Zhou, Z. Carvalho, I. et al. CAS volume2, Articlenumber:399 (2019) Unlike modern birds, Ichthyornis possessed teeth, which are thought to have been used to hold its prey, manipulate objects, and preen its feathers. 6f) is slender and slightly bowed dorsally, as in Eoconfuciusornis11. It is small and slightly curved with a blunt end, somewhat resembling that of Archaeopteryx35. Ichthyornis. This creature was named Archaeopteryx lithographica: ancient wing of the Lithographic limestone. TWO fossils from northeast China are poised to knock Archaeopteryx, the earliest known bird, right off its perch. PLoS ONE 4, e7390 (2009). 5c), and major metacarpal longer than the minor metacarpal (Fig. 7c). b Right ulna. The Ornithothoraces includes Enantiornithes (extinct by the end of the Cretaceous)17 and Ornithuromorpha18 (in which modern birds are nested), and both of them are well-adapted to powered flight. 7a). Chiappe, L. M., ShuAn, J. I. (Cambridge University Press, 2007). Explore the Family Tree of Birds | AMNH A primitive confuciusornithid bird from China and its implications for early avian flight. Turner, A. H., Makovicky, P. J. Lefvre, U., Hu, D., Escuilli, F., Dyke, G. & Godefroit, P. A new long-tailed basal bird from the Lower Cretaceous of north-eastern China. Palasiat. The presence of large vascular canals in the inner bone tissue suggests that the bird underwent a rapid phase of early development. (C) Juvenile Wilsons snipe distal tail, microCT sagittal view. It is noted that these canals are also visible in CT images of other long bones, such as the humerus, and exhibit a similar condition (Fig. The ungual phalanx of the minor digit is incomplete, limiting the observation of morphological features (Fig. The yellow arrow in this and subsequent panels indicates the spinal cord channel. 6AC; Supplementary Fig. Li, D., Sullivan, C., Zhou, Z. Sanz, J. L. et al. Assuming the ossification sequence observed in the chicken was conserved in the Mesozoic, caudal vertebrae in young juveniles likely had reduced calcified processes. 47, 194232 (2009). By five months of age, the core pygostyle vertebrae are fully fused. A pygostyle from a non-avian theropod. 4)22. 1). Whenever possible (40 of the 64 species), at least three specimens per species were measured. Acta Geologica Sinica - English Edition 80, 631635 (2006). Article The coracoid is unfused with the scapula (Fig. & Zhang, F. Anatomy of the primitive bird Sapeornis chaoyangensis from the Early Cretaceous of Liaoning, China. This project was funded by a donation from George Lucas, by an MSU Faculty of Excellence Grant to D. Rashid, and by NIH/NIDCD under award number R01DC009236 to S. Chapman. Zhou, Z. In the most proximal caudal vertebra among the preserved elements, the neural spine is relatively tall dorsoventrally, but narrow craniocaudally with robust prezygapophyses (Fig. Palaeontology 51, 775791 (2008). They are bowed slightly laterally and cranially as in Confuciusornis20 and Sapeornis30 and bear a short neck that separates a round head from the trochanteric region, as in Confuciusornis20. American Museum Novitates, 146 (2007). 2J,K). Unlike Archaeopteryx, there are deep pleurocoels in the vertebrae; the fibula is reduced; and the bony tail is short with an elongated pygostyle (Martin et al., 1998). Five to seven micron sections were cut using a Jung RM2035 microtome, and transferred to glass slides. Nature 475, 465470 (2011). Bennett, S. C. New evidence on the tail of Pterosaur Pteranodon (Archosauria: Pterosauria). (PDF) Morphological coevolution of the pygostyle and - ResearchGate Sci. These have previously been described as transverse processes22, but because they are not neural arch-derived, are termed here as parapophyses (Fig. & Zhang, F. Jeholornis compared to Archaeopteryx, with a new understanding of the earliest avian evolution. Zoologischer Anzeiger 235, 5376 (1996). The chicken was utilized as an easily accessible model to study pygostyle formation, which had not been previously investigated in depth. Pygostyles differ between subadult and adult confuciusornithids, however; foramina present in subadult pygostyles are lost with ontogeny, indicating remodeling similar to that in neornithines. Numbers near each node denote bremer support values. Some of the species are characterised by a smaller or larger perforation through the entire shell in . Thank you for visiting nature.com. Zoological Journal of the Linnean Society 173, 929955 (2015). In terms of age, fossil beds preserving Cretaceous avian specimens younger than 120 million years old are relatively scarce; there is no reason to exclude the possibility that long-tailed birds existed at that time. As suggested for Confuciusornis, this area may be homologous to the acrocoracoidal articular facet of modern birds20,37. Sci. and JavaScript. To investigate how pygostyle relative size evolved throughout the avian lineage, the mean pygostyle length/femur length was calculated for the seven extinct and extant clades; note that stem Ornithuromorpha is paraphyletic. ISSN 2399-3642 (online). With the exception of microCT raw data, all data generated or analyzed during this study are included in this published article (and its Supplementary Information files). Correspondence to PubMedGoogle Scholar. Long and shorttailed birds also diffe . Article The tomographic data were converted into 16-bit.tif format and skeletal elements were segmented and rendered with VGStudio 3.1 and Amira 6.2. All harvesting of live animals were conducted in accordance with approved protocols at Clemson University (post-hatch; Animal Use Protocol 2011-041) and at Montana State University (late-stage embryos, IACUC Protocol 2015-26). supervised the project, collected data, and wrote the paper. This may result from a series of primitive features found in F. prima such as simple and robust furcula, unfused pelvis, metacarpals and metatarsals, as well as a well-developed deltopectoral crest on the humerus extending to the midshaft. Ossification sequence is a critical parameter to consider when analyzing juvenile fossils. In addition, nearly all the Early Cretaceous birds are two-dimensionally preserved, severely limiting the amount of morphologies that can be confidently reconstructed. Additional changes in the avian axial skeleton, including substantial fusion of sacral vertebrae and bone fusions in the extremities have persisted in modern birds, and are a testament to their adaptive advantages. 2). Archaeopteryx ( / rkiptrks /; lit. In the two complete dorsal vertebrae, the neural spines are low cranially, moderately tall caudally, and craniocaudally wide. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate. J. Asian Earth Sci. (B,B) MicroCT scan of 78 week old juvenile chicken pygostyle, mid-sagittal and surface views, respectively; distal to the left. Fossils of early birds were poorly known until the late 20th century. Numerous fossil discoveries from the Late Jurassic and Early Cretaceous are filling in the gaps of the long- to short-tailed transition. At the seven to eight week juvenile stage, von Kossa and Massons trichrome staining (Fig. In the present phylogenetic hypothesis, the fusion of distal caudal vertebrae (Char. The ulna is shorter than the humerus in F. prima in contrast to the proportionally longer ulna of volant ornithothoracines (Fig. 48) with the character ordering the same as in ref. 98, 358370 (2015). 6a). Palasiat. Article In 2013, the first associated skeleton of an Early Cretaceous bird from Japan was collected in Katsuyama, Fukui, central Japan. 3D,E). After pygostyle vertebrae fusion, the spinal cord channel is retained but trabecular bone remodeling removes all traces of intervertebral discs. In extant birds, this is typically associated with a fleshy structure called the rectricial bulb that secures the tail feathers (rectrices) [1]. (J) MicroCT scan, juvenile Eurypyga helias (LACM 104451) partial tail with pygostyle, dorsal view. The major metacarpal is longer than the minor metacarpal, a condition different from that of enantiornithines17. The data shows great variation in relative pygostyle lengths overall, and suggests that confuciusornithiformes and enantiornithes incorporated more vertebrae into their pygostyle (n: number of specimens measured). The elongated pygostyle is also characteristic of more typical enantiornithine birds, but is not found in Mesozoic Ornithurines except for Baptornis ( Martin and Tate, 1976 ). & Norell, M. A. Tissue was then cleared in Clear Rite followed by Tissue Prep paraffin. No lines of arrested growth (LAGs) are recognized (Fig. Pygostylia is a group of avialans which includes the Confuciusornithidae and all of the more advanced species, the Ornithothoraces . An early Cretaceous pellet. 3c). Therefore, analogous to humans, ontogenetic changes in ossification sequence in birds cause significant changes in bony vertebral morphology (Fig. 6, 7141 (2015). 5d). Its highly elongated vertebrae and frond-like configuration of rectrices31 suggest a long tail, and thus it likely did not belong to the Pygostylia group. Pygostyle | Article about Pygostyle by The Free Dictionary The dataset consisted of 280 morphological characters and 71 taxa. To differentiate mineralized bone from unmineralized cartilage, alcian blue and alizarin red staining was performed in wholemount tissue, and von Kossa was performed on unfixed, sliced tissue. Zhou, Z. J.R.H. Introduction Modern. Knoll, F. et al. With this arrangement, growth occurs in the outward direction only, allowing for elongation of ossified processes during this later-stage event. MicroCT raw data is available upon request from D. Rashid. (B) Chicken E19, sagittal view, ossification centers in the pygostyle region; alcian blue and picrosirius red; distal to the left; white arrows indicate ossification centers. 14, 2561 (2015). Nat. In modern birds, the rectrices attach to these. Stained tissue slices were subsequently imaged with either a Unitron TCS tablet mounted on a Zeiss Stemi 200c dissecting microscope for lower resolution images, or a Zeiss Stemi SV11 stereoscope with a Jenoptik ProgRes C14 camera using associated software for higher resolution imaging. 1); the Lower Cretaceous Kitadani Formation (Aptian)23 (seeSupplementary Notes for further details). Article The CT scans were performed in air on a XT H 225ST micro-CT scanner (Nikon Metrology, Brighton, MI) with a PerkinElmer 1621 detector at 70kVp, 100uA, 1000ms exposure, 1000 projections/360 degree and 24dB gain to create an isotropic 1016 micron voxel volume of each specimen. Relevant to Mesozoic specimens, the lack of a pygostyle in juveniles and a variable number of relatively featureless caudal vertebrae can blur the distinction of transitional species. S.C.C. Journal of Vertebrate Paleontology 23, 373386 (2003). PubMed All elements are in cranial, caudal, dorsal, and ventral views from left to right in a through c, and dorsal, ventral, caudal, and cranial views from left to right in d through j. Abbreviations: dc deltopectoral crest, imt intermetacarpal tubercle, oc olecranon, scd semicircular depression. The first phalanx of the alular digit (Fig. In the meantime, to ensure continued support, we are displaying the site without styles Caudally, the surangular is perforated by a circular foramen. Google Scholar. Avian tail ontogeny, pygostyle formation, and interpretation of juvenile Mesozoic specimens, https://doi.org/10.1038/s41598-018-27336-x. It is an evolutionary grade of transitional fossils, the primitive birds halfway between non avian dinosaur ancestors and the derived modern birds (avian dinosaur). This phylogenetic result may imply a complex evolutionary history of basal birds. The dorsal centra are procoelous with subcircular to subrectangular cranial articular surfaces, and relatively flat caudal articular surface (Fig. PDF Confuciusornis sanctus Compared to Archaeopteryx lithographica - Springer While a vertebral foramen is obscured on the proximal articular surface, CT images reveal a canal bounded by thin walls within a vascularized internal pygostyle (Fig. To obtain 9 and Supplementary Fig. Scientific Reports FPDM-V-9769 (FPDM: Fukui Prefectural Dinosaur Museum, Fig. K. Uesugi and M. Hoshino at JASRI assisted the experiments during our work at SPring-8. Chiappe, L. M. & Walker, C. A. Skeletal morphology and systematics of the Cretaceous Euenantiornithes (Ornithothoraces: Enantiornithes). Provini, P., Zhou, Z. H. & Zhang, F. C. A new species of the basal bird Sapeornis from the Early Cretaceous of Liaoning, China. 92, 115 (2018). Furthermore, as described above, F. prima exhibits numerous primitive features comparable to non-ornithothoracine birds but not to the more crownward taxa. (D) Juvenile lesser nighthawk (LACM 111218) microCT dorsal surface view, showing separate ossified elements (yellow arrowheads), analogous to ribs, that fuse into the parapophyses (white arrow) of free caudal vertebrae (pygostyle region noted by white bar). Here, we present a three-dimensionally-preserved skeleton (FPDM-V-9769) of a basal bird from the Early Cretaceous of Fukui, central Japan. Google Scholar. Quarterly Journal of the Geological Society 26, 1231 (1870). Notably, the ossification front between the centrum and the tips presents as an epiphyseal plate, with the distal cartilage serving as the zone of reserve or resting cartilage. Some Mesozoic birds formed a relatively longer pygostyle than extant birds. 371, 1206 (2012). The strict consensus tree was generated based on the MPTs found after the second TBR search. Among non-ornithothoracine avialans, this condition is only seen in Archaeopteryx35. c Left metatarsals. Due to the state of preservation, it is unclear whether uncinate processes are present during life. We now grasp their general diversification and course of evolution in the late Early Cretaceous. In contrast to adult chickens, where the spinal cord channel is craniocaudally short34, that of F. prima seems to extend more distally. Erickson, G. M. et al. a Right rib in cranial and caudal views. These, like Archaeopteryx, sported long ancestral tails and a lack of a distal pygostyle. Total femur length was measured as a proxy for body size39. However, incompleteness of the material and inferences that the specimen is a juvenile obscure its phylogenetic placement. MicroCT scanning was also performed on commercial roaster chickens and on tail tissue extracted from the emu specimens. (F) Chicken 78 week old juvenile, transverse section of left parapophysis, alcian blue and picrosirius red. a Transverse thin section of left ulna. Nearly all cranial and mandibular elements are severely damaged, preventing identification, and many axial elements are missing. Massons Trichrome stain was utilized to differentiate between mineralized (purple) and unmineralized cartilage (blue). Current Biology 27, R215R216 (2017). Rashid, D. et al. Chatterjee, S. The Rise of Birds: 225 Million Years of Evolution, (Johns Hopkins University Press) (1997). The ventrolateral surfaces bear five small projections on both sides; because the number of these notches match that of the pygostyle-forming vertebra, these may be incipient transverse processes (tp? For specific specimen numbers, please see the relevant figure legends in both the manuscript proper as well as in the Supplementary Information online. To further explore the phylogenetic position of F. prima, we added FPDM-V-9769 to the most recent dataset targeting the phylogeny of Mesozoic birds14. Modern birds have extremely short tail skeletons relative to Archaeopteryx and nonavialian theropod dinosaurs. Sano, S. New view of the stratigraphy of the Tetori Group in Central Japan. 2D). Incipient neural spines are distinguishable, indicating that it is composed of at least five vertebrae, whereas this number is eight to ten in Confuciusornis20 and four in Sapeornis30. Intervertebral discs, for example, initially form but are subsequently lost by tissue remodeling, though the discs within the pygostyle are narrower than in the free caudal vertebrae (the unfused vertebrae proximal to the pygostyle) (Fig. The absence of LAGs in the ulna of FPDM-V-9769 suggests the animal died when it was <1 year old. Moodie, R. The sacrum of the Lacertilia, Volume 13, (Lancaster Press) (1907). MOR is the abbreviation for the Museum of the Rockies. 5, 357365 (1868). c Left coracoid in medial, lateral, cranial, and caudal views from top to bottom. CAS This palaeogeographic bias hinders not only our understanding of the global distribution of these most-basal clades but also of the evolution of flight-related features in different environments during this critical temporal span. While the surangular is mediolaterally compressed, it thickens to form a low hillock just caudal to the putative caudal mandibular fenestra and rostral to the articulation surface for the quadrate, as in confuciusornithids26 (seeSupplementary Notes for additional descriptions and comparisons of the surangular). An integrative approach to understanding bird origins. Sci Rep 8, 9014 (2018). and K.M. From dinosaurs to birds: a tail of evolution - EvoDevo To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. For these stains, paraffin sections were dewaxed with xylenes, and rehydrated through a series of EtOH washes to water. Abbreviations: cp caudal projection, bf brevis fossa, gf glenoid fossa, lp lateral process, paw postacetabular wing, sc scapular cotyle. Results from these experiments reveal that the pygostyle, rectrices, rectricial bulbs, and bulbi rectricium musculature form a specialized fanning mechanism. These characters included Char. Commun Biol 2, 399 (2019). a Left femur. Demineralized tissue was then processed for wax embedding in a Tissue Tek VIP 6 processor starting with an ethanol series until dehydrated. Bull. Alizarin red is a calcium-sensitive dye that stains mineralized tissue red, and von Kossa is a silver-based stain that is phosphate sensitive, and stains mineralized tissue black. Calif. Acad. Consequently, pygostyle fusion is loosely associated with ontogenetic stage, so the widely differing timeframes for fusion in different birds are probably reflected in the timeframes required to achieve skeletal maturity. Proc. conducted the CT experiments, M.S. PubMed (PDF) Morphological coevolution of the pygostyle and - ResearchGate 2C). 2E,F). Science 279, 19151919 (1998). These lines of evidence demonstrate that F. prima belongs to non-ornithothoracine avialans. Two cervical vertebrae are recognized, although they are missing neural arches. As increasing numbers of Mesozoic avian fossils are discovered, analyses of these specimens are continually modifying our views of bird evolution. 79 (absence or presence of ossified uncinate processes), Char. PDF Morphological coevolution of the pygostyle and tail - ResearchGate In coding the character states for F. prima, any characters that are likely affected by the immaturity of the specimen were coded missing. A Mesozoic bird from Gondwana preserving feathers. https://doi.org/10.19615/j.cnki.1000-3118.180530 138 (2018). Science 346, 1253293 (2014). This specialized tail is present throughout the entire diversity of living birds, albeit with many modifications for clade-specific behaviors. For extinct taxa, the pygostyle/femur lengths of 40 specimens were collected from published sources28. PLOS ONE 9, e89737 (2014). Archaeopteryx. Natl Acad. There are eight free caudal vertebrae and an extremely large pygostyle, estimated to be composed of 10 to 15 fused vertebrae (Sanz and Bonaparte 1988, 1992). Untitled Document [bio.sunyorange.edu] PubMed Central GEOL 104 Lecture 22: Archaeopteryx and the Origin of Birds I - UMD Until a full-grown specimen is discovered, to indicate whether adults of this species had unfused pygostyle vertebrae, the Zhongornis haoae holotype cannot be definitively identified as an intermediate in the long- to short-tailed transition. Wang, M. & Zhou, Z. Commun. Analyses of relative pygostyle lengths in extant and Cretaceous birds suggests the number of vertebrae incorporated into the pygostyle has varied considerably, further complicating the interpretation of potential transitional species. played an overall supervisory role, and contributed to funding acquisition. Two caudal vertebrae are articulated with each other. On the other hand, a semicircular depression is present on the craniodorsal corner of the humeral head and presumably proximal to the deltopectoral crest (scd in Fig. contributed to data collection, including all specimen measurements, participated in project conceptualization, and contributed to figure preparation. Institute of Dinosaur Research, Fukui Prefectural University, 4-1-1 Matsuoka Kenjojima, Eiheiji, Fukui, 910-1195, Japan, Takuya Imai,Yoichi Azuma,Soichiro Kawabe&Masateru Shibata, Fukui Prefectural Dinosaur Museum, 51-11 Terao, Muroko, Katsuyama, Fukui, 911-8601, Japan, Takuya Imai,Yoichi Azuma,Soichiro Kawabe,Masateru Shibata&Kazunori Miyata, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 142 Xizhimenwai Street, 100044, Beijing, China, Center for Excellence in Life and Paleoenvironment, Chinese Academy of Sciences, 142 Xizhimenwai Street, 100044, Beijing, China, You can also search for this author in
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