10.1016/j.cub.2014.08.034DOI Listing
October 2014

An expanded combined evidence approach to the Gavialis problem using geometric morphometric data from crocodylian braincases and Eustachian systems.

PLoS One 2014 8;9(9):e105793. Epub 2014 Sep 8.

Richard Gilder Graduate School, American Museum of Natural History, New York, New York, United States of America; Division of Paleontology, American Museum of Natural History, New York, New York, United States of America.

The phylogenetic position of the Indian gharial (Gavialis gangeticus) is disputed--morphological characters place Gavialis as the sister to all other extant crocodylians, whereas molecular and combined analyses find Gavialis and the false gharial (Tomistoma schlegelii) to be sister taxa. Geometric morphometric techniques have only begun to be applied to this issue, but most of these studies have focused on the exterior of the skull. The braincase has provided useful phylogenetic information for basal crurotarsans, but has not been explored for the crown group. The Eustachian system is thought to vary phylogenetically in Crocodylia, but has not been analytically tested. To determine if gross morphology of the crocodylian braincase proves informative to the relationships of Gavialis and Tomistoma, we used two- and three-dimensional geometric morphometric approaches. Internal braincase images were obtained using high-resolution computerized tomography scans. A principal components analysis identified that the first component axis was primarily associated with size and did not show groupings that divide the specimens by phylogenetic affinity. Sliding semi-landmarks and a relative warp analysis indicate that a unique Eustachian morphology separates Gavialis from other extant members of Crocodylia. Ontogenetic expansion of the braincase results in a more dorsoventrally elongate median Eustachian canal. Changes in the shape of the Eustachian system do provide phylogenetic distinctions between major crocodylian clades. Each morphometric dataset, consisting of continuous morphological characters, was added independently to a combined cladistic analysis of discrete morphological and molecular characters. The braincase data alone produced a clade that included crocodylids and Gavialis, whereas the Eustachian data resulted in Gavialis being considered a basally divergent lineage. When each morphometric dataset was used in a combined analysis with discrete morphological and molecular characters, it generated a tree that matched the topology of the molecular phylogeny of Crocodylia.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0105793PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4157744PMC
May 2015