Ontogenetic evidence for the Paleozoic ancestry of salamanders

The phylogenetic positions of frogs, salamanders, and caecilians have been difficult to establish. Data matrices based primarily on Paleozoic taxa support a monophyletic origin of all Lissamphibia but have resulted in widely divergent hypotheses of the nature of their common ancestor. Analysis that concentrates on the character states of the stem taxa of the extant orders, in contrast, suggests a polyphyletic origin from divergent Paleozoic clades. Comparison of patterns of larval development in Paleozoic and modern amphibians provides a means to test previous phylogenies based primarily on adult characteristics. This proves to be highly informative in the case of the origin of salamanders. Putative ancestors of salamanders are recognized from the Permo-Carboniferous boundary of Germany on the basis of ontogenetic changes observed in fossil remains of larval growth series. The entire developmental sequence from hatching to metamorphosis is revealed in an assemblage of over 600 specimens from a single locality, all belonging to the genus Apateon. Apateon forms the most speciose genus of the neotenic temnospondyl family Branchiosauridae. The sequence of ossification of individual bones and the changing configuration of the skull closely parallel those observed in the development of primitive living salamanders. These fossils provide a model of how derived features of the salamander skull may have evolved in the context of feeding specializations that appeared in early larval stages of members of the Branchiosauridae. Larvae of Apateon share many unique derived characters with salamanders of the families Hynobiidae, Salamandridae, and Ambystomatidae, which have not been recognized in any other group of Paleozoic amphibians.     

The shape of pterosaur evolution: evidence from the fossil record

Abstract Although pterosaurs are a well‐known lineage of Mesozoic flying reptiles, their fossil record and evolutionary dynamics have never been adequately quantified. On the basis of a comprehensive data set of fossil occurrences correlated with taxon‐specific limb measurements, we show that the geological ages of pterosaur specimens closely approximate hypothesized patterns of phylogenetic divergence. Although the fossil record has expanded greatly in recent years, collectorship still approximates a sigmoid curve over time as many more specimens (and thus taxa) still remain undiscovered, yet our data suggest that the pterosaur fossil record is unbiased by sites of exceptional preservation (lagerstätte). This is because as new species are discovered the number of known formations and sites yielding pterosaur fossils has also increased – this would not be expected if the bulk of the record came from just a few exceptional faunas. Pterosaur morphological diversification is, however, strongly age biased: rarefaction analysis shows that peaks of diversity occur in the Late Jurassic and Early Cretaceous correlated with periods of increased limb disparity. In this respect, pterosaurs appear unique amongst flying vertebrates in that their disparity seems to have peaked relatively late in clade history. Comparative analyses also show that there is little evidence that the evolutionary diversification of pterosaurs was in any way constrained by the appearance and radiation of birds.     

Three extant genera of freshwater thalassiosiroid diatoms from Middle Eocene sediments in northern Canada

The evolutionary history of diatoms is only constrained partially by the fossil record. The timing of several key events, such as initial colonization of freshwater habitats by marine taxa, remains poorly resolved. Numerous specimens of the genera Cyclotella, Discostella, and Puncticulata (Ochrophyta: Thalassiosirales) have been recovered in Middle Eocene lacustrine sediments from the Giraffe Pipe locality in the Northwest Territories, Canada. These diatoms extend the fossil record of the family Stephanodiscaceae to at least 40 million years before present (Ma) and thus provide a new evolutionary milepost for the thalassiosiroid diatoms, an important clade of centric diatoms with global representation in both marine and freshwater environments. The quality of the fossil material enables detailed investigations of areolae, fultoportulae, and rimoportulae, revealing direct morphological affinities with a number of extant taxa. These observations extend the antiquity of several characters of phylogenetic importance within the thalassiosiroid diatoms, including the fultoportula, and imply that the entire lineage is considerably older than prior constraints from the fossil record, as suggested independently by several recent molecular phylogenies.     

A comparative study of adult facial morphology and its ontogeny in the fossil macaque Macaca majori from Capo Figari, Sardinia, Italy

This study examines the morphology of the face in the fossil macaque Macaca majori from Capo Figari (north-eastern Sardinia, Italy) in a comparative ontogenetic context. Thus, a fairly complete face from an adult representative of this fossil species is compared with 3 extant macaque species: Macaca sylvanus (of which species it is questioned whether it is a subspecies, M. sylvanus majori), Macaca mulatta and Macaca fascicularis. Additional incomplete subadult and adult specimens are also examined in order to compare their facial ontogeny with that of the same living species. The comparisons are based on facial landmark data and are undertaken using geometric morphometric methods. These studies indicate that the adult facial morphology and ontogeny of face size and shape in M. majori share much in common with extant macaque species. However, the adult M. majori face displays some unique morphological features, in particular with regard to lateral flaring and relative size of the zygomatic roots. From the study of a limited sample of fossils there is an indication that this flaring arises during postnatal growth, and in consequence the ontogeny of the face of this fossil species may be different from that of M. sylvanus and the other macaque species included in this analysis. From these studies, we conclude that M. majori shows differences in adult facial morphology and possibly in ontogeny from M. sylvanus compatible with a specific rather than subspecific distinction.     

Incorporating phylogenetic uncertainty on phylogeny‐based palaeontological dating and the timing of turtle diversification

Methods improving the performance of molecular dating of divergence time of clades have improved dramatically in recent years. The calibration of molecular dating using the first appearance of a clade in the fossil record is a crucial step towards inferring the minimal diversification time of various groups and the choice of extinct taxa can strongly influence the molecular dates. Here, we evaluate the uncertainty on the phylogenetic position of extinct taxa through non‐parametric bootstrapping. The recognition of phylogenetic uncertainty resulted in the definition of the Bootstrap Uncertainty Range (BUR) for the age of first appearance of a given clade. The BUR is calculated as the interval of geological time in which the diversification of a given clade can be inferred to have occurred, based on the temporal information of the fossil record and the topologies of the bootstrap trees. Divergence times based on BUR analyses were calculated for three clades of turtles: Testudines, Pleurodira and Cryptodira. This resulted in extensive uncertainty ranges of topology‐dependent minimal divergence dates for these clades.     

Global Completeness of the Bat Fossil Record

Bats are unique among mammals in their use of powered flight and their widespread capacity for laryngeal echolocation. Understanding how and when these and other abilities evolved could be improved by examining the bat fossil record. However, the fossil record of bats is commonly believed to be very poor. Quantitative analyses of this record have rarely been attempted, so it has been difficult to gauge just how depauperate the bat fossil record really is. A crucial step in analyzing the quality of the fossil record is to be able to accurately estimate completeness. Measures of completeness of the fossil record have important consequences for our understanding of evolutionary rates and patterns among bats. In this study, we applied previously developed statistical methods of analyzing completeness to the bat fossil record. The main utility of these methods over others used to study completeness is their independence from phylogeny. This phylogenetic-independence is desirable, given the recent state of flux in the higher-level phylogenetic relationships of bats. All known fossil bat genera were tabulated at the geologic stage or sub-epoch level. This binning strategy allowed an estimate of the extinction rate for each bat genus per bin. Extinction rate—together with per-genus estimates of preservation probability and original temporal distributions—was used to calculate completeness. At the genus level, the bat fossil record is estimated to be 12% complete. Within the order, Pteropodidae is missing most of its fossil history, while Rhinolophoidea and Vespertilionoidea are missing the least. These results suggest that 88% of bats that existed never left a fossil record, and that the fossil record of bats is indeed poor. Much of the taxonomic and evolutionary history of bats has yet to be uncovered.     

Age rank/clade rank metrics--sampling,taxonomy, and the meaning of "stratigraphic consistency"

Paleontologists frequently contrast clade rank (i.e., nodal or patristic distance from the base of a cladogram) with age rank (i.e., relative first known appearances of the analyzed taxa) to measure the degree of congruence between the estimated phylogeny and the fossil record. Although some potential biases of these methods have been examined (e.g., the effect of tree imbalance), other properties of age rank/clade rank (ARCR) comparisons have not been studied in detail. A basic premise of ARCR metrics is that outgroup taxa diverged earlier than ingroups and thus should first appear in older strata. For example, given phylogeny (A,(B,C)), then taxon A should be sampled before either taxon B or taxon C. We examine this premise in the context of (1) phylogenetic theory, (2) taxonomic practice, (3) sampling intensity (R), and (4) factors other than sampling intensity (including cladogram accuracy). Simulations combining clade evolution and sampling over time indicate a poor relationship between ARCR metrics and R when all taxa are apomorphy-based monophyletic groups. However, a good relationship exists when taxa are either stem-based monophyletic groups or if workers include taxa without a priori decisions about monophyly or paraphyly. These results are not surprising because cladograms predict the order in which lineages diverged (which applies to stem-based monophyletic taxa) and the order in which morphologic grades appeared (which applies to paraphyletic taxa relative to derived monophyletic groups). Other factors that increase ARCR metrics when the average R stays the same include high temporal variation in R, budding instead of bifurcating speciation patterns, low extinction rates, cladogram inaccuracy, and (to a much lesser extent) large clade size. These results suggest several plausible explanations for patterned differences in ARCR metrics among clades, thereby compromising their validity as measures of the quality of the fossil record.     

A new holocrinid (Articulata) from the Paris Biota (Bear Lake County,Idaho, USA) highlights the high diversity of Early Triassic crinoids

After the end-Permian crisis and the extinction of their four Paleozoic subclasses, crinoids rapidly recovered. This group is classically believed to have radiated from a small surviving clade and to have diversified during the Middle and Upper Triassic from two lineages. Nevertheless, recent findings suggested that several lineages of crinoids had already diversified during the Early Triassic, and that their diversity has been overlooked. Here we describe a new form of holocrinid, Holocrinus nov. sp., from the earliest Spathian (Early Triassic) of southeastern Idaho (USA). So far, the exceptional completeness of sampled specimens, with skeletal elements of arms and stem in connection, is unique for the Early Triassic. They show that derived morphological features had already evolved ∼1.3 million years after the Permian–Triassic boundary, supporting the scenario of a rapid Early Triassic diversification of crinoids.     

Evolving between land and water: key questions on the emergence and history of the Hippopotamidae (Hippopotamoidea,Cetancodonta, Cetartiodactyla)

The fossil record of the Hippopotamidae can shed light on three major issues in mammalian evolution. First, as the Hippopotamidae are the extant sister group of Cetacea, gaining a better understanding of the origin of the Hippopotamidae and of their Paleogene ancestors will be instrumental in clarifying phylogenetic relationships within Cetartiodactyla. Unfortunately, the data relevant to hippopotamid origins have generally been ignored in phylogenetic analyses of cetartiodactyls. In order to obtain better resolution, future analyses should consider hypotheses of hippopotamid Paleogene relationships. Notably, an emergence of the Hippopotamidae from within anthracotheriids has received growing support, leading to reconciliation between genetic and morphological evidence for the clade Cetancodonta (Hippopotamidae + Cetacea). Secondly, full account needs to be taken of the Hippopotamidae when studying the impact of environmental change on faunal evolution. This group of semi‐aquatic large herbivores has a clear and distinct ecological role and a diverse and abundant fossil record, particularly in the African Neogene. We examine three major phases of hippopotamid evolution, namely the sudden appearance of hippopotamines in the late Miocene (the “Hippopotamine Event”), the subsequent rampant endemism in African basins, and the Pleistocene expansion of Hippopotamus. Each may have been influenced by multiple factors, including: late Miocene grass expansion, African hydrographical network disruption, and a unique set of adaptations that allowed Hippopotamus to respond efficiently to early Pleistocene environmental change. Thirdly, the fossil record of the Hippopotamidae documents the independent emergence of adaptive character complexes in relation to semiaquatic habits and in response to insular isolation. The semiaquatic specializations of fossil hippopotamids are particularly useful in interpreting the functional morphology and ecology of other, extinct groups of large semiaquatic herbivores. Hippopotamids can also serve as models to elucidate the evolutionary dynamics of island mammals.     

Earliest record of fossil insect oothecae confirms the presence of crown-dictyopteran taxa in the Late Triassic

Although dissimilar in their overall appearance and life habits, the praying mantises (Mantodea) and cockroaches (Blattodea, including their eusocial relatives, the termites [Isoptera]) are grouped within the clade Dictyoptera, based on – among other significant characteristics – the laying of eggs in a compound structure called an ootheca. The origin of the Dictyoptera and the currently recognized taxa within is, however, a controversial topic among entomologists. This has resulted from disparities in the divergence age estimates obtained from phylogenetic analyses based on molecular data together with the limited and controversial fossil evidence attributable to these groups. Here, we report two new oothecae ichnospecies found in a Carnian (237 to 227 mya. lowermost Upper Triassic) deposit from Argentina. Morphological comparisons and Scanning Electron Microscope and X-ray Energy Dispersive Spectroscopy analyses of fossil and extant oothecae of mantises and cockroaches were performed in an attempt to solve their systematic placement within Dictyoptera and fossil allies, such as †Alienoptera. In addition to being the earliest known record of oothecae, this discovery moves the origin of this specialized reproductive strategy back by 100 million years. As direct fossil evidence, these specimens provide an important calibration and reference point that can inform future research on the origins and timing of diversification of the Dictyoptera.     

True enamel covering in teeth of the Australian lungfish Neoceratodus forsteri

Lungfish are a unique order of sarcopterygian fish cleidographically positioned between tetrapods and fish. An uninterrupted 400-million-year-old fossil record has documented lungfish skeletal elements to remain virtually unchanged since the Early Devonian. In the current study we investigated the enamel layer of lungfish teeth in order to determine whether there was evidence for higher vertebrate "true" enamel in the Australian lungfish. Juvenile lungfish from the Brisbane River were processed for light and electron microscopy and analyzed for parameters indicative of true enamel formation. Using anti-amelogenin primary antibodies for immunodetection and Western blots, enamel protein epitopes were detected in developing lungfish teeth. Using transmission electron microscopy and electron diffraction analysis, long and parallel-oriented hydroxyapatite crystals were observed in lungfish outer tooth coverings. Our findings indicate that Australian lungfish teeth are covered by a layer of true enamel. Based on the lungfish fossil record we conclude that features of true enamel formation may be as old as 400 million years. Based on taxonomic classification we confirm that true enamel is found not only in tetrapods but also in the sarcopterygian clade of the Gnathostomata.     

Brief communication: two human fossil deciduous molars from the Sangiran dome (Java, Indonesia): outer and inner morphology

Currently, the human deciduous dental record from the Pleistocene deposits of the Sangiran Dome, Java, consists of only eight specimens. Here we report two deciduous crowns collected near the village of Pucung. While their precise geo-chronological context remains unknown, a provenance from the Early-Middle Pleistocene Kabuh Formation, or from the Early Pleistocene "Grenzbank Zone," is very likely. These isolated specimens consist of an upper first molar (PCG.1) and a lower second molar (PCG.2). Taxonomic discrimination of the Indonesian tooth record is difficult because of the convergence in crown size and appearance between Pongo and Homo. Accordingly, as PCG.2 still bears a concretion masking most of its features, we coupled the outer analysis of the two specimens with an investigation of their inner morphology. In addition to external characteristics, virtual imaging and quantitative assessment of inner morphology and tissue proportions support an attribution to the taxon Homo, and we preliminary allocate both specimens toH. erectus.     

Pisanosaurus mertii and the Triassic ornithischian crisis: could phylogeny offer a solution?

Abstract

Two recent studies have independently recovered Pisanosaurus mertii – long thought to represent the oldest known member of Ornithischia – within Silesauridae. These finds are expanded upon here, as are the implications of this hypothesis. Based upon these finds, it now appears that Ornithischia was absent in the Triassic Period entirely, which constitutes a major incongruence between the fossil record and current phylogenetic hypotheses, particularly the traditional model of dinosaur interrelationships in which Ornithischia and Saurischia are sister-taxa. It has been suggested previously that Ornithischia was simply a rare component of Late Triassic faunas, or that perhaps the clade’s ecology or geographic distribution were not conducive to producing a fossil record. Here I propose that phylogeny could hold the solution to this problem. I examine how an alternative position for Ornithischia – nested either within Theropoda or Sauropodomorpha – could be the reason behind their later appearance and relative rarity in the Early Jurassic. An Early Jurassic origin of Ornithischia would force us to consider that the anatomical similarities between ornithischians and Early Jurassic taxa might not be convergences, and to broaden the current datasets of early dinosaurs to test these ideas.     

Interactions within and between clades shaped the diversification of terrestrial carnivores

A longstanding debate in evolutionary biology and paleontology is whether ecological interactions such as competition impose diversity dependence on speciation and extinction rates. Here, we analyze the fossil record of terrestrial mammalian carnivores in North America and Eurasia using a Bayesian framework to assess whether their diversity dynamics were affected by diversity dependence within and between families (12 in Eurasia, 10 in North America). We found eight instances of within‐clade diversity dependence suppressing speciation rates and detected between‐clade effects increasing extinction rates in six instances. Diversity dependence often involved lineages that migrated between continents and we found that speciation was more responsive to diversity changes within the clade, whereas extinction responded to diversity of taxa in other clades. The analysis of the fossil record of Carnivora suggests that interactions within and between clades are associated with different speciation and extinction regimes, opening room for a broader theory of diversity dependence.     

Evo-devo: the evolution of a new discipline

The history of life documented in the fossil record shows that the evolution of complex organisms such as animals and plants has involved marked changes in morphology, and the appearance of new features. However, evolutionary change occurs not by the direct transformation of adult ancestors into adult descendants but rather when developmental processes produce the features of each generation in an evolving lineage. Therefore, evolution cannot be understood without understanding the evolution of development, and how the process of development itself blases or constrains evolution. A revolutionary synthesis of developmental biology and evolution is in progress.     

Dating the origin of the major lineages of Branchiopoda

Despite the well-established phylogeny and good fossil record of branchiopods, a consistent macro-evolutionary timescale for the group remains elusive. This study focuses on the early branchiopod divergence dates where fossil record is extremely fragmentary or missing. On the basis of a large genomic dataset and carefully evaluated fossil calibration points, we assess the quality of the branchiopod fossil record by calibrating the tree against well-established first occurrences, providing paleontological estimates of divergence times and completeness of their fossil record. The maximum age constraints were set using a quantitative approach of Marshall (2008). We tested the alternative placements of Yicaris and Wujicaris in the referred arthropod tree via the likelihood checkpoints method. Divergence dates were calculated using Bayesian relaxed molecular clock and penalized likelihood methods. Our results show that the stem group of Branchiopoda is rooted in the late Neoproterozoic (563 ± 7 Ma); the crown-Branchiopoda diverged during middle Cambrian to Early Ordovician (478–512 Ma), likely representing the origin of the freshwater biota; the Phyllopoda clade diverged during Ordovician (448–480 Ma) and Diplostraca during Late Ordovician to early Silurian (430–457 Ma). By evaluating the congruence between the observed times of appearance of clade in the fossil record and the results derived from molecular data, we found that the uncorrelated rate model gave more congruent results for shallower divergence events whereas the auto-correlated rate model gives more congruent results for deeper events.     

Evolution of antennules of cytheroidean ostracods (Crustacea)

Phylogenetic analysis and fossil records indicate that antennules with whip-like setae are the most plesiomorphic state in cytheroidean ostracods and that antennulae with claw-like setae are derived from antennulae with whip-like setae. Character distributions on the 18S rDNA molecular phylogenetic tree suggest that two phenotypic features of cytheroidean antennules (W/L ratio and claw-like/whip-like setae) have morphological plasticity. These features have evolved as an ethological adaptation rather than due to phylogenetic constraints such as the evolution of shell outline in cytheroideans. However, the species of the Leptocytheridae–Trachyleberididae clade generally have stout, robust antennules, indicating a phylogenetic constraint. The character state of setae (claw/whip) in cytheroidean ostracods is reflected more through their ethology than the W/L ratio of the antennules. On the basis of the present analysis and the fossil record, diversification in the morphology of the antennules seems to have occurred during the early Mesozoic.     

Is Palaeospondylus gunni a fossil larval lungfish? Insights from Neoceratodus forsteri development

The enigmatic Devonian fossil Palaeospondylus gunni was identified as a larval form, metamorphosing into the lungfish Dipterus valenciennesi. Morphological features used to identify P. gunni as a larval lungfish include enlarged cranial ribs, rudimentary limb girdles, and absence of teeth. However, this combination of features does not characterize the extant lungfish Neoceratodus forsteri, even at very young stages, nor early stages of Devonian and younger fossil lungfish. Absence of teeth is problematic because early ontogenetic stages of fossil and living lungfish possess full dentitions including marginal teeth. Also problematic are cranial ribs as a defining character of lungfish, as these also occur in certain actinopterygians.It is argued that Neoceratodus is an obligate neotene (reproductively mature larva), with the implication that metamorphosis was a feature of the ontogeny of early lungfish. Pedomorphic characters have been recognized in Neoceratodus and other post-Devonian lungfish, including large cells and correspondingly large genome size; these latter characters correlate with neoteny in salamanders. Small cells preserved in fossil bone suggest that Devonian lungfish had a smaller genome than post-Devonian lungfish, implying that they were not neotenic. As fossil lungfish cell sizes (and genomes) increased in the late Paleozoic, the diversity of lungfish morphologies decreased, so that taxa like Sagenodus and Conchopoma show morphological similarity to Neoceratodus, marking a point in phylogeny at which metamorphosis was potentially lost. Since ancestral larval characters are retained in neotenic adults, we predict that Devonian larvae should resemble these post-Devonian taxa, a prediction which Palaeospondylus does not fulfill.     

LIFE-CYCLE EVOLUTION AS RESPONSE TO DIVERSE LAKE HABITATS IN PALEOZOIC AMPHIBIANS

The evolution of life cycles forms the subject of numerous studies on extant organisms, but is rarely documented in the fossil record. Here, I analyze patterns of development in time-averaged samples of late Carboniferous and early Permian amphibians, and compare them to paleoecological patterns derived from the same deposits located within a large sedimentary basin (Saar-Nahe, Germany). In 300-297 million years (myr) old Sclerocephalus haeuseri (1–1.7 m), adult size, morphology, and the course of ontogeny varied with respect to the habitats in which the species existed. These differences are best exemplified by ontogenetic trajectories, which reveal a full range of modifications correlating with environmental parameters (lake properties, food resources, competitors). In a 2- to 3-myr-long interval, six different lake habitats were inhabited by this species, which responded to changes by modification of growth rate, adult size, developmental sequence, skeletal features, prey preference, and relative degree of terrestriality.