91 results on '"Ahlberg PE"'
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2. Morphology and histology of acanthodian fin spines from the late Silurian Ramsåsa E locality, Skåne, Swede
- Author
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Jerve, A, primary, Bremer, O, additional, Sanchez, S, additional, and Ahlberg, PE, additional
- Published
- 2017
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3. Uniquely preserved gut contents illuminate trilobite palaeophysiology.
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Kraft P, Vaškaninová V, Mergl M, Budil P, Fatka O, and Ahlberg PE
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- Animals, Biological Evolution, Crustacea enzymology, Synchrotrons, Hydrogen-Ion Concentration, Aquatic Organisms enzymology, Aquatic Organisms physiology, Arthropods anatomy & histology, Arthropods enzymology, Arthropods physiology, Fossils, Intestines chemistry, Intestines enzymology, Intestines metabolism
- Abstract
Trilobites are among the most iconic of fossils and formed a prominent component of marine ecosystems during most of their 270-million-year-long history from the early Cambrian period to the end Permian period
1 . More than 20,000 species have been described to date, with presumed lifestyles ranging from infaunal burrowing to a planktonic life in the water column2 . Inferred trophic roles range from detritivores to predators, but all are based on indirect evidence such as body and gut morphology, modes of preservation and attributed feeding traces; no trilobite specimen with internal gut contents has been described3,4 . Here we present the complete and fully itemized gut contents of an Ordovician trilobite, Bohemolichas incola, preserved three-dimensionally in a siliceous nodule and visualized by synchrotron microtomography. The tightly packed, almost continuous gut fill comprises partly fragmented calcareous shells indicating high feeding intensity. The lack of dissolution of the shells implies a neutral or alkaline environment along the entire length of the intestine supporting digestive enzymes comparable to those in modern crustaceans or chelicerates. Scavengers burrowing into the trilobite carcase targeted soft tissues below the glabella but avoided the gut, suggesting noxious conditions and possibly ongoing enzymatic activity., (© 2023. The Author(s).)- Published
- 2023
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4. Ancient vertebrate dermal armor evolved from trunk neural crest.
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Stundl J, Martik ML, Chen D, Raja DA, Franěk R, Pospisilova A, Pšenička M, Metscher BD, Braasch I, Haitina T, Cerny R, Ahlberg PE, and Bronner ME
- Subjects
- Animals, Skull, Osteogenesis, Fishes, Biological Evolution, Neural Crest, Vertebrates genetics
- Abstract
Bone is an evolutionary novelty of vertebrates, likely to have first emerged as part of ancestral dermal armor that consisted of osteogenic and odontogenic components. Whether these early vertebrate structures arose from mesoderm or neural crest cells has been a matter of considerable debate. To examine the developmental origin of the bony part of the dermal armor, we have performed in vivo lineage tracing in the sterlet sturgeon, a representative of nonteleost ray-finned fish that has retained an extensive postcranial dermal skeleton. The results definitively show that sterlet trunk neural crest cells give rise to osteoblasts of the scutes. Transcriptional profiling further reveals neural crest gene signature in sterlet scutes as well as bichir scales. Finally, histological and microCT analyses of ray-finned fish dermal armor show that their scales and scutes are formed by bone, dentin, and hypermineralized covering tissues, in various combinations, that resemble those of the first armored vertebrates. Taken together, our results support a primitive skeletogenic role for the neural crest along the entire body axis, that was later progressively restricted to the cranial region during vertebrate evolution. Thus, the neural crest was a crucial evolutionary innovation driving the origin and diversification of dermal armor along the entire body axis.
- Published
- 2023
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5. Response to comment on "Exceptional preservation of organs in Devonian placoderms from the Gogo largerstätte".
- Author
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Trinajstic K, Long J, Sanchez S, Boisvert CA, Snitting D, Tafforeau P, Dupret V, Clement AM, Currie PD, Roelofs B, Bevitt JJ, Lee MSY, and Ahlberg PE
- Subjects
- Animals, Fishes physiology, Biological Evolution, Fossils, Preservation, Biological, Heart
- Abstract
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.
- Published
- 2023
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6. The Bothriolepis (Placodermi, Antiarcha) material from the Valentia Slate Formation of the Iveragh Peninsula (middle Givetian, Ireland): Morphology, evolutionary and systematic considerations, phylogenetic and palaeogeographic implications.
- Author
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Dupret V, Byrne HM, Castro N, Hammer Ø, Higgs KT, Long JA, Niedźwiedzki G, Qvarnström M, Stössel I, and Ahlberg PE
- Subjects
- Animals, Phylogeny, Ireland, China, Biological Evolution, Skull
- Abstract
Material of the antiarch placoderm Bothriolepis from the middle Givetian of the Valentia Slate Formation in Iveragh Peninsula, Ireland, is described and attributed to a new species, B. dairbhrensis sp. nov. A revision of the genus Bothriolepis is proposed, and its taxonomic content and previous phylogenetic analyses are reviewed, as well as the validity of morphologic characteristics considered important for the establishment of the genus, such as the shape of the preorbital recess of the neurocranium. A series of computerised phylogenetic analyses was performed, which reveals that our new species is the sister taxon to the Frasnian Scottish form B. gigantea. New phylogenetic and biogeographic analyses of the genus Bothriolepis together with comparisons between faunal assemblages reveal a first northward dispersal wave from Gondwana to Euramerica at the latest in the mid Givetian. Other Euramerican species of Bothriolepis seem to belong to later dispersal waves from Gondwana, non-excluding southward waves from Euramerica. Questions remain open such as the taxonomic validity and stratigraphic constraints for the most ancient forms of Bothriolepis in China, and around the highly speciose nature of the genus., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2023 Dupret et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)
- Published
- 2023
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7. A high latitude Gondwanan species of the Late Devonian tristichopterid Hyneria (Osteichthyes: Sarcopterygii).
- Author
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Gess RW and Ahlberg PE
- Subjects
- Animals, Phylogeny, Jaw anatomy & histology, Skull anatomy & histology, Fossils, Vertebrates anatomy & histology, Fishes
- Abstract
We describe the largest bony fish in the Late Devonian (late Famennian) fossil assemblage from Waterloo Farm near Makhanda/Grahamstown, South Africa. It is a giant member of the extinct clade Tristichopteridae (Sarcopterygii: Tetrapodomorpha) and most closely resembles Hyneria lindae from the late Famennian Catskill Formation of Pennsylvania, USA. Notwithstanding the overall similarity, it can be distinguished from H. lindae on a number of morphological points and is accordingly described as a new species, H. udlezinye sp. nov. The preserved material comprises most of the dermal skull, lower jaw, gill cover and shoulder girdle. The cranial endoskeleton appears to have been unossified and is not preserved, apart from a fragment of the hyoid arch adhering to a subopercular, but the postcranial endoskeleton is represented by an ulnare, some semi-articulated neural spines, and the basal plate of a median fin. The discovery of H. udlezinye shows that Hyneria is a cosmopolitan genus extending into the high latitudes of Gondwana, not a Euramerican endemic. It supports the contention that the derived clade of giant tristichopterids, which alongside Hyneria includes such genera as Eusthenodon, Edenopteron and Mandageria, originated in Gondwana., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2023 Gess, Ahlberg. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)
- Published
- 2023
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8. Exceptional preservation of organs in Devonian placoderms from the Gogo lagerstätte.
- Author
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Trinajstic K, Long JA, Sanchez S, Boisvert CA, Snitting D, Tafforeau P, Dupret V, Clement AM, Currie PD, Roelofs B, Bevitt JJ, Lee MSY, and Ahlberg PE
- Subjects
- Animals, Jaw anatomy & histology, Phylogeny, Western Australia, Biological Evolution, Catfishes anatomy & histology, Catfishes classification, Fossils
- Abstract
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.
- Published
- 2022
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9. The oldest complete jawed vertebrates from the early Silurian of China.
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Zhu YA, Li Q, Lu J, Chen Y, Wang J, Gai Z, Zhao W, Wei G, Yu Y, Ahlberg PE, and Zhu M
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- Animals, China, Fishes anatomy & histology, Fishes classification, Phylogeny, Skull anatomy & histology, Fossils, Jaw anatomy & histology, Vertebrates anatomy & histology, Vertebrates classification
- Abstract
Molecular studies suggest that the origin of jawed vertebrates was no later than the Late Ordovician period (around 450 million years ago (Ma))
1,2 . Together with disarticulated micro-remains of putative chondrichthyans from the Ordovician and early Silurian period3-8 , these analyses suggest an evolutionary proliferation of jawed vertebrates before, and immediately after, the end-Ordovician mass extinction. However, until now, the earliest complete fossils of jawed fishes for which a detailed reconstruction of their morphology was possible came from late Silurian assemblages (about 425 Ma)9-13 . The dearth of articulated, whole-body fossils from before the late Silurian has long rendered the earliest history of jawed vertebrates obscure. Here we report a newly discovered Konservat-Lagerstätte, which is marked by the presence of diverse, well-preserved jawed fishes with complete bodies, from the early Silurian (Telychian age, around 436 Ma) of Chongqing, South China. The dominant species, a 'placoderm' or jawed stem gnathostome, which we name Xiushanosteus mirabilis gen. et sp. nov., combines characters from major placoderm subgroups14-17 and foreshadows the transformation of the skull roof pattern from the placoderm to the osteichthyan condition10 . The chondrichthyan Shenacanthus vermiformis gen. et sp. nov. exhibits extensive thoracic armour plates that were previously unknown in this lineage, and include a large median dorsal plate as in placoderms14-16 , combined with a conventional chondrichthyan bauplan18,19 . Together, these species reveal a previously unseen diversification of jawed vertebrates in the early Silurian, and provide detailed insights into the whole-body morphology of the jawed vertebrates of this period., (© 2022. The Author(s), under exclusive licence to Springer Nature Limited.)- Published
- 2022
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10. Morphometric analysis of lungfish endocasts elucidates early dipnoan palaeoneurological evolution.
- Author
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Clement AM, Challands TJ, Cloutier R, Houle L, Ahlberg PE, Collin SP, and Long JA
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- Animals, Brain diagnostic imaging, Fishes, Paleontology, Skull anatomy & histology, Skull diagnostic imaging, Biological Evolution, Fossils
- Abstract
The lobe-finned fish, lungfish (Dipnoi, Sarcoptergii), have persisted for ~400 million years from the Devonian Period to present day. The evolution of their dermal skull and dentition is relatively well understood, but this is not the case for the central nervous system. While the brain has poor preservation potential and is not currently known in any fossil lungfish, substantial indirect information about it and associated structures (e.g. labyrinths) can be obtained from the cranial endocast. However, before the recent development of X-ray tomography as a palaeontological tool, these endocasts could not be studied non-destructively, and few detailed studies were undertaken. Here, we describe and illustrate the endocasts of six Palaeozoic lungfish from tomographic scans. We combine these with six previously described digital lungfish endocasts (4 fossil and 2 recent taxa) into a 12-taxon dataset for multivariate morphometric analysis using 17 variables. We find that the olfactory region is more highly plastic than the hindbrain, and undergoes significant elongation in several taxa. Further, while the semicircular canals covary as an integrated module, the utriculus and sacculus vary independently of each other. Functional interpretation suggests that olfaction has remained a dominant sense throughout lungfish evolution, and changes in the labyrinth may potentially reflect a change from nektonic to near-shore environmental niches. Phylogenetic implications show that endocranial form fails to support monophyly of the 'chirodipterids'. Those with elongated crania similarly fail to form a distinct clade, suggesting these two paraphyletic groups have converged towards either head elongation or truncation driven by non-phylogenetic constraints., Competing Interests: AC, TC, RC, LH, PA, SC, JL No competing interests declared, (© 2022, Clement et al.)
- Published
- 2022
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11. Feeding ecology has shaped the evolution of modern sharks.
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Bazzi M, Campione NE, Kear BP, Pimiento C, and Ahlberg PE
- Subjects
- Animals, Ecology, Ecosystem, Extinction, Biological, Fossils, Sharks anatomy & histology
- Abstract
Sharks are iconic predators in today's oceans, yet their modern diversity has ancient origins. In particular, present hypotheses suggest that a combination of mass extinction, global climate change, and competition has regulated the community structure of dominant mackerel (Lamniformes) and ground (Carcharhiniformes) sharks over the last 66 million years. However, while these scenarios advocate an interplay of major abiotic and biotic events, the precise drivers remain obscure. Here, we focus on the role of feeding ecology using a geometric morphometric analysis of 3,837 fossil and extant shark teeth. Our results reveal that morphological segregation rather than competition has characterized lamniform and carcharhiniform evolution. Moreover, although lamniforms suffered a long-term disparity decline potentially linked to dietary "specialization," their recent disparity rivals that of "generalist" carcharhiniforms. We further confirm that low eustatic sea levels impacted lamniform disparity across the end-Cretaceous mass extinction. Adaptations to changing prey availability and the proliferation of coral reef habitats during the Paleogene also likely facilitated carcharhiniform dispersals and cladogenesis, underpinning their current taxonomic dominance. Ultimately, we posit that trophic partitioning and resource utilization shaped past shark ecology and represent critical determinants for their future species survivorship., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2021 The Author(s). Published by Elsevier Inc. All rights reserved.)
- Published
- 2021
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12. Age constraints for the Trachilos footprints from Crete.
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Kirscher U, El Atfy H, Gärtner A, Dallanave E, Munz P, Niedźwiedzki G, Athanassiou A, Fassoulas C, Linnemann U, Hofmann M, Bennett M, Ahlberg PE, and Böhme M
- Abstract
We present an updated time frame for the 30 m thick late Miocene sedimentary Trachilos section from the island of Crete that contains the potentially oldest hominin footprints. The section is characterized by normal magnetic polarity. New and published foraminifera biostratigraphy results suggest an age of the section within the Mediterranean biozone MMi13d, younger than ~ 6.4 Ma. Calcareous nannoplankton data from sediments exposed near Trachilos and belonging to the same sub-basin indicate deposition during calcareous nannofossil biozone CN9bB, between 6.023 and 6.727 Ma. By integrating the magneto- and biostratigraphic data we correlate the Trachilos section with normal polarity Chron C3An.1n, between 6.272 and 6.023 Ma. Using cyclostratigraphic data based on magnetic susceptibility, we constrain the Trachilos footprints age at ~ 6.05 Ma, roughly 0.35 Ma older than previously thought. Some uncertainty remains related to an inaccessible interval of ~ 8 m section and the possibility that the normal polarity might represent the slightly older Chron C3An.2n. Sediment accumulation rate and biostratigraphic arguments, however, stand against these points and favor a deposition during Chron C3An.1n., (© 2021. The Author(s).)
- Published
- 2021
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13. Tooth morphology elucidates shark evolution across the end-Cretaceous mass extinction.
- Author
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Bazzi M, Campione NE, Ahlberg PE, Blom H, and Kear BP
- Subjects
- Animals, Ecosystem, Biological Evolution, Extinction, Biological, Fossils anatomy & histology, Sharks anatomy & histology, Tooth anatomy & histology
- Abstract
Sharks (Selachimorpha) are iconic marine predators that have survived multiple mass extinctions over geologic time. Their prolific fossil record is represented mainly by isolated shed teeth, which provide the basis for reconstructing deep time diversity changes affecting different selachimorph clades. By contrast, corresponding shifts in shark ecology, as measured through morphological disparity, have received comparatively limited analytical attention. Here, we use a geometric morphometric approach to comprehensively examine tooth morphologies in multiple shark lineages traversing the catastrophic end-Cretaceous mass extinction-this event terminated the Mesozoic Era 66 million years ago. Our results show that selachimorphs maintained virtually static levels of dental disparity in most of their constituent clades across the Cretaceous-Paleogene interval. Nevertheless, selective extinctions did impact apex predator species characterized by triangular blade-like teeth. This is particularly evident among lamniforms, which included the dominant Cretaceous anacoracids. Conversely, other groups, such as carcharhiniforms and orectolobiforms, experienced disparity modifications, while heterodontiforms, hexanchiforms, squaliforms, squatiniforms, and †synechodontiforms were not overtly affected. Finally, while some lamniform lineages disappeared, others underwent postextinction disparity increases, especially odontaspidids, which are typified by narrow-cusped teeth adapted for feeding on fishes. Notably, this increase coincides with the early Paleogene radiation of teleosts as a possible prey source, and the geographic relocation of disparity sampling "hotspots," perhaps indicating a regionally disjunct extinction recovery. Ultimately, our study reveals a complex morphological response to the end-Cretaceous mass extinction and highlights an event that influenced the evolution of modern sharks., Competing Interests: The authors have declared that no competing interests exist.
- Published
- 2021
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14. Exceptionally preserved beetles in a Triassic coprolite of putative dinosauriform origin.
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Qvarnström M, Fikáček M, Vikberg Wernström J, Huld S, Beutel RG, Arriaga-Varela E, Ahlberg PE, and Niedźwiedzki G
- Subjects
- Animals, Phylogeny, Amber, Coleoptera genetics, Fossils
- Abstract
The Triassic was a crucial period for the early evolution and diversification of insects, including Coleoptera
1-3 -the most diverse order of organisms on Earth. The study of Triassic beetles, however, relies almost exclusively on flattened fossils with limited character preservation. Using synchrotron microtomography, we investigated a fragmentary Upper Triassic coprolite, which contains a rich record of 3D-preserved minute beetle remains of Triamyxa coprolithica gen. et sp. nov. Some specimens are nearly complete, preserving delicate structures of the legs and antennae. Most of them are congruent morphologically, implying that they are conspecific. Phylogenetic analyses suggest that T. coprolithica is a member of Myxophaga, a small suborder of beetles with a sparse fossil record, and that it represents the only member of the extinct family Triamyxidae fam. nov. Our findings highlight that coprolites can contain insect remains, which are almost as well preserved as in amber. They are thus an important source of information for exploring insect evolution before the Cretaceous-Neogene "amber time window." Treated as food residues, insect remains preserved in coprolites also have important implications for the paleoecology of insectivores, in this case, likely the dinosauriform Silesaurus opolensis., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved.)- Published
- 2021
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15. Fossilized cell structures identify an ancient origin for the teleost whole-genome duplication.
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Davesne D, Friedman M, Schmitt AD, Fernandez V, Carnevale G, Ahlberg PE, Sanchez S, and Benson RBJ
- Subjects
- Animals, Phylogeny, Evolution, Molecular, Fishes genetics, Fossils, Gene Duplication, Genome, Genomics methods
- Abstract
Teleost fishes comprise one-half of all vertebrate species and possess a duplicated genome. This whole-genome duplication (WGD) occurred on the teleost stem lineage in an ancient common ancestor of all living teleosts and is hypothesized as a trigger of their exceptional evolutionary radiation. Genomic and phylogenetic data indicate that WGD occurred in the Mesozoic after the divergence of teleosts from their closest living relatives but before the origin of the extant teleost groups. However, these approaches cannot pinpoint WGD among the many extinct groups that populate this 50- to 100-million-y lineage, preventing tests of the evolutionary effects of WGD. We infer patterns of genome size evolution in fossil stem-group teleosts using high-resolution synchrotron X-ray tomography to measure the bone cell volumes, which correlate with genome size in living species. Our findings indicate that WGD occurred very early on the teleost stem lineage and that all extinct stem-group teleosts known so far possessed duplicated genomes. WGD therefore predates both the origin of proposed key innovations of the teleost skeleton and the onset of substantial morphological diversification in the clade. Moreover, the early occurrence of WGD allowed considerable time for postduplication reorganization prior to the origin of the teleost crown group. This suggests at most an indirect link between WGD and evolutionary success, with broad implications for the relationship between genomic architecture and large-scale evolutionary patterns in the vertebrate Tree of Life., Competing Interests: The authors declare no competing interest.
- Published
- 2021
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16. A comparative genomic framework for the fish-tetrapod transition.
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Ahlberg PE
- Subjects
- Amphibians anatomy & histology, Amphibians genetics, Animal Fins anatomy & histology, Animal Fins metabolism, Animals, Birds anatomy & histology, Birds genetics, Extremities anatomy & histology, Fishes anatomy & histology, Fishes classification, Gene Expression Profiling methods, Lung anatomy & histology, Lung metabolism, Mammals anatomy & histology, Mammals genetics, Reptiles anatomy & histology, Reptiles genetics, Vertebrates anatomy & histology, Vertebrates classification, Evolution, Molecular, Fishes genetics, Genomics methods, Phylogeny, Vertebrates genetics
- Published
- 2021
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17. Endocast and Bony Labyrinth of a Devonian "Placoderm" Challenges Stem Gnathostome Phylogeny.
- Author
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Zhu YA, Giles S, Young GC, Hu Y, Bazzi M, Ahlberg PE, Zhu M, and Lu J
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- Animals, Bayes Theorem, Biological Evolution, Fishes genetics, Phylogeny, Vertebrates genetics, Ear, Inner, Fossils
- Abstract
Our understanding of the earliest evolution of jawed vertebrates depends on a credible phylogenetic framework for the jawed stem gnathostomes collectively known as "placoderms".
1 However, their relationships, and whether placoderms represent a single radiation or a paraphyletic array, remain contentious.2-13 This uncertainty is compounded by an uneven understanding of anatomy across the group, particularly of the phylogenetically informative braincase and brain cavity-endocast. Based on new tomographic data, we here describe the endocast and bony labyrinth of Brindabellaspis stensioi from the Early Devonian of New South Wales.14 The taxon was commonly recovered as branching near the base of placoderms.5-9 , 11 , 12 , 15-17 Previous studies of Brindabellaspis emphasized its resemblances with fossil jawless fishes in the braincase anatomy14 and endocast proportions1 , 18 and its distinctive features were interpreted as autapomorphies, such as the elongated premedian region.19 Although our three-dimensional data confirmed the resemblance of its endocast to those of jawless vertebrates, we discovered that the inner ear and endolymphatic complex display a repertoire of previously unrecognized characters close to modern or crown-group jawed vertebrates, including a pronounced sinus superior and a vertical duct that connects the endolymphatic sac and the labyrinth cavity. Both parsimony and Bayesian analyses suggest that prevailing hypotheses of placoderm relationships are unstable, with newly revealed anatomy pointing to a radical revision of early gnathostome evolution. Our results call into question the appropriateness of arthrodire-like placoderms as models of primitive gnathostome anatomy and raise questions of homology relating to key cranial features., Competing Interests: Declaration of Interests The authors declare no competing interests., (Copyright © 2020 Elsevier Inc. All rights reserved.)- Published
- 2021
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18. The developmental relationship between teeth and dermal odontodes in the most primitive bony fish Lophosteus .
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Chen D, Blom H, Sanchez S, Tafforeau P, Märss T, and Ahlberg PE
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- Animals, Phylogeny, Skin diagnostic imaging, Synchrotrons, Tooth diagnostic imaging, X-Ray Microtomography, Biological Evolution, Dentition, Fishes anatomy & histology, Fossils, Odontogenesis, Skin anatomy & histology, Tooth anatomy & histology
- Abstract
The ontogenetic trajectory of a marginal jawbone of Lophosteus superbus (Late Silurian, 422 Million years old), the phylogenetically most basal stem osteichthyan, visualized by synchrotron microtomography, reveals a developmental relationship between teeth and dermal odontodes that is not evident from the adult morphology. The earliest odontodes are two longitudinal founder ridges formed at the ossification center. Subsequent odontodes that are added lingually to the ridges turn into conical teeth and undergo cyclic replacement, while those added labially achieve a stellate appearance. Stellate odontodes deposited directly on the bony plate are aligned with the alternate files of teeth, whereas new tooth positions are inserted into the files of sequential addition when a gap appears. Successive teeth and overgrowing odontodes show hybrid morphologies around the oral-dermal boundary, suggesting signal cross-communication. We propose that teeth and dermal odontodes are modifications of a single system, regulated and differentiated by the oral and dermal epithelia., Competing Interests: DC, HB, SS, PT, TM, PA No competing interests declared, (© 2020, Chen et al.)
- Published
- 2020
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19. Specialized Craniofacial Anatomy of a Titanosaurian Embryo from Argentina.
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Kundrát M, Coria RA, Manning TW, Snitting D, Chiappe LM, Nudds J, and Ahlberg PE
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- Animals, Argentina, Biological Evolution, Dinosaurs growth & development, Embryonic Development physiology, Fossils anatomy & histology, Maxillofacial Development physiology, Osteogenesis physiology, Skull growth & development, Dinosaurs embryology, Embryo, Nonmammalian anatomy & histology, Face embryology, Skull embryology
- Abstract
The first dinosaur embryos found inside megaloolithid eggs from Auca Mahuevo, Patagonia, were assigned to sauropod dinosaurs that lived approximately 80 million years ago. Discovered some 25 years ago, these considerably flattened specimens still remain the only unquestionable embryonic remains of a sauropod dinosaur providing an initial glimpse into titanosaurian in ovo ontogeny. Here we describe an almost intact embryonic skull, which indicates the early development of stereoscopic vision, and an unusual monocerotic face for a sauropod. The new fossil also reveals a neurovascular sensory system in the premaxilla and a partly calcified braincase, which potentially refines estimates of its prenatal stage. The embryo was found in an egg with thicker eggshell and a partly different geochemical signature than those from the egg-bearing layers described in Auca Mahuevo. The cranial bones are comparably ossified as in previously described specimens but differ in facial anatomy and size. The new specimen reveals significant heterochrony in cranial ossifications when compared with non-sauropod sauropodomorph embryos, and demonstrates that the specialized craniofacial morphology preceded the postnatal transformation of the skull anatomy in adults of related titanosaurians., Competing Interests: Declaration of Interests The authors declare no competing interests., (Copyright © 2020 Elsevier Inc. All rights reserved.)
- Published
- 2020
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20. Correction to 'A key environmental driver of osteichthyan evolution and the fish-tetrapod transition?'
- Author
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Byrne HM, Green JAM, Balbus SA, and Ahlberg PE
- Abstract
[This corrects the article DOI: 10.1098/rspa.2020.0355.]., (© 2020 The Author(s).)
- Published
- 2020
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21. Tides: A key environmental driver of osteichthyan evolution and the fish-tetrapod transition?
- Author
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Byrne HM, Green JAM, Balbus SA, and Ahlberg PE
- Abstract
Tides are a major component of the interaction between the marine and terrestrial environments, and thus play an important part in shaping the environmental context for the evolution of shallow marine and coastal organisms. Here, we use a dedicated tidal model and palaeogeographic reconstructions from the Late Silurian to early Late Devonian (420 Ma, 400 Ma and 380 Ma, Ma = millions of years ago) to explore the potential significance of tides for the evolution of osteichthyans (bony fish) and tetrapods (land vertebrates). The earliest members of the osteichthyan crown-group date to the Late Silurian, approximately 425 Ma, while the earliest evidence for tetrapods is provided by trackways from the Middle Devonian, dated to approximately 393 Ma, and the oldest tetrapod body fossils are Late Devonian, approximately 373 Ma. Large tidal ranges could have fostered both the evolution of air-breathing organs in osteichthyans to facilitate breathing in oxygen-depleted tidal pools, and the development of weight-bearing tetrapod limbs to aid navigation within the intertidal zones. We find that tidal ranges over 4 m were present around areas of evolutionary significance for the origin of osteichthyans and the fish-tetrapod transition, highlighting the possible importance of tidal dynamics as a driver for these evolutionary processes., Competing Interests: We declare we have no competing interests., (© 2020 The Author(s).)
- Published
- 2020
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22. Marginal dentition and multiple dermal jawbones as the ancestral condition of jawed vertebrates.
- Author
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Vaškaninová V, Chen D, Tafforeau P, Johanson Z, Ekrt B, Blom H, and Ahlberg PE
- Subjects
- Animals, Czech Republic, Electron Microscope Tomography, Fossils, Phylogeny, Synchrotrons, Tooth anatomy & histology, Biological Evolution, Dentition, Jaw anatomy & histology, Vertebrates anatomy & histology, Vertebrates classification
- Abstract
The dentitions of extant fishes and land vertebrates vary in both pattern and type of tooth replacement. It has been argued that the common ancestral condition likely resembles the nonmarginal, radially arranged tooth files of arthrodires, an early group of armoured fishes. We used synchrotron microtomography to describe the fossil dentitions of so-called acanthothoracids, the most phylogenetically basal jawed vertebrates with teeth, belonging to the genera Radotina , Kosoraspis , and Tlamaspis (from the Early Devonian of the Czech Republic). Their dentitions differ fundamentally from those of arthrodires; they are marginal, carried by a cheekbone or a series of short dermal bones along the jaw edges, and teeth are added lingually as is the case in many chondrichthyans (cartilaginous fishes) and osteichthyans (bony fishes and tetrapods). We propose these characteristics as ancestral for all jawed vertebrates., (Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)
- Published
- 2020
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23. The smallest known Devonian tetrapod shows unexpectedly derived features.
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Ahlberg PE and Clack JA
- Abstract
A new genus and species of Devonian tetrapod, Brittagnathus minutus gen. et sp. nov., is described from a single complete right lower jaw ramus recovered from the Acanthostega mass-death deposit in the upper part of the Britta Dal Formation (upper Famennian) of Stensiö Bjerg, Gauss Peninsula, East Greenland. Visualization by propagation phase contrast synchrotron microtomography allows a complete digital dissection of the specimen. With a total jaw ramus length of 44.8 mm, Brittagnathus is by far the smallest Devonian tetrapod described to date. It differs from all previously known Devonian tetrapods in having only a fang pair without a tooth row on the anterior coronoid and a large posterior process on the posterior coronoid. The presence of an incipient surangular crest and a concave prearticular margin to the adductor fossa together cause the fossa to face somewhat mesially, reminiscent of the condition in Carboniferous tetrapods. A phylogenetic analysis places Brittagnathus crownward to other Devonian tetrapods, adjacent to the Tournaisian genus Pederpes . Together with other recent discoveries, it suggests that diversification of 'Carboniferous-grade' tetrapods had already begun before the end of the Devonian and that the group was not greatly affected by the end-Devonian mass extinction., Competing Interests: We declare we have no competing interests., (© 2020 The Authors.)
- Published
- 2020
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24. Morphology of the earliest reconstructable tetrapod Parmastega aelidae.
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Beznosov PA, Clack JA, Lukševičs E, Ruta M, and Ahlberg PE
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- Animals, Bayes Theorem, Palate anatomy & histology, Russia, Skull anatomy & histology, Vertebrates classification, Fossils, Phylogeny, Vertebrates anatomy & histology
- Abstract
The known diversity of tetrapods of the Devonian period has increased markedly in recent decades, but their fossil record consists mostly of tantalizing fragments
1-15 . The framework for interpreting the morphology and palaeobiology of Devonian tetrapods is dominated by the near complete fossils of Ichthyostega and Acanthostega; the less complete, but partly reconstructable, Ventastega and Tulerpeton have supporting roles2,4,16-34 . All four of these genera date to the late Famennian age (about 365-359 million years ago)-they are 10 million years younger than the earliest known tetrapod fragments5,10 , and nearly 30 million years younger than the oldest known tetrapod footprints35 . Here we describe Parmastega aelidae gen. et sp. nov., a tetrapod from Russia dated to the earliest Famennian age (about 372 million years ago), represented by three-dimensional material that enables the reconstruction of the skull and shoulder girdle. The raised orbits, lateral line canals and weakly ossified postcranial skeleton of P. aelidae suggest a largely aquatic, surface-cruising animal. In Bayesian and parsimony-based phylogenetic analyses, the majority of trees place Parmastega as a sister group to all other tetrapods.- Published
- 2019
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25. Filter feeding in Late Jurassic pterosaurs supported by coprolite contents.
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Qvarnström M, Elgh E, Owocki K, Ahlberg PE, and Niedźwiedzki G
- Abstract
Diets of pterosaurs have mainly been inferred from indirect evidence such as comparative anatomy, associations of co-occurring fossils, and functional morphology. Gut contents are rare, and until now there is only a single coprolite (fossil dropping), with unidentified inclusions, known. Here we describe three coprolites collected from a palaeosurface with numerous pterosaur tracks found in early Kimmeridgian (Hypselocyclum Zone) intertidal deposits of the Wierzbica Quarry, Poland. The specimens' morphology and association to the tracks suggest a pterosaur producer. Synchrotron scans reveal numerous small inclusions, with foraminifera making up the majority of the identifiable ones. Other small remains include shells/carapaces (of bivalves, ostracods, and other crustaceans/arthropods) and bristles (some possibly of polychaete worms). The high density of the small shelly inclusions suggest that they were not accidently ingested, but constituted an important food source for the pterosaur(s), perhaps together with unpreserved soft-bodied animals. The combined evidence from the tracks and coprolites suggest a filter-feeding ctenochasmatid as the most likely tracemaker. If true, this significantly expands the bromalite record for this pterosaur group, which was previously only known from gastroliths. Moreover, this study also provides the first direct evidence of filter feeding in Jurassic pterosaurs and shows that they had a similar diet to the recent Chilean flamingo ( Phoenicopterus chilensis )., Competing Interests: The authors declare there are no competing interests.
- Published
- 2019
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26. Beetle-bearing coprolites possibly reveal the diet of a Late Triassic dinosauriform.
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Qvarnström M, Wernström JV, Piechowski R, Tałanda M, Ahlberg PE, and Niedźwiedzki G
- Abstract
Diets of extinct animals can be difficult to analyse if no direct evidence, such as gut contents, is preserved in association with body fossils. Inclusions from coprolites (fossil faeces), however, may also reflect the diet of the host animal and become especially informative if the coprolite producer link can be established. Here we describe, based on propagation phase-contrast synchrotron microtomography (PPC-SRμCT), the contents of five morphologically similar coprolites collected from two fossil-bearing intervals from the highly fossiliferous Upper Triassic locality at Krasiejów in Silesia, Poland. Beetle remains, mostly elytra, and unidentified exoskeleton fragments of arthropods are the most conspicuous inclusions found in the coprolites. The abundance of these inclusions suggests that the coprolite producer deliberately targeted beetles and similar small terrestrial invertebrates as prey, but the relatively large size of the coprolites shows that it was not itself a small animal. The best candidate from the body fossil record of the locality is the dinosauriform Silesaurus opolensis Dzik, 2003, which had an anatomy in several ways similar to those of bird-like neotheropod dinosaurs and modern birds. We hypothesize that the beak-like jaws of S. opolensis were used to efficiently peck small insects off the ground, a feeding behaviour analogous to some extant birds., Competing Interests: The authors declare no competing interests.
- Published
- 2019
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27. Tyrannosaurid-like osteophagy by a Triassic archosaur.
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Qvarnström M, Ahlberg PE, and Niedźwiedzki G
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- Animals, Poland, Biological Evolution, Dinosaurs anatomy & histology, Dinosaurs classification, Dinosaurs physiology, Feeding Behavior physiology, Fossils
- Abstract
Here we present evidence for osteophagy in the Late Triassic archosaur Smok wawelski Niedźwiedzki, Sulej and Dzik, 2012, a large theropod-like predator from Poland. Ten medium to large-sized coprolites are matched, by their dimensions and by association with body fossils and footprints, to S. wawelski. The coprolites contain fragments of large serrated teeth as well as up to 50 percent by volume of bone fragments, with distinct fragmentation and angularity, from several prey taxa. This suggests pronounced osteophagy. Further evidence for bone-crushing behaviour is provided by isolated worn teeth, bone-rich regurgitalites (fossil regurgitates) and numerous examples of crushed or bite-marked dicynodont bones, all collected from the same bone-bearing beds in the Lipie Śląskie clay-pit. Several of the anatomical characters related to osteophagy, such as a massive head and robust body, seem to be shared by S. wawelski and the tyrannosaurids, despite their wide phylogenetic separation. These large predators thus provide evidence of convergence driven by similar feeding ecology at the beginning and end of the age of dinosaurs.
- Published
- 2019
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28. Soft-tissue evidence for homeothermy and crypsis in a Jurassic ichthyosaur.
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Lindgren J, Sjövall P, Thiel V, Zheng W, Ito S, Wakamatsu K, Hauff R, Kear BP, Engdahl A, Alwmark C, Eriksson ME, Jarenmark M, Sachs S, Ahlberg PE, Marone F, Kuriyama T, Gustafsson O, Malmberg P, Thomen A, Rodríguez-Meizoso I, Uvdal P, Ojika M, and Schweitzer MH
- Subjects
- Adaptation, Physiological, Adipose Tissue anatomy & histology, Adipose Tissue chemistry, Animals, Dermis anatomy & histology, Dermis chemistry, Dolphins, Epidermis anatomy & histology, Epidermis chemistry, Female, Keratinocytes chemistry, Lipids analysis, Male, Melanins analysis, Melanophores chemistry, Porpoises, Proteins analysis, Biological Evolution, Body Temperature Regulation, Dinosaurs anatomy & histology, Dinosaurs physiology, Fossils, Homeostasis
- Abstract
Ichthyosaurs are extinct marine reptiles that display a notable external similarity to modern toothed whales. Here we show that this resemblance is more than skin deep. We apply a multidisciplinary experimental approach to characterize the cellular and molecular composition of integumental tissues in an exceptionally preserved specimen of the Early Jurassic ichthyosaur Stenopterygius. Our analyses recovered still-flexible remnants of the original scaleless skin, which comprises morphologically distinct epidermal and dermal layers. These are underlain by insulating blubber that would have augmented streamlining, buoyancy and homeothermy. Additionally, we identify endogenous proteinaceous and lipid constituents, together with keratinocytes and branched melanophores that contain eumelanin pigment. Distributional variation of melanophores across the body suggests countershading, possibly enhanced by physiological adjustments of colour to enable photoprotection, concealment and/or thermoregulation. Convergence of ichthyosaurs with extant marine amniotes thus extends to the ultrastructural and molecular levels, reflecting the omnipresent constraints of their shared adaptation to pelagic life.
- Published
- 2018
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29. Unique pelvic fin in a tetrapod-like fossil fish, and the evolution of limb patterning.
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Jeffery JE, Storrs GW, Holland T, Tabin CJ, and Ahlberg PE
- Subjects
- Animal Fins embryology, Animals, Biological Evolution, Extremities anatomy & histology, Femur anatomy & histology, Fishes anatomy & histology, Fishes classification, Fossils anatomy & histology, Phylogeny, Skeleton, Animal Fins anatomy & histology, Body Patterning physiology, Extremities embryology
- Abstract
All living tetrapods have a one-to-two branching pattern in the embryonic proximal limb skeleton, with a single element at the base of the limb (the humerus or femur) that articulates distally with two parallel radials (the ulna and radius or the tibia and fibula). This pattern is also seen in the fossilized remains of stem-tetrapods, including the fishlike members of the group, in which despite the absence of digits, the proximal parts of the fin skeleton clearly resemble those of later tetrapods. However, little is known about the developmental mechanisms that establish and canalize this highly conserved pattern. We describe the well-preserved pelvic fin skeleton of Rhizodus hibberti , a Carboniferous sarcopterygian (lobe-finned) fish, and member of the tetrapod stem group. In this specimen, three parallel radials, each robust with a distinct morphology, articulate with the femur. We review this unexpected morphology in a phylogenetic and developmental context. It implies that the developmental patterning mechanisms seen in living tetrapods, now highly constrained, evolved from mechanisms flexible enough to accommodate variation in the zeugopod (even between pectoral and pelvic fins), while also allowing each element to have a unique morphology., Competing Interests: The authors declare no conflict of interest., (Copyright © 2018 the Author(s). Published by PNAS.)
- Published
- 2018
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30. Static Dental Disparity and Morphological Turnover in Sharks across the End-Cretaceous Mass Extinction.
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Bazzi M, Kear BP, Blom H, Ahlberg PE, and Campione NE
- Subjects
- Animals, Biological Evolution, Tooth anatomy & histology, Dentition, Extinction, Biological, Fossils anatomy & histology, Sharks anatomy & histology
- Abstract
The Cretaceous-Palaeogene (K-Pg) mass extinction profoundly altered vertebrate ecosystems and prompted the radiation of many extant clades [1, 2]. Sharks (Selachimorpha) were one of the few larger-bodied marine predators that survived the K-Pg event and are represented by an almost-continuous dental fossil record. However, the precise dynamics of their transition through this interval remain uncertain [3]. Here, we apply 2D geometric morphometrics to reconstruct global and regional dental morphospace variation among Lamniformes (Mackerel sharks) and Carcharhiniformes (Ground sharks). These clades are prevalent predators in today's oceans, and were geographically widespread during the late Cretaceous-early Palaeogene. Our results reveal a decoupling of morphological disparity and taxonomic richness. Indeed, shark disparity was nearly static across the K-Pg extinction, in contrast to abrupt declines among other higher-trophic-level marine predators [4, 5]. Nevertheless, specific patterns indicate that an asymmetric extinction occurred among lamniforms possessing low-crowned/triangular teeth and that a subsequent proliferation of carcharhiniforms with similar tooth morphologies took place during the early Paleocene. This compositional shift in post-Mesozoic shark lineages hints at a profound and persistent K-Pg signature evident in the heterogeneity of modern shark communities. Moreover, such wholesale lineage turnover coincided with the loss of many cephalopod [6] and pelagic amniote [5] groups, as well as the explosive radiation of middle trophic-level teleost fishes [1]. We hypothesize that a combination of prey availability and post-extinction trophic cascades favored extant shark antecedents and laid the foundation for their extensive diversification later in the Cenozoic [7-10]., (Copyright © 2018 The Author(s). Published by Elsevier Ltd.. All rights reserved.)
- Published
- 2018
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31. A tetrapod fauna from within the Devonian Antarctic Circle.
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Gess R and Ahlberg PE
- Subjects
- Animals, Antarctic Regions, Fossils, Jaw anatomy & histology, South Africa, Biological Evolution, Vertebrates anatomy & histology
- Abstract
Until now, all known fossils of tetrapods (limbed vertebrates with digits) and near-tetrapods (such as Elpistostege , Tiktaalik , and Panderichthys ) from the Devonian period have come from localities in tropical to subtropical paleolatitudes. Most are from Laurussia, a continent incorporating Europe, Greenland, and North America, with only one body fossil and one footprint locality from Australia representing the southern supercontinent Gondwana. Here we describe two previously unknown tetrapods from the Late Devonian (late Famennian) Gondwana locality of Waterloo Farm in South Africa, then located within the Antarctic Circle, which demonstrate that Devonian tetrapods were not restricted to warm environments and suggest that they may have been global in distribution., (Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)
- Published
- 2018
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32. Neurocranial anatomy of an enigmatic Early Devonian fish sheds light on early osteichthyan evolution.
- Author
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Clement AM, King B, Giles S, Choo B, Ahlberg PE, Young GC, and Long JA
- Subjects
- Animals, Australia, Bayes Theorem, Ear, Inner anatomy & histology, Ear, Inner diagnostic imaging, Ear, Inner physiology, Extinction, Biological, Fishes classification, Fishes physiology, Fossils diagnostic imaging, Fossils history, History, Ancient, Skull diagnostic imaging, Skull physiology, X-Ray Microtomography, Biological Evolution, Fishes anatomy & histology, Fossils anatomy & histology, Phylogeny, Skull anatomy & histology
- Abstract
The skull of ' Ligulalepis ' from the Early Devonian of Australia (AM-F101607) has significantly expanded our knowledge of early osteichthyan anatomy, but its phylogenetic position has remained uncertain. We herein describe a second skull of ' Ligulalepis ' and present micro-CT data on both specimens to reveal novel anatomical features, including cranial endocasts. Several features previously considered to link ' Ligulalepis' with actinopterygians are now considered generalized osteichthyan characters or of uncertain polarity. The presence of a lateral cranial canal is shown to be variable in its development between specimens. Other notable new features include the presence of a pineal foramen, the some detail of skull roof sutures, the shape of the nasal capsules, a placoderm-like hypophysial vein, and a chondrichthyan-like labyrinth system. New phylogenetic analyses place ' Ligulalepis ' as a stem osteichthyan, specifically as the sister taxon to 'psarolepids' plus crown osteichthyans. The precise position of 'psarolepids' differs between parsimony and Bayesian analyses., Competing Interests: AC No competing interests declared, (© 2018, Clement et al.)
- Published
- 2018
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33. Non-marine palaeoenvironment associated to the earliest tetrapod tracks.
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Qvarnström M, Szrek P, Ahlberg PE, and Niedźwiedzki G
- Subjects
- Animals, Paleontology, Biological Evolution, Fossils, Vertebrates
- Abstract
Opinions differ on whether the evolution of tetrapods (limbed vertebrates) from lobe-finned fishes was directly linked to terrestrialization. The earliest known tetrapod fossils, from the Middle Devonian (approximately 390 million years old) of Zachełmie Quarry in Poland, are trackways made by limbs with digits; they document a direct environmental association and thus have the potential to help answer this question. However, the tetrapod identity of the tracks has recently been challenged, despite their well-preserved morphology, on account of their great age and supposedly shallow marine (intertidal or lagoonal) depositional environment. Here we present a new palaeoenvironmental interpretation of the track-bearing interval from Zachełmie, showing that it represents a succession of ephemeral lakes with a restricted and non-marine biota, rather than a marginal marine environment as originally thought. This context suggests that the trackmaker was capable of terrestrial locomotion, consistent with the appendage morphology recorded by the footprints, and thus provides additional support for a tetrapod identification.
- Published
- 2018
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34. Evolution of the vertebrate neurocranium: problems of the premandibular domain and the origin of the trabecula.
- Author
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Kuratani S and Ahlberg PE
- Abstract
The subdivision of the gnathostome neurocranium into an anterior neural crest-derived moiety and a posterior mesodermal moiety has attracted the interest of researchers for nearly two centuries. We present a synthetic scenario for the evolution of this structure, uniting developmental data from living cyclostomes and gnathostomes with morphological data from fossil stem gnathostomes in a common phylogenetic framework. Ancestrally, vertebrates had an anteroposteriorly short forebrain, and the neurocranium was essentially mesodermal; skeletal structures derived from premandibular ectomesenchyme were mostly anterior to the brain and formed part of the visceral arch skeleton. The evolution of a one-piece neurocranial 'head shield' in jawless stem gnathostomes, such as galeaspids and osteostracans, caused this mesenchyme to become incorporated into the neurocranium, but its position relative to the brain and nasohypophyseal duct remained unchanged. Basically similar distribution of the premandibular ectomesenchyme is inferred, even in placoderms, the earliest jawed vertebrates, in which the separation of hypophyseal and nasal placodes obliterated the nasohypophyseal duct, leading to redeployment of this ectomesenchyme between the separate placodes and permitting differentiation of the crown gnathostome trabecula that floored the forebrain. Initially this region was very short, and the bulk of the premandibular cranial part projected anteroventral to the nasal capsule, as in jawless stem gnathostomes. Due to the lengthening of the forebrain, the anteriorly projecting 'upper lip' was lost, resulting in the modern gnathostome neurocranium with a long forebrain cavity floored by the trabeculae., Competing Interests: Not applicableNot applicableThe authors declare that they have no competing interests.Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
- Published
- 2018
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35. Vascularization and odontode structure of a dorsal ridge spine of Romundina stellina Ørvig 1975.
- Author
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Jerve A, Qu Q, Sanchez S, Ahlberg PE, and Haitina T
- Subjects
- Animals, Fossils, Diatoms, Spine anatomy & histology
- Abstract
There are two types of dermal skeletons in jawed vertebrates: placoderms and osteichthyans carry large bony plates (macromery), whereas chondrichthyans and acanthodians are covered by small scales (micromery). Fin spines are one of the last large dermal structures found on micromeric taxa and offer a potential source of histology and morphology that can be compared to those found on macromeric groups. Dermal fin spines offer a variety of morphology but aspects of their growth modes and homology are unclear. Here, we provide detailed descriptions of the microstructure and growth of a dorsal ridge spine from the acanthothoracid placoderm, Romundina stellina, using virtual three-dimensional paleohistological datasets. From these data we identify several layers of dentine ornamentation covering the lateral surfaces of the spine and reconstructed their growth pattern. We show that this spine likely grew posteriorly and proximally from a narrow portion of bone located along the leading edge of the spine. The spine is similarly constructed to the scales with a few exceptions, including the absence of polarized fibers distributed throughout the bone and the presence of a thin layer of perichondral bone. The composition of the spine (semidentine odontodes, dermal bone, perichondral bone) is identical to that of the Romundina dermal plates. These results illustrate the similarities and differences between the dermal tissues in Romundina and indicate that the spine grew differently from the dentinous fin spines from extant and fossil chondrichthyans. The morphology and histology of Romundina is most similar to the fin spine of the probable stem osteichthyan Lophosteus, with a well-developed inner cellular bony base and star-shaped odontodes on the surface. Results from these studies will undoubtedly have impact on our understanding of fossil fin spine histology and evolution, contributing to the on-going revision of early gnathostome phylogeny.
- Published
- 2017
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36. A Devonian tetrapod-like fish reveals substantial parallelism in stem tetrapod evolution.
- Author
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Zhu M, Ahlberg PE, Zhao WJ, and Jia LT
- Subjects
- Animals, Bayes Theorem, Phylogeny, Biological Evolution, Fishes anatomy & histology, Fishes classification
- Abstract
The fossils assigned to the tetrapod stem group document the evolution of terrestrial vertebrates from lobe-finned fishes. During the past 18 years the phylogenetic structure of this stem group has remained remarkably stable, even when accommodating new discoveries such as the earliest known stem tetrapod Tungsenia and the elpistostegid (fish-tetrapod intermediate) Tiktaalik. Here we present a large lobe-finned fish from the Late Devonian period of China that disrupts this stability. It combines characteristics of rhizodont fishes (supposedly a basal branch in the stem group, distant from tetrapods) with derived elpistostegid-like and tetrapod-like characters. This mélange of characters may reflect either detailed convergence between rhizodonts and elpistostegids plus tetrapods, under a phylogenetic scenario deduced from Bayesian inference analysis, or a previously unrecognized close relationship between these groups, as supported by maximum parsimony analysis. In either case, the overall result reveals a substantial increase in homoplasy in the tetrapod stem group. It also suggests that ecological diversity and biogeographical provinciality in the tetrapod stem group have been underestimated.
- Published
- 2017
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37. Hidden morphological diversity among early tetrapods.
- Author
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Pardo JD, Szostakiwskyj M, Ahlberg PE, and Anderson JS
- Subjects
- Animals, Calibration, Extremities anatomy & histology, Fishes anatomy & histology, Osteogenesis, Skull anatomy & histology, Spine anatomy & histology, X-Ray Microtomography, Fossils, Phylogeny
- Abstract
Phylogenetic analysis of early tetrapod evolution has resulted in a consensus across diverse data sets in which the tetrapod stem group is a relatively homogenous collection of medium- to large-sized animals showing a progressive loss of 'fish' characters as they become increasingly terrestrial, whereas the crown group demonstrates marked morphological diversity and disparity. The oldest fossil attributed to the tetrapod crown group is the highly specialized aïstopod Lethiscus stocki, which shows a small size, extreme axial elongation, loss of limbs, spool-shaped vertebral centra, and a skull with reduced centres of ossification, in common with an otherwise disparate group of small animals known as lepospondyls. Here we use micro-computed tomography of the only known specimen of Lethiscus to provide new information that strongly challenges this consensus. Digital dissection reveals extremely primitive cranial morphology, including a spiracular notch, a large remnant of the notochord within the braincase, an open ventral cranial fissure, an anteriorly restricted parasphenoid element, and Meckelian ossifications. The braincase is elongate and lies atop a dorsally projecting septum of the parasphenoid bone, similar to stem tetrapods such as embolomeres. This morphology is consistent in a second aïstopod, Coloraderpeton, although the details differ. Phylogenetic analysis, including critical new braincase data, places aïstopods deep on the tetrapod stem, whereas another major lepospondyl lineage is displaced into the amniotes. These results show that stem group tetrapods were much more diverse in their body plans than previously thought. Our study requires a change in commonly used calibration dates for molecular analyses, and emphasizes the importance of character sampling for early tetrapod evolutionary relationships.
- Published
- 2017
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38. Synchrotron phase-contrast microtomography of coprolites generates novel palaeobiological data.
- Author
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Qvarnström M, Niedźwiedzki G, Tafforeau P, Žigaitė Ž, and Ahlberg PE
- Abstract
Coprolites (fossil faeces) reveal clues to ancient trophic relations, and contain inclusions representing organisms that are rarely preserved elsewhere. However, much information is lost by classical techniques of investigation, which cannot find and image the inclusions in an adequate manner. We demonstrate that propagation phase-contrast synchrotron microtomography (PPC-SRμCT) permits high-quality virtual 3D-reconstruction of coprolite inclusions, exemplified by two coprolites from the Upper Triassic locality Krasiejów, Poland; one of the coprolites contains delicate beetle remains, and the other one a partly articulated fish and fragments of bivalves.
- Published
- 2017
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- View/download PDF
39. Development of cyclic shedding teeth from semi-shedding teeth: the inner dental arcade of the stem osteichthyan Lophosteus .
- Author
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Chen D, Blom H, Sanchez S, Tafforeau P, Märss T, and Ahlberg PE
- Abstract
The numerous cushion-shaped tooth-bearing plates attributed to the stem group osteichthyan Lophosteus superbus , which are argued here to represent an early form of the osteichthyan inner dental arcade, display a previously unknown and presumably primitive mode of tooth shedding by basal hard tissue resorption. They carry regularly spaced, recumbent, gently recurved teeth arranged in transverse tooth files that diverge towards the lingual margin of the cushion. Three-dimensional reconstruction from propagation phase-contrast synchrotron microtomography (PPC-SRµCT) reveals remnants of the first-generation teeth embedded in the basal plate, a feature never previously observed in any taxon. These teeth were shed by semi-basal resorption with the periphery of their bases retained as dentine rings. The rings are highly overlapped, which evidences tooth shedding prior to adding the next first-generation tooth at the growing edge of the plate. The first generation of teeth is thus diachronous. Successor teeth at the same sites underwent cyclical replacing and shedding through basal resorption, producing stacks of buried resorption surfaces separated by bone of attachment. The number and spatial arrangement of resorption surfaces elucidates that basal resorption of replacement teeth had taken place at the older tooth sites before the addition of the youngest first-generation teeth at the lingual margin. Thus, the replacement tooth buds cannot have been generated by a single permanent dental lamina at the lingual edge of the tooth cushion, but must have arisen either from successional dental laminae associated with the individual predecessor teeth, or directly from the dental epithelium of these teeth. The virtual histological dissection of these Late Silurian microfossils broadens our understanding of the development of the gnathostome dental systems and the acquisition of the osteichthyan-type of tooth replacement., Competing Interests: We declare we have no competing interests.
- Published
- 2017
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40. The origin of novel features by changes in developmental mechanisms: ontogeny and three-dimensional microanatomy of polyodontode scales of two early osteichthyans.
- Author
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Qu Q, Sanchez S, Zhu M, Blom H, and Ahlberg PE
- Subjects
- Animal Scales anatomy & histology, Animals, China, Fishes classification, Fishes growth & development, Phylogeny, Biological Evolution, Fishes anatomy & histology, Fossils
- Abstract
Recent advances in synchrotron imaging allow us to study the three-dimensional (3D) histology of vertebrate fossils, including microfossils (e.g. teeth and scales) of early jawed vertebrates. These microfossils can often be scanned at submicron resolution (<1 µm) because of their small size. The resulting voxel (3D pixel) stacks can be processed into virtual thin sections revealing almost every internal detail of the samples, comparable to traditional thin sections. In addition, 3D models of the internal microanatomical structures, such as embedded odontodes and vasculature, can be assembled and examined in situ. Scales of two early osteichthyans, Psarolepis romeri from the Early Devonian of China and Andreolepis hedei from the Late Silurian of Sweden, were scanned using propagation phase-contrast synchrotron X-ray microtomography (PPC-SRµCT), and 3D models of internal canal systems and buried odontodes were created from the scans. Based on these new data, we review the evolutionary origin of cosmine and its associated pore-canal system, which has been long recognized as a synapomorphy of sarcopterygians. The first odontode that appeared during growth shows almost identical morphology in the two scales, but the second odontode of the Psarolepis scale shows a distinctive morphology with several pores on the surface. It is suggested that a shift from ridge-like odontode to pore-bearing odontode was the key step in the origin of cosmine, which was then elaborated further in more-derived sarcopterygians. We perform a detailed comparison between the two scales and propose a primary homology framework to generate microanatomical characters, which can be used in the phylogenetic analysis of early osteichthyans when more 3D data become available. Our results highlight the importance of 3D data for the study of histology and ontogeny of the dermal skeleton of early jawed vertebrates, especially scales of the polyodontode type. The traditional microvertebrate collection is not only useful for biostratigraphic studies, but also preserves invaluable biological information about the growth of vertebrate hard tissues. Today, we are only beginning to understand the biological meaning of the new 3D data. The increasing availability of such data will enable, and indeed require, a complete revision of traditional palaeohistological studies on early vertebrates., (© 2016 Cambridge Philosophical Society.)
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- 2017
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41. Unique diversity of acanthothoracid placoderms (basal jawed vertebrates) in the Early Devonian of the Prague Basin, Czech Republic: A new look at Radotina and Holopetalichthys.
- Author
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Vaškaninová V and Ahlberg PE
- Subjects
- Animals, Biodiversity, Czech Republic, Fossils, History, Ancient, Paleontology, Chordata anatomy & histology
- Abstract
The taxonomy of Early Devonian placoderm material from the Lochkovian and Pragian of the Prague basin, previously attributed to the genera Radotina and Holopetalichthys, is revised. The Pragian species Radotina tesselata Gross 1958 shares detailed similarities with the holotype of the Lochkovian Radotina kosorensis Gross 1950, which is also the holotype of the genus; the assignation of both species to Radotina is supported. However, the Lochkovian material previously attributed to Radotina kosorensis also contains two unrecognised taxa, distinguishable from Radotina at the generic level: these are here named Tlamaspis and Sudaspis. The disputed genus Holopetalichthys, synonymised with Radotina by some previous authors, is shown to be valid. Furthermore, whereas Radotina, Tlamaspis and Sudaspis can all be assigned to the group Acanthothoracii, on the basis of several features including possession of a projecting prenasal region of the endocranium, Holopetalichthys lacks such a region and is probably not an acanthothoracid. Skull roof patterns and other aspects of morphology vary greatly between these taxa. Radotina has a substantially tesselated skull roof, whereas the skull roofs of Tlamaspis and Holopetalichthys appear to lack tesserae altogether. Tlamaspis has an extremely elongated facial region and appears to lack a premedian plate. Sudaspis has a long prenasal region, but unlike Tlamaspis the postnasal face is not elongated. Past descriptions of the braincase of 'Radotina' and the skull roofs of 'Radotina' and 'Holopetalichthys' incorporate data from more than one taxon, giving rise to spurious characterisations including an apparently extreme degree of skull roof variability. These descriptions should all be disregarded.
- Published
- 2017
- Full Text
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42. The first direct evidence of a Late Devonian coelacanth fish feeding on conodont animals.
- Author
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Zatoń M, Broda K, Qvarnström M, Niedźwiedzki G, and Ahlberg PE
- Subjects
- Animals, Aquatic Organisms, Diet, Poland, Feeding Behavior, Fishes physiology, Fossils
- Abstract
We describe the first known occurrence of a Devonian coelacanth specimen from the lower Famennian of the Holy Cross Mountains, Poland, with a conodont element preserved in its digestive tract. A small spiral and phosphatic coprolite (fossil excrement) containing numerous conodont elements and other unrecognized remains was also found in the same deposits. The coprolite is tentatively attributed to the coelacanth. Although it is unclear whether the Late Devonian coelacanth from Poland was an active predator or a scavenger, these finds provide the first direct evidence of feeding on conodont animals by early coelacanth fish, and one of the few evidences of feeding on these animals known to date. It also expands our knowledge about the diet and trophic relations between the Paleozoic marine animals in general.
- Published
- 2017
- Full Text
- View/download PDF
43. The internal cranial anatomy of Romundina stellina Ørvig, 1975 (Vertebrata, Placodermi, Acanthothoraci) and the origin of jawed vertebrates-Anatomical atlas of a primitive gnathostome.
- Author
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Dupret V, Sanchez S, Goujet D, and Ahlberg PE
- Subjects
- Animals, Fossils, Imaging, Three-Dimensional, Models, Anatomic, Paleontology, Vertebrates classification, Jaw anatomy & histology, Skull anatomy & histology, Vertebrates anatomy & histology
- Abstract
Placoderms are considered as the first jawed vertebrates and constitute a paraphyletic group in the stem-gnathostome grade. The acanthothoracid placoderms are among the phylogenetically most basal and morphologically primitive gnathostomes, but their neurocranial anatomy is poorly understood. Here we present a near-complete three-dimensional skull of Romundina stellina, a small Early Devonian acanthothoracid from the Canadian Arctic Archipelago, scanned with propagation phase contrast microtomography at a 7.46 μm isotropic voxel size at the European Synchrotron Radiation Facility, Grenoble, France. This is the first model of an early gnathostome skull produced using this technique, and as such represents a major advance in objectivity compared to past descriptions of placoderm neurocrania on the basis of grinding series. Despite some loss of material along an oblique crack, most of the internal structures are remarkably preserved, and most of the missing structures can be reconstructed by symmetry. This virtual approach offers the possibility to connect with certainty all the external foramina to the blood and nerve canals and the central structures, and thus identify accurate homologies without destroying the specimen. The high level of detail enables description of the main arterial, venous and nerve canals of the skull, and other perichondrally ossified endocranial structures such as the palatoquadrate articulations, the endocranial cavity and the inner ear cavities. The braincase morphology appears less extreme than that of Brindabellaspis, and is in some respects more reminiscent of a basal arthrodire such as Kujdanowiaspis., Competing Interests: Daniel Goujet was employed by Muséum National d’Histoire Naturelle during part of the study. The commercial affiliation (MNHN) of DG does not alter the authors' adherence to PLOS ONE policies on sharing data and materials.
- Published
- 2017
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44. The stem osteichthyan Andreolepis and the origin of tooth replacement.
- Author
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Chen D, Blom H, Sanchez S, Tafforeau P, and Ahlberg PE
- Subjects
- Animals, Jaw anatomy & histology, Microscopy, Phase-Contrast, Synchrotrons, Tomography, Fishes, Fossils, Tooth anatomy & histology, Tooth growth & development
- Abstract
The teeth of gnathostomes (jawed vertebrates) show rigidly patterned, unidirectional replacement that may or may not be associated with a shedding mechanism. These mechanisms, which are critical for the maintenance of the dentition, are incongruently distributed among extant gnathostomes. Although a permanent tooth-generating dental lamina is present in all chondrichthyans, many tetrapods and some teleosts, it is absent in the non-teleost actinopterygians. Tooth-shedding by basal hard tissue resorption occurs in most osteichthyans (including tetrapods) but not in chondrichthyans. Here we report a three-dimensional virtual dissection of the dentition of a 424-million-year-old stem osteichthyan, Andreolepis hedei, using propagation phase-contrast synchrotron microtomography, with a reconstruction of its growth history. Andreolepis, close to the common ancestor of all extant osteichthyans, shed its teeth by basal resorption but probably lacked a permanent dental lamina. This is the earliest documented instance of resorptive tooth shedding and may represent the primitive osteichthyan mode of tooth replacement.
- Published
- 2016
- Full Text
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45. Three-dimensional paleohistology of the scale and median fin spine of Lophosteus superbus (Pander 1856).
- Author
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Jerve A, Qu Q, Sanchez S, Blom H, and Ahlberg PE
- Abstract
Lophosteus superbus is one of only a handful of probable stem-group osteichthyans known from the fossil record. First collected and described in the late 19th century from the upper Silurian Saaremaa Cliff locality in Estonia, it is known from a wealth of disarticulated scales, fin spines, and bone fragments. In this study we provide the first description of the morphology and paleohistology of a fin spine and scale from Lophosteus using virtual thin sections and 3D reconstructions that were segmented using phase-contrast synchrotron X-ray microtomography. These data reveal that both structures have fully or partially buried odontodes, which retain fine morphological details in older generations, including sharp nodes and serrated ridgelets. The vascular architecture of the fin spine tip, which is composed of several layers of longitudinally directed bone vascular canals, is much more complex compared to the bulbous horizontal canals within the scale, but they both have distinctive networks of ascending canals within each individual odontode. Other histological characteristics that can be observed from the data are cell spaces and Sharpey's fibers that, when combined with the vascularization, could help to provide insights into the growth of the structure. The 3D data of the scales from Lophosteus superbus is similar to comparable data from other fossil osteichthyans, and the morphology of the reconstructed buried odontodes from this species is identical to scale material of Lophosteus ohesaarensis , casting doubt on the validity of that species. The 3D data presented in this paper is the first for fossil fin spines and so comparable data is not yet available. However, the overall morphology and histology seems to be similar to the structure of placoderm dermal plates. The 3D datasets presented here provide show that microtomography is a powerful tool for investigating the three-dimensional microstructure of fossils, which is difficult to study using traditional histological methods. These results also increase the utility of fin spines and scales suggest that these data are a potentially rich source of morphological data that could be used for studying questions relating to early vertebrate growth and evolution., Competing Interests: The authors declare there are no competing interests.
- Published
- 2016
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46. A Silurian maxillate placoderm illuminates jaw evolution.
- Author
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Zhu M, Ahlberg PE, Pan Z, Zhu Y, Qiao T, Zhao W, Jia L, and Lu J
- Subjects
- Animals, Dental Arch anatomy & histology, Fossils, Paleontology, Phylogeny, Biological Evolution, Fishes anatomy & histology, Fishes classification, Mandible anatomy & histology, Maxilla anatomy & histology
- Abstract
The discovery of Entelognathus revealed the presence of maxilla, premaxilla, and dentary, supposedly diagnostic osteichthyan bones, in a Silurian placoderm. However, the relationship between these marginal jaw bones and the gnathal plates of conventional placoderms, thought to represent the inner dental arcade, remains uncertain. Here we report a second Silurian maxillate placoderm, which bridges the gnathal and maxillate conditions. We propose that the maxilla, premaxilla, and dentary are homologous to the gnathal plates of placoderms and that all belong to the same dental arcade. The gnathal-maxillate transformation occurred concurrently in upper and lower jaws, predating the addition of infradentary bones to the lower jaw., (Copyright © 2016, American Association for the Advancement of Science.)
- Published
- 2016
- Full Text
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47. The cranial endocast of Dipnorhynchus sussmilchi (Sarcopterygii: Dipnoi) and the interrelationships of stem-group lungfishes.
- Author
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Clement AM, Challands TJ, Long JA, and Ahlberg PE
- Abstract
The first virtual cranial endocast of a lungfish from the Early Devonian, Dipnorhynchus sussmilchi , is described. Dipnorhynchus, only the fourth Devonian lungfish for which a near complete cranial endocast is known, is a key taxon for clarifying primitive character states within the group. A ventrally-expanded telencephalic cavity is present in the endocast of Dipnorhynchus demonstrating that this is the primitive state for "true" Dipnoi. Dipnorhynchus also possesses a utricular recess differentiated from the sacculolagenar pouch like that seen in stratigraphically younger lungfish ( Dipterus, Chirodipterus, Rhinodipterus ), but absent from the dipnomorph Youngolepis . We do not find separate pineal and para-pineal canals in contrast to a reconstruction from previous authors. We conduct the first phylogenetic analysis of Dipnoi based purely on endocast characters, which supports a basal placement of Dipnorhynchus within the dipnoan stem group, in agreement with recent analyses. Our analysis demonstrates the value of endocast characters for inferring phylogenetic relationships., Competing Interests: The authors declare there are no competing interests.
- Published
- 2016
- Full Text
- View/download PDF
48. Early Gnathostome Phylogeny Revisited: Multiple Method Consensus.
- Author
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Qiao T, King B, Long JA, Ahlberg PE, and Zhu M
- Subjects
- Animals, Classification methods, Consensus, Fishes classification, Fishes genetics, Reproducibility of Results, Species Specificity, Vertebrates classification, Vertebrates genetics, Fishes anatomy & histology, Fossils, Jaw anatomy & histology, Phylogeny, Vertebrates anatomy & histology
- Abstract
A series of recent studies recovered consistent phylogenetic scenarios of jawed vertebrates, such as the paraphyly of placoderms with respect to crown gnathostomes, and antiarchs as the sister group of all other jawed vertebrates. However, some of the phylogenetic relationships within the group have remained controversial, such as the positions of Entelognathus, ptyctodontids, and the Guiyu-lineage that comprises Guiyu, Psarolepis and Achoania. The revision of the dataset in a recent study reveals a modified phylogenetic hypothesis, which shows that some of these phylogenetic conflicts were sourced from a few inadvertent miscodings. The interrelationships of early gnathostomes are addressed based on a combined new dataset with 103 taxa and 335 characters, which is the most comprehensive morphological dataset constructed to date. This dataset is investigated in a phylogenetic context using maximum parsimony (MP), Bayesian inference (BI) and maximum likelihood (ML) approaches in an attempt to explore the consensus and incongruence between the hypotheses of early gnathostome interrelationships recovered from different methods. Our findings consistently corroborate the paraphyly of placoderms, all 'acanthodians' as a paraphyletic stem group of chondrichthyans, Entelognathus as a stem gnathostome, and the Guiyu-lineage as stem sarcopterygians. The incongruence using different methods is less significant than the consensus, and mainly relates to the positions of the placoderm Wuttagoonaspis, the stem chondrichthyan Ramirosuarezia, and the stem osteichthyan Lophosteus-the taxa that are either poorly known or highly specialized in character complement. Given that the different performances of each phylogenetic approach, our study provides an empirical case that the multiple phylogenetic analyses of morphological data are mutually complementary rather than redundant., Competing Interests: The authors have declared that no competing interests exist.
- Published
- 2016
- Full Text
- View/download PDF
49. Life history of the stem tetrapod Acanthostega revealed by synchrotron microtomography.
- Author
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Sanchez S, Tafforeau P, Clack JA, and Ahlberg PE
- Subjects
- Age Determination by Skeleton, Animals, Aquatic Organisms, Biological Evolution, Bone and Bones anatomy & histology, Extremities anatomy & histology, Greenland, Osteogenesis, Sex Characteristics, Fossils, Life Cycle Stages, Synchrotrons, Tomography methods, Vertebrates anatomy & histology
- Abstract
The transition from fish to tetrapod was arguably the most radical series of adaptive shifts in vertebrate evolutionary history. Data are accumulating rapidly for most aspects of these events, but the life histories of the earliest tetrapods remain completely unknown, leaving a major gap in our understanding of these organisms as living animals. Symptomatic of this problem is the unspoken assumption that the largest known Devonian tetrapod fossils represent adult individuals. Here we present the first, to our knowledge, life history data for a Devonian tetrapod, from the Acanthostega mass-death deposit of Stensiö Bjerg, East Greenland. Using propagation phase-contrast synchrotron microtomography (PPC-SRμCT) to visualize the histology of humeri (upper arm bones) and infer their growth histories, we show that even the largest individuals from this deposit are juveniles. A long early juvenile stage with unossified limb bones, during which individuals grew to almost final size, was followed by a slow-growing late juvenile stage with ossified limbs that lasted for at least six years in some individuals. The late onset of limb ossification suggests that the juveniles were exclusively aquatic, and the predominance of juveniles in the sample suggests segregated distributions of juveniles and adults at least at certain times. The absolute size at which limb ossification began differs greatly between individuals, suggesting the possibility of sexual dimorphism, adaptive strategies or competition-related size variation.
- Published
- 2016
- Full Text
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50. A new method for reconstructing brain morphology: applying the brain-neurocranial spatial relationship in an extant lungfish to a fossil endocast.
- Author
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Clement AM, Strand R, Nysjö J, Long JA, and Ahlberg PE
- Abstract
Lungfish first appeared in the geological record over 410 million years ago and are the closest living group of fish to the tetrapods. Palaeoneurological investigations into the group show that unlike numerous other fishes-but more similar to those in tetrapods-lungfish appear to have had a close fit between the brain and the cranial cavity that housed it. As such, researchers can use the endocast of fossil taxa (an internal cast of the cranial cavity) both as a source of morphological data but also to aid in developing functional and phylogenetic implications about the group. Using fossil endocast data from a three-dimensional-preserved Late Devonian lungfish from the Gogo Formation, Rhinodipterus, and the brain-neurocranial relationship in the extant Australian lungfish, Neoceratodus, we herein present the first virtually reconstructed brain of a fossil lungfish. Computed tomographic data and a newly developed 'brain-warping' method are used in conjunction with our own distance map software tool to both analyse and present the data. The brain reconstruction is adequate, but we envisage that its accuracy and wider application in other taxonomic groups will grow with increasing availability of tomographic datasets.
- Published
- 2016
- Full Text
- View/download PDF
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