The affinities of the Late Triassic Cryptovaranoides and the age of crown squamates.

Most living reptile diversity is concentrated in Squamata (lizards, including snakes), which have poorly known origins in space and time. Recently, †Cryptovaranoides microlanius from the Late Triassic of the United Kingdom was described as the oldest crown squamate. If true, this result would push back the origin of all major lizard clades by 30-65 Myr and suggest that divergence times for reptile clades estimated using genomic and morphological data are grossly inaccurate. Here, we use computed tomography scans and expanded phylogenetic datasets to re-evaluate the phylogenetic affinities of †Cryptovaranoides and other putative early squamates. We robustly reject the crown squamate affinities of †Cryptovaranoides, and instead resolve †Cryptovaranoides as a potential member of the bird and crocodylian total clade, Archosauromorpha. Bayesian total evidence dating supports a Jurassic origin of crown squamates, not Triassic as recently suggested. We highlight how features traditionally linked to lepidosaurs are in fact widespread across Triassic reptiles. Our study reaffirms the importance of critically choosing and constructing morphological datasets and appropriate taxon sampling to test the phylogenetic affinities of problematic fossils and calibrate the Tree of Life.

A giant armoured skink from Australia expands lizard morphospace and the scope of the Pleistocene extinctions.

There are more species of lizards and snakes (squamates) alive today than any other order of land vertebrates, yet their fossil record has been poorly documented compared with other groups. Here, we describe a gigantic Pleistocene skink from Australia based on extensive material that includes much of the skull and postcranial skeleton, and spans ontogenetic stages from neonate to adult. Tiliqua frangens substantially expands the known ecomorphological diversity of squamates. At approximately 2.4 kg, it was more than double the mass of any living skink, with an exceptionally broad, deep skull, squat limbs and heavy, ornamented body armour. It probably filled the armoured herbivore niche that land tortoises (testudinids), absent from Australia, occupy on other continents. Tiliqua frangens and other giant Plio-Pleistocene skinks suggest that small-bodied groups that dominate vertebrate biodiversity might have lost their largest and often most morphologically extreme representatives in the Late Pleistocene, expanding the scope of these extinctions.

Response to comment on "Exceptional preservation of organs in Devonian placoderms from the Gogo largerstätte".

Jensen et al. (1) question evidence presented of a chambered heart within placoderms, citing its small size and apparently ventral atrium. However, they fail to note the belly-up orientation of the placoderm within one nodule, and the variability of heart morphology within extant taxa. Thus, we remain confident in our interpretation of the mineralized organ as the heart.

Multiple modes of inference reveal less phylogenetic signal in marsupial basicranial shape compared with the rest of the cranium.

Incorporating morphological data into modern phylogenies allows integration of fossil evidence, facilitating divergence dating and macroevolutionary inferences. Improvements in the phylogenetic utility of morphological data have been sought via Procrustes-based geometric morphometrics (GMM), but with mixed success and little clarity over what anatomical areas are most suitable. Here, we assess GMM-based phylogenetic reconstructions in a heavily sampled source of discrete characters for mammalian phylogenetics-the basicranium-in 57 species of marsupial mammals, compared with the remainder of the cranium. We show less phylogenetic signal in the basicranium compared with a 'Rest of Cranium' partition, using diverse metrics of phylogenetic signal (Kmult, phylogenetically aligned principal components analysis, comparisons of UPGMA/neighbour-joining/parsimony trees and cophenetic distances to a reference phylogeny) for scaled, Procrustes-aligned landmarks and allometry-corrected residuals. Surprisingly, a similar pattern emerged from parsimony-based analyses of discrete cranial characters. The consistent results across methods suggest that easily computed metrics such as Kmult can provide good guidance on phylogenetic information in a landmarking configuration. In addition, GMM data may be less informative for intricate but conservative anatomical regions such as the basicranium, while better-but not necessarily novel-phylogenetic information can be expected for broadly characterized shapes such as entire bones. This article is part of the theme issue 'The mammalian skull: development, structure and function'.

A new look at an old Australian raptor places Taphaetus lacertosus de Vis 1905 in the Old World vultures (Accipitridae: Aegypiinae).

The Australian Pleistocene fossil record of the Accipitridae (hawks, eagles and Old World vultures) is sparse and poorly known. Only two extinct confirmed accipitrid species have been described for this time period; both have received little investigation since their description. One is Taphaetus lacertosus de Vis, 1905, described from a distal humerus and a quadrate from north-eastern South Australia. While this species was verified as an accipitrid in subsequent studies, its more precise taxonomic affinities have remained conjectural. In this study, a new analysis incorporating newly referred material and phylogenetic analyses using a wide range of accipitriforms reveals that the lectotype humerus of T. lacertosus is an Old World vulture in the subfamily Aegypiinae. The associated quadrate, one of two original syntypes from which de Vis named this species, is of an indeterminate species of ardeid. We erect the novel genus Cryptogyps, to accommodate the species lacertosus, as it cannot be placed in Taphaetus de Vis, 1891, because the type species of this genus, Uroaetus brachialis de Vis, 1889, was transferred back to the genus Uroaetus, a synonym of Aquila Brisson, by de Vis in 1905. Further, U. brachialis is now considered a synonym of Aquila audax (Latham, 1801). Moreover, Taphaetus de Vis, 1891 is a senior homonym of Taphaetus de Vis, 1905, type species Taphaetus lacertosus de Vis, 1905, making the 1905 version of the genus unavailable. Newly referred fossils from Wellington Caves (NSW) and the Nullarbor Plains (WA) reveal this taxon had a wide geographical range across Pleistocene Australia. The referred tarsometatarsus lacks hyper-developed trochleae, indicating that Cryptogyps lacertosus (de Vis, 1905) comb. nov., was probably a scavenger like other aegypiines. Identification of Cryptogyps lacertosus as an aegypiine significantly expands the palaeogeographical range of the Old World vultures, hitherto unknown in Australia. The avian guild of large, obligate scavenging birds of prey, is currently absent in the modern Australian biota, but its former presence is not surprising given the megafauna-rich communities of the Pleistocene.

Exceptional preservation of organs in Devonian placoderms from the Gogo lagerstätte.

The origin and early diversification of jawed vertebrates involved major changes to skeletal and soft anatomy. Skeletal transformations can be examined directly by studying fossil stem gnathostomes; however, preservation of soft anatomy is rare. We describe the only known example of a three-dimensionally mineralized heart, thick-walled stomach, and bilobed liver from arthrodire placoderms, stem gnathostomes from the Late Devonian Gogo Formation in Western Australia. The application of synchrotron and neutron microtomography to this material shows evidence of a flat S-shaped heart, which is well separated from the liver and other abdominal organs, and the absence of lungs. Arthrodires thus show the earliest phylogenetic evidence for repositioning of the gnathostome heart associated with the evolution of the complex neck region in jawed vertebrates.

The impact of molecular data on the phylogenetic position of the putative oldest crown crocodilian and the age of the clade.

The use of molecular data for living groups is vital for interpreting fossils, especially when morphology-only analyses retrieve problematic phylogenies for living forms. These topological discrepancies impact on the inferred phylogenetic position of many fossil taxa. In Crocodylia, morphology-based phylogenetic inferences differ fundamentally in placing Gavialis basal to all other living forms, whereas molecular data consistently unite it with crocodylids. The Cenomanian Portugalosuchus azenhae was recently described as the oldest crown crocodilian, with affinities to Gavialis, based on morphology-only analyses, thus representing a potentially important new molecular clock calibration. Here, we performed analyses incorporating DNA data into these morphological datasets, using scaffold and supermatrix (total evidence) approaches, in order to evaluate the position of basal crocodylians, including Portugalosuchus. Our analyses incorporating DNA data robustly recovered Portugalosuchus outside Crocodylia (as well as thoracosaurs, planocraniids and Borealosuchus spp.), questioning the status of Portugalosuchus as crown crocodilian and any future use as a node calibration in molecular clock studies. Finally, we discuss the impact of ambiguous fossil calibration and how, with the increasing size of phylogenomic datasets, the molecular scaffold might be an efficient (though imperfect) approximation of more rigorous but demanding supermatrix analyses.

Lions and brown bears colonized North America in multiple synchronous waves of dispersal across the Bering Land Bridge.

The Bering Land Bridge connecting North America and Eurasia was periodically exposed and inundated by oscillating sea levels during the Pleistocene glacial cycles. This land connection allowed the intermittent dispersal of animals, including humans, between Western Beringia (far northeast Asia) and Eastern Beringia (northwest North America), changing the faunal community composition of both continents. The Pleistocene glacial cycles also had profound impacts on temperature, precipitation and vegetation, impacting faunal community structure and demography. While these palaeoenvironmental impacts have been studied in many large herbivores from Beringia (e.g., bison, mammoths, horses), the Pleistocene population dynamics of the diverse guild of carnivorans present in the region are less well understood, due to their lower abundances. In this study, we analyse mitochondrial genome data from ancient brown bears (Ursus arctos; n = 103) and lions (Panthera spp.; n = 39), two megafaunal carnivorans that dispersed into North America during the Pleistocene. Our results reveal striking synchronicity in the population dynamics of Beringian lions and brown bears, with multiple waves of dispersal across the Bering Land Bridge coinciding with glacial periods of low sea levels, as well as synchronous local extinctions in Eastern Beringia during Marine Isotope Stage 3. The evolutionary histories of these two taxa underline the crucial biogeographical role of the Bering Land Bridge in the distribution, turnover and maintenance of megafaunal populations in North America.

A late-surviving stem-ctenophore from the Late Devonian of Miguasha (Canada).

Like other soft-bodied organisms, ctenophores (comb jellies) produce fossils only under exceptional taphonomic conditions. Here, we present the first record of a Late Devonian ctenophore from the Escuminac Formation from Miguasha in eastern Canada. Based on the 18-fold symmetry of this disc-shaped fossil, we assign it to the total-group Ctenophora. Our phylogenetic analyses suggest that the new taxon Daihuoides jakobvintheri gen. et sp. nov. falls near Cambrian stem ctenophores such as 'dinomischids' and 'scleroctenophorans'. Accordingly, Daihuoides is a Lazarus-taxon, which post-dates its older relatives by over 140 million years, and overlaps temporally with modern ctenophores, whose oldest representatives are known from the Early Devonian. Our analyses also indicate that the fossil record of ctenophores does not provide strong evidence for or against the phylogenomic hypothesis that ctenophores are sister to all other metazoans.

Plicidentine and the repeated origins of snake venom fangs.

Snake fangs are an iconic exemplar of a complex adaptation, but despite striking developmental and morphological similarities, they probably evolved independently in several lineages of venomous snakes. How snakes could, uniquely among vertebrates, repeatedly evolve their complex venom delivery apparatus is an intriguing question. Here we shed light on the repeated evolution of snake venom fangs using histology, high-resolution computed tomography (microCT) and biomechanical modelling. Our examination of venomous and non-venomous species reveals that most snakes have dentine infoldings at the bases of their teeth, known as plicidentine, and that in venomous species, one of these infoldings was repurposed to form a longitudinal groove for venom delivery. Like plicidentine, venom grooves originate from infoldings of the developing dental epithelium prior to the formation of the tooth hard tissues. Derivation of the venom groove from a large plicidentine fold that develops early in tooth ontogeny reveals how snake venom fangs could originate repeatedly through the co-option of a pre-existing dental feature even without close association to a venom duct. We also show that, contrary to previous assumptions, dentine infoldings do not improve compression or bending resistance of snake teeth during biting; plicidentine may instead have a role in tooth attachment.

Evolution: Morphological saturation and release in mammals.

Mammal evolution in the Mesozoic was thought to be heavily constrained by competition and predation by dinosaurs. A new study suggests that placental mammals remained constrained for several million years after non-avian dinosaurs perished, perhaps due to competition from archaic mammals.

Holocene population expansion of a tropical bee coincides with early human colonization of Fiji rather than climate change.

There is substantial debate about the relative roles of climate change and human activities on biodiversity and species demographies over the Holocene. In some cases, these two factors can be resolved using fossil data, but for many taxa such data are not available. Inferring historical demographies of taxa has become common, but the methodologies are mostly recent and their shortcomings often unexplored. The bee genus Homalictus is developing into a tractable model system for understanding how native bee populations in tropical islands have responded to past climate change. We greatly expand on previous studies using sequences of the mitochondrial gene COI from 474 specimens and between 171 and 3928 autosomal (DArTSeq) single nucleotide polymorphism loci from 19 specimens of the native Fijian bee, Homalictus fijiensis, to explore its historical demography using coalescent and mismatch analyses. We ask whether past changes in demography were human- or climate-driven, while considering analytical assumptions. We show that inferred changes in population sizes are too recent to be explained by past climate change. Instead we find that a dramatic increase in population size for the main island of Viti Levu coincides with increasing occupation by humans and their modification of the environment. We found no corresponding change in bee population size for another major island, Kadavu, where human populations and agricultural activities have been historically very low. Our analyses indicate that molecular approaches can be used to disentangle the impacts of humans and climate change on a major tropical pollinator and that stringent analytical approaches are required for reliable interpretation of results.

Erratum: Cretaceous blind snake from Brazil fills major gap in snake evolution.

[This corrects the article DOI: 10.1016/j.isci.2020.101834.].

Cretaceous Blind Snake from Brazil Fills Major Gap in Snake Evolution.

Blind snakes (Scolecophidia) are minute cryptic snakes that diverged at the base of the evolutionary radiation of modern snakes. They have a scant fossil record, which dates back to the Upper Paleocene-Lower Eocene (∼56 Ma); this late appearance conflicts with molecular evidence, which suggests a much older origin for the group (during the Mesozoic: 160-125 Ma). Here we report a typhlopoid blind snake from the Late Cretaceous of Brazil, Boipeba tayasuensis gen. et sp. nov, which extends the scolecophidian fossil record into the Mesozoic and reduces the fossil gap predicted by molecular data. The new species is estimated to have been over 1 m long, much larger than typical modern scolecophidians (<30 cm). This finding sheds light on the early evolution of blind snakes, supports the hypothesis of a Gondwanan origin for the Typhlopoidea, and indicates that early scolecophidians had large body size, and only later underwent miniaturization.

Author Correction: Elpistostege and the origin of the vertebrate hand.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Radiation of tropical island bees and the role of phylogenetic niche conservatism as an important driver of biodiversity.

Island biogeography explores how biodiversity in island ecosystems arises and is maintained. The topographical complexity of islands can drive speciation by providing a diversity of niches that promote adaptive radiation and speciation. However, recent studies have argued that phylogenetic niche conservatism, combined with topographical complexity and climate change, could also promote speciation if populations are episodically fragmented into climate refugia that enable allopatric speciation. Adaptive radiation and phylogenetic niche conservatism therefore both predict that topographical complexity should encourage speciation, but they differ strongly in their inferred mechanisms. Using genetic (mitochondrial DNA (mtDNA) and single-nucleotide polymorphism (SNP)) and morphological data, we show high species diversity (22 species) in an endemic clade of Fijian Homalictus bees, with most species restricted to highlands and frequently exhibiting narrow geographical ranges. Our results indicate that elevational niches have been conserved across most speciation events, contradicting expectations from an adaptive radiation model but concordant with phylogenetic niche conservatism. Climate cycles, topographical complexity, and niche conservatism could interact to shape island biodiversity. We argue that phylogenetic niche conservatism is an important driver of tropical island bee biodiversity but that this phylogenetic inertia also leads to major extinction risks for tropical ectotherms under future warming climates.

Elpistostege and the origin of the vertebrate hand.

The evolution of fishes to tetrapods (four-limbed vertebrates) was one of the most important transformations in vertebrate evolution. Hypotheses of tetrapod origins rely heavily on the anatomy of a few tetrapod-like fish fossils from the Middle and Late Devonian period (393-359 million years ago)1. These taxa-known as elpistostegalians-include Panderichthys2, Elpistostege3,4 and Tiktaalik1,5, none of which has yet revealed the complete skeletal anatomy of the pectoral fin. Here we report a 1.57-metre-long articulated specimen of Elpistostege watsoni from the Upper Devonian period of Canada, which represents-to our knowledge-the most complete elpistostegalian yet found. High-energy computed tomography reveals that the skeleton of the pectoral fin has four proximodistal rows of radials (two of which include branched carpals) as well as two distal rows that are organized as digits and putative digits. Despite this skeletal pattern (which represents the most tetrapod-like arrangement of bones found in a pectoral fin to date), the fin retains lepidotrichia (fin rays) distal to the radials. We suggest that the vertebrate hand arose primarily from a skeletal pattern buried within the fairly typical aquatic pectoral fin of elpistostegalians. Elpistostege is potentially the sister taxon of all other tetrapods, and its appendages further blur the line between fish and land vertebrates.

Activity of two key toxin groups in Australian elapid venoms show a strong correlation to phylogeny but not to diet.

BACKGROUND: The relative influence of diet and phylogeny on snake venom activity is a poorly understood aspect of snake venom evolution. We measured the activity of two enzyme toxin groups - phospholipase A2 (PLA2), and L-amino acid oxidase (LAAO) - in the venom of 39 species of Australian elapids (40% of terrestrial species diversity) and used linear parsimony and BayesTraits to investigate any correlation between enzyme activity and phylogeny or diet. RESULTS: PLA2 activity ranged from 0 to 481 nmol/min/mg of venom, and LAAO activity ranged from 0 to 351 nmol/min/mg. Phylogenetic comparative methods, implemented in BayesTraits showed that enzyme activity was strongly correlated with phylogeny, more so for LAAO activity. For example, LAAO activity was absent in both the Vermicella and Pseudonaja/Oxyuranus clade, supporting previously proposed relationships among these disparate taxa. There was no association between broad dietary categories and either enzyme activity. There was strong evidence for faster initial rates of change over evolutionary time for LAAO (delta parameter mean 0.2), but no such pattern in PLA2 (delta parameter mean 0.64). There were some exceptions to the phylogenetic patterns of enzyme activity: different PLA2 activity in the ecologically similar sister-species Denisonia devisi and D. maculata; large inter-specific differences in PLA2 activity in Hoplocephalus and Austrelaps. CONCLUSIONS: We have shown that phylogeny is a stronger influence on venom enzyme activity than diet for two of the four major enzyme families present in snake venoms. PLA2 and LAAO activities had contrasting evolutionary dynamics with the higher delta value for PLA2 Some species/individuals lacked activity in one protein family suggesting that the loss of single protein family may not incur a significant fitness cost.

The morphological diversity of the quadrate bone in squamate reptiles as revealed by high-resolution computed tomography and geometric morphometrics.

We examined the morphological diversity of the quadrate bone in squamate reptiles (i.e. lizards, snakes, amphisbaenians). The quadrate is the principal splanchnocranial element involved in suspending the lower jaw from the skull, and its shape is of particular interest because it is potentially affected by several factors, such as phylogenetic history, allometry, ecology, skull kinesis and hearing capabilities (e.g. presence or absence of a tympanic ear). Due to its complexity, the quadrate bone is also considered one of the most diagnostic elements in fragmentary fossil taxa. We describe quadrates from 38 species spread across all major squamate clades, using qualitative and quantitative (e.g. geometric morphometrics) methods. We test for possible correlations between shape variation and factors such as phylogeny, size, ecology and presence/absence of a tympanum. Our results show that the shape of the quadrate is highly evolutionarily plastic, with very little of the diversity explained by phylogenetic history. Size variation (allometric scaling) is similarly unable to explain much shape diversity in the squamate quadrate. Ecology (terrestrial/fossorial/aquatic) and presence of a tympanic ear are more significant, but together explain only about 20% of the diversity observed. Other unexplored and more analytically complex factors, such as skull biomechanics, likely play additional major roles in shaping the quadrates of lizards and snakes.

The phylogenetic significance of the morphology of the syrinx, hyoid and larynx, of the southern cassowary, Casuarius casuarius (Aves, Palaeognathae).

BACKGROUND: Palaeognathae is a basal clade within Aves and include the large and flightless ratites and the smaller, volant tinamous. Although much research has been conducted on various aspects of palaeognath morphology, ecology, and evolutionary history, there are still areas which require investigation. This study aimed to fill gaps in our knowledge of the Southern Cassowary, Casuarius casuarius, for which information on the skeletal systems of the syrinx, hyoid and larynx is lacking - despite these structures having been recognised as performing key functional roles associated with vocalisation, respiration and feeding. Previous research into the syrinx and hyoid have also indicated these structures to be valuable for determining evolutionary relationships among neognath taxa, and thus suggest they would also be informative for palaeognath phylogenetic analyses, which still exhibits strong conflict between morphological and molecular trees. RESULTS: The morphology of the syrinx, hyoid and larynx of C. casuarius is described from CT scans. The syrinx is of the simple tracheo-bronchial syrinx type, lacking specialised elements such as the pessulus; the hyoid is relatively short with longer ceratobranchials compared to epibranchials; and the larynx is comprised of entirely cartilaginous, standard avian anatomical elements including a concave, basin-like cricoid and fused cricoid wings. As in the larynx, both the syrinx and hyoid lack ossification and all three structures were most similar to Dromaius. We documented substantial variation across palaeognaths in the skeletal character states of the syrinx, hyoid, and larynx, using both the literature and novel observations (e.g. of C. casuarius). Notably, new synapomorphies linking Dinornithiformes and Tinamidae are identified, consistent with the molecular evidence for this clade. These shared morphological character traits include the ossification of the cricoid and arytenoid cartilages, and an additional cranial character, the articulation between the maxillary process of the nasal and the maxilla. CONCLUSION: Syrinx, hyoid and larynx characters of palaeognaths display greater concordance with molecular trees than do other morphological traits. These structures might therefore be less prone to homoplasy related to flightlessness and gigantism, compared to typical morphological traits emphasised in previous phylogenetic studies.