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How many dinosaur species were there? Fossil bias and true richness estimated using a Poisson sampling model (TRiPS)

The fossil record is a rich source of information about biological diversity in the past. However, the fossil record is not only incomplete but has inherent biases due to geological, physical, chemical and biological factors. Our knowledge of past life is also biased because of differences in academic and amateur interests and sampling efforts. As a result, not all individuals or species that lived in the past are equally likely to be discovered at any point in time or space. To reconstruct temporal dynamics of diversity using the fossil record, biased sampling must be explicitly taken into account. Here, we introduce an approach that utilizes the variation in the number of times each species is observed in the fossil record to estimate both sampling bias and true richness. We term our technique TRiPS (True Richness estimated using a Poisson Sampling model) and explore its robustness to violation of its assumptions via simulations. We then venture to estimate sampling bias and absolute species richness of dinosaurs in the geological stages of the Mesozoic. Using TRiPS, we estimate that 1936 (1543-2468) species of dinosaurs roamed the Earth during the Mesozoic. We also present improved estimates of species richness trajectories of the three major dinosaur clades; the sauropodomorphs, ornithischians and theropods, casting doubt on the Jurassic-Cretaceous extinction event and demonstrating that all dinosaur groups are subject to considerable sampling bias throughout the Mesozoic.

Paleontology

Common species link global ecosystems to climate change

Common species shape the world around us, and changes in their commonness signify large-scale shifts in ecosystem structure and function1-4. Dominant taxa drive productivity and biogeochemical cycling, in direct interaction with abiotic components of the Earth system3,4. However, our understanding of the dynamic response of ecosystems to global environmental changes in the past is limited by our ability to robustly estimate fossil taxonomic richness5,6, and by our neglect of the importance of common species. To rectify this, we use observations of the most common and widespread species to track global changes in their distribution in the deep geological past. Our simple approach is robust to factors that bias richness estimators, including widely used sampling-standardization methods5, which we show are highly sensitive to variability in the species-abundance distribution. Causal analyses of common species frequency in the deep-sea sedimentary record detect a lagged response in the ecological prominence of planktonic foraminifera to oceanographic changes captured by deep-ocean temperature records over the last 65 million years, encompassing one of Earth's major climate transitions. Our results demonstrate that common species can act as tracers of a past global ecosystem and its response to physical changes in Earth's dynamic history.

Paleontology

Fossil calibrations for the arthropod Tree of Life

Fossil age data and molecular sequences are increasingly combined to establish a timescale for the Tree of Life. Arthropods, as the most species-rich and morphologically disparate animal phylum, have received substantial attention, particularly with regard to questions such as the timing of habitat shifts (e.g. terrestrialisation), genome evolution (e.g. gene family duplication and functional evolution), origins of novel characters and behaviours (e.g. wings and flight, venom, silk), biogeography, rate of diversification (e.g. Cambrian explosion, insect coevolution with angiosperms, evolution of crab body plans), and the evolution of arthropod microbiomes. We present herein a series of rigorously vetted calibration fossils for arthropod evolutionary history, taking into account recently published guidelines for best practice in fossil calibration. These are restricted to Palaeozoic and Mesozoic fossils, no deeper than ordinal taxonomic level, nonetheless resulting in 80 fossil calibrations for 102 clades. This work is especially timely owing to the rapid growth of molecular sequence data and the fact that many included fossils have been described within the last five years. This contribution provides a resource for systematists and other biologists interested in deep-time questions in arthropod evolution.\n\nABBREVIATIONS

Paleontology

MUSCLES OF FACIAL EXPRESSION IN EXTINCT SPECIES OF THE GENUS HOMO

We display a detailed description of mimetic muscles in extinct human species, framed in comparative and phylogenetic contexts. Using known facial landmarks, we assessed the arrangement of muscles of facial expression in Homo sapiens, neanderthalensis, erectus, heidelbergensis and ergaster. In modern humans, several perioral muscles are proportionally smaller in size (levator labii superioris, zygomaticus minor, zygomaticus major and triangularis) and/or located more medially (levator labii superioris, zygomaticus minor and quadratus labii inferioris) than in other human species. As mimetic musculature is examined in the most ancient specimens up to the most recent, there is a general trend towards an increase in size of corrugator supercillii and triangularis. Homo ergasters mimetic musculature closely resembles modern Homo, both in size and in location; furthermore, Homo erectus and Homo neanderthalensis share many muscular features. The extinct human species had an elaborate and highly graded facial communication system, but it remained qualitatively different from that reported in modern Homo. Compared with other human species, Homo sapiens clearly exhibits a lower degree of facial expression, possibly correlated with more sophisticated social behaviours and with enhanced speech capabilities. The presence of anatomical variation among species of the genus Homo raises important questions about the possible taxonomic value of mimetic muscles.

Paleontology

The case for species selection

The mere existence of speciation and extinction make macro-evolutionary processes possible. Speciation and extinction introduce discontinuities in the microevolutionary change within lineages by initiating, disrupting, and terminating the continuity of species lineages. Within a clade, speciation and extinction become potent means of macroevolution in and of themselves. This process, termed species selection, is a macroevolutionary analogue of natural selection, with species playing an analogous part akin to that played by organisms in microevolution. That said, it has proven difficult to think about levels of selection. The concept of species sorting was introduced to help our thinking on this issue by identifying two aspects inherent in hierarchical systems can confuse our attempts to understand them: uncertainty in the level that selection acts and uncertainty about if the pattern of selection is in fact caused at all. Thanks to insights from evolutionary transitions in individuality, we now know more about how to identify the level of selection and how to parse the causal structure in hierarchical evolutionary circumstances. We know that if the fitness of organisms causes the fitness of more inclusive species then they must covary. However, there is no evidence of such a covariance between fitnesses at these two levels. This covariance is just not observed; neither between cells and organisms nor between organisms and species. Rather, speciation and extinction rates appear to be completely divorced from organismal fitness. With this insight, the concept of species sorting shrinks so that it only covers the two processes of species selection and drift. I argue that we are better off focusing on understanding the processes of species selection and drift and that there is therefore no further need for the concept of species sorting.

paleontology

A SUPERNOVA AT 50 PC: EFFECTS ON THE EARTHS ATMOSPHERE AND BIOTA

Recent 60Fe results have suggested that the estimated distances of supernovae in the last few million years should be reduced from [~]100 pc to [~]50 pc. Two events or series of events are suggested, one about 2.7 million years to 1.7 million years ago, and another may at 6.5 to 8.7 million years ago. We ask what effects such supernovae are expected to have on the terrestrial atmosphere and biota. Assuming that the Local Bubble was formed before the event being considered, and that the supernova and the Earth were both inside a weak, disordered magnetic field at that time, TeV-PeV cosmic rays at Earth will increase by a factor of a few hundred. Tropospheric ionization will increase proportionately, and the overall muon radiation load on terrestrial organisms will increase by a factor of [~]150. All return to pre-burst levels within 10kyr. In the case of an ordered magnetic field, effects depend strongly on the field orientation. The upper bound in this case is with a largely coherent field aligned along the line of sight to the supernova, in which case TeV-PeV cosmic ray flux increases are [~]104; in the case of a transverse field they are below current levels. We suggest a substantial increase in the extended effects of supernovae on Earth and in the \"lethal distance\" estimate; more work is needed. This paper is an explicit followup to Thomas et al. (2016). We also here provide more detail on the computational procedures used in both works.

paleontology

Coral reefs in crisis: The reliability of deep-time food web reconstructions as analogs for the present

Ongoing anthropogenic alterations of the biosphere have shifted emphasis in conservation biology from individual species to entire ecosystems. Modern measures of ecosystem change, however, lack the extended temporal scales necessary to forecast future change under increasingly stressful environmental conditions. Accordingly, the assessment and reconstruction of ecosystem dynamics during previous intervals of environmental stress and climate change in deep time has garnered increasing attention. The nature of the fossil record, though, raises questions about the difficulty of reconstructing paleocommunity and paleoecosystem-level dynamics. In this study, we assess the reliability of such reconstructions by simulating the fossilization of a highly threatened and disturbed modern ecosystem, a Caribbean coral reef. Using a high-resolution coral reef food web from Jamaica, we compare system structures of the modern and simulated fossil reefs, including guild richness and evenness, trophic level distribution, predator dietary breadth, food chain lengths, and modularity. Results indicate that despite the loss of species, guilds, and trophospecies interactions, particularly zooplankton and other soft-bodied organisms, the overall guild diversity, structure, and modularity of the reef ecosystem remained intact. These results have important implications for the integrity of fossil food web studies and coral reef conservation, demonstrating that fossil reef communities can be used to understand reef community dynamics during past regimes of environmental change.

paleontology

A Posteriori Evaluation Of Molecular Divergence Dates Using Empirical Estimates Of Time-Heterogeneous Fossilization Rates

The application of molecular clock concepts in phylogenetics permits estimating the divergence times of clades with an incomplete fossil record. However, the reliability of this approach is disputed, because the resulting estimates are often inconsistent with different sets of fossils and other parameters (clock models and prior settings) in the analyses. Here, we present the {lambda} statistic, a likelihood approach for a posteriori evaluating the reliability of estimated divergence times. The {lambda} statistic is based on empirically derived fossilization rates and evaluates the fit of estimated divergence times to the fossil record. We tested the performance of this measure with simulated data sets. Furthermore, we applied it to the estimated divergence times of (i) Clavigeritae beetles of the family Staphylinidae and (ii) all extant insect orders. The reanalyzed beetle data supports the originally published results, but shows that several fossil calibrations used do not increase the reliability of the divergence time estimates. Analyses of estimated inter-ordinal insect divergences indicate that uniform priors with soft bounds marginally outperform log-normal priors on node ages. Furthermore, a posteriori evaluation of the original published analysis indicates that several inter-ordinal divergence estimates might be too young. The {lambda} statistic allows the comparative evaluation of any clade divergence estimate derived from different calibration approaches. Consequently, the application of different algorithms, software tools, and calibration schemes can be empirically assessed.

paleontology

A new genus of horse from Pleistocene North America

The extinct \"New World stilt-legged\", or NWSL, equids constitute a perplexing group of Pleistocene horses endemic to North America. Their slender distal limb bones resemble those of Asiatic asses, such as the Persian onager. Previous palaeogenetic studies, however, have suggested a closer relationship to caballine horses than to Asiatic asses. Here, we report complete mitochondrial and partial nuclear genomes from NWSL equids from across their geographic range. Although multiple NWSL equid species have been named, our palaeogenomic and morphometric analyses support the idea that there was only a single species of middle to late Pleistocene NWSL equid, and demonstrate that it falls outside of crown group Equus. We therefore propose a new genus, Haringtonhippus, for the sole species H. francisci. Our combined genomic and phenomic approach to resolving the systematics of extinct megafauna will allow for an improved understanding of the full extent of the terminal Pleistocene extinction event.

paleontology

Three-dimensional mobility and muscle attachments in the pectoral limb of the Triassic cynodont Massetognathus pascuali

The musculoskeletal configuration of the mammalian pectoral limb has been heralded as a key anatomical feature leading to the adaptive radiation of mammals, but limb function in the cynodont outgroup remains unresolved. Conflicting reconstructions of abducted and adducted posture are based on mutually-incompatible interpretations of ambiguous osteology. We reconstruct the pectoral limb of the Triassic non-mammalian cynodont Massetognathus pascuali in three dimensions, by combining skeletal morphology from micro-computed tomography with muscle anatomy from an extended extant phylogenetic bracket. Conservative tests of maximum range of motion suggest a degree of girdle mobility, as well as substantial freedom at the shoulder and the elbow joints. The glenoid fossa supports a neutral pose in which the distal end of the humerus points 45{degrees} posterolaterally from the body wall, intermediate between classically \"sprawling\" and \"parasagittal\" limb postures. Massetognathus is reconstructed as having a near-mammalian complement of shoulder muscles, including an incipient rotator cuff (m. subscapularis, m. infraspinatus, m. supraspinatus, and m. teres minor). Based on close inspection of the morphology of the glenoid fossa, we hypothesize a posture-driven scenario for the evolution of the therian ball-and-socket shoulder joint. The musculoskeletal reconstruction presented here provides the anatomical scaffolding for more detailed examination of locomotor evolution in the precursors to mammals.

paleontology

The measurement of species selection on evolving characters

Many processes can contribute to macroevolutionary change. This fact is the source of the wide variety of macroevolutionary change across time and taxa as well as the bane of pale-obiological research trying to understand how macroevolution works. Here, I present a general framework for understanding the variety of macroevolutionary phenomena. Based on Prices theorem, this framework provides a simple quantitative means to understand (1) the macroevolutionary processes that are possible and (2) the way those processes interact with each other. The major qualitative features of macroevolution depend first on the number of processes that co-occur and then on the magnitudes and evolutionary directions of those processes. Species selection, the major macroevolutionary process, consists of patterns of differential rates of speciation and extinction. Its macroevolutionary efficacy depends on the presences of sufficient microevolutionary change. Conversely, microevolutionary change is limited in power by the independent evolution of species, and species selection acting across populations of species can amplify or suppress microevolution. Non-trends may result if species selection sufficiently neutralizes microevolution and may yield stable macroevolutionary patterns over many millions of years.

paleontology

History is written by the victors: the effect of the push of the past on the fossil record

Phylogenies may be modelled using \"birth-death\" models for speciation and extinction, but even when a homogeneous rate of diversification is used, survivorship biases can generate remarkable rate heterogeneities through time. One such bias has been termed the \"push of the past\", by which the length of time a clade has survived is conditioned on the rate of diversification that happened to pertain at its origin. This creates the illusion of a secular rate slow-down through time that is, rather, a reversion to the mean. Here we model the controls on the push of the past, and the effect it has on clade origination times, and show that it largely depends on underlying extinction rates. An extra effect increasing early rates of lineage generation is also seen in large clades. These biases are important but relatively neglected influences on many aspects of diversification patterns, such as diversification spikes after mass extinctions and at the origins of clades; they also influence rates of fossilisation, changes in rates of phenotypic evolution and even molecular clocks. These inevitable features of surviving and/or large clades should thus not be generalised to the diversification process as a whole without additional study of small and extinct clades.

paleontology

An Early Devonian permineralized rhyniopsid from the Battery Point Formation of Gaspe (Canada)

The Emsian deposits of the Battery Point Formation (GaspeCanada) host the most diverse Early Devonian flora in North America. While most of this diversity has been described from plant compressions, the permineralized component of the flora is incompletely explored. Based on >15 axes studied in serial sections, we describe a new anatomically preserved rhyniopsid from the Battery Point Formation, Eddianna gaspiana gen. & sp. nov.. Eddianna axes are up to 2 mm in diameter and have a well-developed terete xylem strand with potential centrarch maturation (comprising 80% of the cross sectional surface area) that features Sennicaulis-type tracheid wall thickenings. A thin layer interpreted as phloem is preserved around the central xylem and an irregular sclerenchymatous cortex forms longitudinal anastomosing ridges on the outside of the axes. The anatomy of Eddianna axes suggests that they represent lower portions, specialized in efficient water transfer, of a larger plant whose distal regions have yet to be discovered. Eddianna, the first permineralized rhyniopsid described from the Battery Point Formation, is one of only four anatomically preserved plants reported from this unit. These fossils reiterate the potential for additional discoveries of anatomically preserved plants in the Battery Point Formation.

paleontology

Uneven Data Quality and the Earliest Occupation of Europe: The Case of Untermassfeld (Germany)

The database regarding the earliest occupation of Europe has increased significantly in quantity and quality of data points over the last two decades, mainly through the addition of new sites as a result of long-term systematic excavations and large-scale prospections of Early and early Middle Pleistocene exposures. The site distribution pattern suggests an ephemeral presence of hominins in the south of Europe from around one million years ago, with occasional short northward expansions along the western coastal areas when temperate conditions permitted. From around 600,000-700,000 years ago Acheulean artefacts appear in Europe and somewhat later hominin presence seems to pick up, with more sites and now some also present in colder climatic settings. It is again only later, around 350,000 years ago, that the first sites show up in more continental, central parts of Europe, east of the Rhine. A series of recent papers on the Early Pleistocene palaeontological site of Untermassfeld (Germany) makes claims that are of great interest for studies of earliest Europe and are at odds with the described pattern: the papers suggest that Untermassfeld has yielded stone tools and humanly modified faunal remains, evidence for a one million years old hominin presence in European continental mid-latitudes, and additional evidence that hominins were well-established in Europe already around that time period. Here we evaluate these claims and demonstrate that these studies are severely flawed in terms of data on provenance of the materials studied and in the interpretation of faunal remains and lithics as testifying to a hominin presence at the site. In actual fact any reference to the Untermassfeld site as an archaeological one is unwarranted. Furthermore, it is not the only European Early Pleistocene site where inferred evidence for hominin presence is problematic. The strength of the spatiotemporal patterns of hominin presence and absence depend on the quality of the data points we work with, and data base maintenance, including critical evaluation of new sites, is crucial to advance our knowledge of the expansions and contractions of hominin ranges during the Pleistocene.

paleontology

A primitive starfish ancestor from the Early Ordovician of Morocco reveals the origin of crown group Echinodermata

The somasteroids are Ordovician star-shaped animals widely regarded as ancestors of Asterozoa, the group of extant echinoderms that includes brittle stars and starfish. The phylogenetic position of somasteroids makes them critical for understanding the origin and early evolution of crown group Echinodermata. However, the early evolution of asterozoans, the origin of their distinctive body organization and their relationships with other Cambrian and Ordovician echinoderms, such as edrioasteroids, blastozoans, crinoids, and other asterozoans, remain problematic due to the difficulties of comparing the calcitic endoskeleton of these disparate groups. Here we describe the new somasteroid Cantabrigiaster fezouataensis from the Early Ordovician (Tremadocian) Fezouata Lagerstatte in Morocco. Cantabrigiaster shares with other somasteroids the presence of rod-like virgal ossicles that articulate with the ambulacrals, but differs from all other known asterozoans in the absence of adambulacral ossicles defining the arm margins. The unique arm construction evokes parallels with non-asterozoan echinoderms. Developmentally informed Bayesian and parsimony based phylogenetic analyses, which reflect the homology of the biserial ambulacral ossicles in Paleozoic echinoderms according to the Extraxial-Axial Theory, recover Cantabrigiaster as basal within stem group Asterozoa. Our results indicate that Cantabrigiaster is the earliest diverging stem group asterozoan, revealing the ancestral morphology of this major clade and clarifying the affinities of problematic Ordovician taxa. Somasteroids are resolved as a paraphyletic grade within stem and crown group Asterozoa (starfishes), whereas stenuroids are paraphyletic within stem group Ophiuroidea (brittle stars). Cantabrigiaster also illuminates the relationship between Ordovician crown group Echinodermata and its Cambrian stem lineage, which includes sessile forms with incipient radial symmetry such as edrioasteroids and blastozoans. The contentious Pelmatozoa hypothesis (i.e. monophyly of blastozoans and crinoids) is not supported; instead, blastozoans represent the most likely sister-taxon of crown group Echinodermata.\n\nAuthor summaryStarfish and brittle stars, collectively known as asterozoans, constitute a diverse and ecologically successful group of echinoderms that first appear in the fossil record some 480Ma. However, the early evolution of asterozoans, the origin of their distinctive body organization, and their phylogenetic relationships with Cambrian echinoderms remain largely unresolved. We describe Cantabrigiaster fezouataensis gen. et sp. nov., a primitive asterozoan from the Fezouata Lagerstatte, Morocco, with a unique endoskeletal arm organization that reveals the ancestral morphology of this major clade. Bayesian and parsimony based phylogenetic analyses indicate that Cantabrigiaster is the earliest diverging stem group asterozoan, and resolve the phylogenetic position of Ordovician asterozoans such as somasteroids. Our analyses clarify the origin of crown group echinoderms relative to their problematic Cambrian stem group representatives.

paleontology

What drives results in Bayesian morphological clock analyses?

Recently, approaches that estimate species divergence times using fossil taxa and models of morphological evolution have exploded in popularity. These methods incorporate diverse biological and geological information to inform posterior reconstructions, and have been applied to several high-profile clades to positive effect. However, there are important examples where morphological data are misleading, resulting in unrealistic age estimates. While several studies have demonstrated that these approaches can be robust and internally consistent, the causes and limitations of these patterns remain unclear. In this study, we dissect signal in Bayesian dating analyses of three mammalian clades. For two of the three examples, we find that morphological characters provide little information regarding divergence times as compared to geological range information, with posterior estimates largely recapitulating those recovered under the prior. However, in the cetacean dataset, we find that morphological data do appreciably inform posterior divergence time estimates. We supplement these empirical analyses with a set of simulations designed to explore the efficiency and limitations of binary and 3-state character data in reconstructing node ages. Our results demonstrate areas of both strength and weakness for morphological clock analyses, and help to outline conditions under which they perform best and, conversely, when they should be eschewed in favour of purely geological approaches.

paleontology

Root grooves on two adjacent anterior teeth of Australopithecus africanus

Tooth root grooves and other ante-mortem dental tissue loss not associated with caries found on or near the cementoenamel junction (CEJ) are commonly termed non-carious cervical lesions. Three main processes are implicated in forming these lesions: abrasion, dental erosion, and abfraction. As yet, these lesions have not been described in non-Homo hominins. In this study South African fossil hominin collections were examined for evidence of any type of non-carious cervical lesion. Only one individual shows ante-mortem root grooves consistent with non-carious cervical lesions. Two teeth, a mandibular right permanent lateral incisor (STW 270) and canine (STW 213), belonging to the same Australopithecus africanus individual, show clear ante-mortem grooves on the labial root surface. These lesions start below the CEJ, extend over a third of the way toward the apex, and taper to a point towards the lingual side. Microscopic examination revealed no clear directional striations. The shape of these grooves is extremely similar to clinical examples of dental erosion, with the lack of striations supporting this diagnosis. These are the oldest hominin examples of non-carious cervical lesions and first described in a genus other than Homo; further, the lesions suggest that this individual regularly consumed or processed acidic food items.

paleontology

Terrestrial effects of moderately nearby supernovae

Recent data indicate one or more moderately nearby supernovae in the early Pleistocene, with additional events likely in the Miocene. This has motivated more detailed computations, using new information about the nature of supernovae and the distances of these events to describe in more detail the sorts of effects that are indicated at the Earth. This short communication/review is designed to describe some of these effects so that they may possibly be related to changes in the biota around these times.\n\nSummaryIt has been known for some time that moderately nearby supernovae may have substantial effects on the Earth. Events at {small tilde}150 light years will happen on average every few Myr, but will tend to happen in groups, with long periods between with no events. The effects of cosmic rays from such events appears to be greater than estimated previously. Ozone depletion and the increase of hazardous UVB continues to be important, but new effects come to the fore. Muon irradiation on the ground and hundreds of meters down into the ocean will increase cancer and mutation rates, the differences being most notable in terrestrial megafauna and benthic organisms. Typically larger organisms live long enough to develop cancer; in microorganisms the primary effects would be associated with mutation rates. Atmospheric ionization in the troposphere will greatly increase lightning rates, with a concomitant increase in the rate of wildfires.

paleontology