Pterosaurs and the origin of feathers

Reconstructed T. imperator skeleton, National Museum of Brazil. From Wikimedia Commons

Feathers were once considered to be unique avialan structures linked to birds evolutionary success. Primitive theropods, such as Sinosauropteryx and the tyrannosaurs Dilong and Yutyrannus, and some plant-eating ornithischian dinosaurs, such as Tianyulong, and Kulindadromeus are known from their spectacularly preserved fossils covered in simple, hair-like filaments called ‘protofeathers’. Other integumentary filaments, termed pycnofibres, has been reported in several pterosaur specimens. The discovery of integumentary structures in other pterosaurs, such as Pterorhynchus wellnhoferi (a rhamphorhynchoid pterosaur), and other exquisitely preserved specimens from China, suggest that all Avemetatarsalia (the wide clade that includes dinosaurs, pterosaurs and close relatives) were ancestrally feathered.

A new specimen of an adult Tupandactylus imperator, a tapejarid pterosaur from north-eastern Brazil, preserves extensive soft tissues which provides more evidence that pterosaurs had feathers. The fossil, originally poached from an undetermined outcrop of the Early Cretaceous Crato Formation, was in privated hands for an unknown period of time and later deposited at the Royal Belgian Institute of Natural Sciences (RBINS). The fossil was repatriated to Brazil early this year.

Details of the cranial crest of MCT.R.1884 and the scanning electron microscope images of melanosomes (g-i). Scale bars, 50 mm (a); 5 mm (b); 2 mm (c); 250 μm (d–f); 2 μm (g–i). From Cincotta et al., 2022.

The new specimen (MCT.R.1884) comprises the posterior portion of the cranium and the remains of a soft tissue cranial crest preserved on five separate slabs. Two types of fibrous integumentary structures were present. The monofilaments (approximately 30 mm long and 60–90 μm wide) resemble those present in the anurognathid Jeholopterus ningchengensis and the ornithischian dinosaur Tianyulong. The most striking feature is the presence of fossil melanosomes with diverse morphologies that supports the hypothesis that the branched integumentary structures in pterosaurs are feathers.

Melanosomes are granules of the pigment melanin. The diverse shape of the melanosomes recovered from the skin fibres in the crest, monofilaments and branched feathers resembles that in the skin of extant birds and mammals. This is an indication that pterosaurs had the genetic machinery to control the colors of their feathers.

References:

Cincotta, A., Nicolaï, M., Campos, H.B.N. et al. Pterosaur melanosomes support signalling functions for early feathers. Nature (2022). https://doi.org/10.1038/s41586-022-04622-3

On Pterosaurs and feathers.

Reconstruction of one of the studied anurognathid pterosaurs. Credit: Yuan Zhang/Nature Ecology & Evolution.

Feathers were once considered to be unique avialan structures. Recent studies indicated that non avian dinosaurs, as part of Archosauria, possessed the entirety of the known non keratin protein-coding toolkit for making feathers. Primitive theropods, such as Sinosauropteryx and the tyrannosaurs Dilong and Yutyrannus, and some plant-eating ornithischian dinosaurs, such as Tianyulong and Kulindadromeus, are known from their spectacularly preserved fossils covered in simple, hair-like filaments called ‘protofeathers’.

Other integumentary filaments, termed pycnofibres, has been reported in several pterosaur specimens, but there is still a substantial disagreement regarding their interpretation. J. Yang and colleagues described two specimens of short-tailed pterosaurs (NJU–57003 and CAGS–Z070) from the Middle-Late Jurassic Yanliao Biota, in northeast China (around 165-160 million years ago) with preserved structural fibres (actinofibrils) and four different types of pycnofibres. The specimens resemble Jeholopterus and Dendrorhynchoides, but they are relatively small.

 

Drawing of of (a) NJU–57003 and (b) CAGS–Z070 with skeletal element identification, outline of
preserved integument, and distribution of the four types of pycnofibres. From Yang et al., 2018.

Types 1 and 4 of pycnofibres occur in both specimens, but types 2 and 3 occur only in CAGS–Z070. This may reflect original biological differences or differences in the taphonomy of the two specimens. The pterosaur type 1 filaments resemble monofilaments in the ornithischian dinosaurs Tianyulong and Psittacosaurus and the coelurosaur Beipiaosaurus. The pterosaur type 2 filaments resemble the brush-like bundles of filaments in the coelurosaurs Epidexipteryx and Yi. Type 3 filaments resemble bristles in modern birds, but surprisingly do not correspond to any reported morphotype in non-avian dinosaurs. The pterosaur type 4 filaments are identical to the radially branched, downy feather-like morphotype found widely in coelurosaurs such as Caudipteryx and Dilong. Functions of these structures could include insulation, tactile sensing, streamlining and colouration (primarily for camouflage and signalling), as for bristles, down feathers and mammalian hairs.

Type 3 filaments (arrows) and similar structures (triangles). Scale bars: 10 mm in a, c and d; 1 mm in b. From Yang et al., 2018

Pterosaurs were winged cousins of the dinosaurs and lived from around 200 million years ago to 66 million years ago. In the early 1800’s, a fuzzy integument was first reported from the holotype of Scaphognathus crassirostris. A recent study on this specimen shows a subset of pycnofibers and actinofibrils. The discovery of integumentary structures in other pterosaurs, such as Pterorhynchus wellnhoferi (another rhamphorhynchoid pterosaur), and these exquisitely preserved pterosaurs from China, suggest that all Avemetatarsalia (the wide clade that includes dinosaurs, pterosaurs and close relatives) were ancestrally feathered.

References:

Yang Z. et al., 2018. Pterosaur integumentary structure with complex feather-like branching. Nature Ecology and Evolution https://doi.org/10.1038/s41559-018-0728-7

Barrett PM, Evans DC, Campione NE. 2015 Evolution of dinosaur epidermal structures. Biol. Lett. 11: 20150229. http://dx.doi.org/10.1098/rsbl.2015.0229

Kai R.K. Jäger, Helmut Tischlinger, Georg Oleschinski, and P. Martin Sander, Goldfuß was right: Soft part preservation in the Late Jurassic pterosaur Scaphognathus crassirostris revealed by reflectance transformation imaging (RTI) and UV light and the auspicious beginnings of paleo-art, https://doi.org/10.26879/713

Craig B. Lowe, Julia A. Clarke, Allan J. Baker, David Haussler and Scott V. Edwards, Feather Development Genes and Associated Regulatory Innovation Predate the Origin of Dinosauria, Mol Biol Evol (2015) 32 (1): 23-28. doi: 10.1093/molbev/msu309

A mid-Cretaceous enantiornithine frozen in time

Overview of HPG-15-1 in right lateral view. (From Xing et al., 2017)

Overview of HPG-15-1 in right lateral view. (From Xing et al., 2017)

Amber from the Hukawng Valley in northern Myanmar, called Burmese amber, has been commercially exploited for millennia. Of the seven major deposits of amber from the Cretaceous Period, Burmese amber has probably the most diverse paleobiota, including the tail of a non-avian coelurosaurian theropod, and three juvenile enantiornithine birds. The third specimen, HPG-15-1, is the most complete fossil bird discovered in Burmese amber. It comes from the Angbamo site, and measures approximately 86 mm x 30 mm x 57 mm, and weighs 78 g. It  was encapsulated during the earliest stages of its feather production, and  plumage preserves an unusual combination of precocial and altricial features unlike any living hatchling bird.

 Details of the head in HPG-15-1. A, x-ray µCT reconstruction in left lateral view

Details of the head in HPG-15-1. A, x-ray µCT reconstruction in left lateral view (From Xing et al., 2017)

The skull was split when the amber was cut. The rostrum is preserved in one section and the neck and most of the braincase in the other. The skull is mesorostrine. A  single tooth is visible in the left premaxilla. As in Early Cretaceous enantiornithines, the premaxillary corpus is short, forming approximately one-third of the rostrum. The exoccipitals contributed to the dorsal portion of the condyle and were unfused at the time of death. The frontals articulate for most of their length with a small gap between their rostral ends as in Archaeopteryx.  The inner ear and its semicircular canals are preserved. There are at least six articulated cervical vertebrae, including the atlas and axis, preserved in articulation with the skull. The post-axial vertebrae are rectangular with large neural canals, low and caudally displaced neural spines, and a ventral keel as in many enantiornithines. The articulated skull and series of cervical vertebrae bear plumage in dense fields. The individual feathers  are dark brown in color, and appear to consist of tufts of four or more barbs. Skin is preserved as a translucent film in unfeathered regions of both the head and neck.

Microstructure and pigmentation of feathers on wing and body of HPG-15-1. Scale bars equal 1 mm in (A, C); 0.5 mm in (B, D). From Xing et al., 2017

The new specimen also preserves a partial distal wing, the distal right tibiotarsus and complete right foot as well as part of the left pes. Both skeletal material and integumentary structures from the wing’s apex are well-preserved. The plumage consists of fragments of some of the primaries, and alula feathers, some of the secondaries and coverts, and traces of contours from the wing base. The hind limbs preserve feathers and traces of skin. The absence of fusion between the tarsals indicates that the specimen is ontogenetically immature. The proportions of the pedal digits suggest an arboreal lifestyle. Plumage within the femoral and crural tracts consists of neoptile feathers with a short or absent rachis. These feathers are nearly transparent, suggesting that they were pale or white. The skin beneath the crural tract is thin and smooth. The tip of the tail clearly preserves the remains of a single large sheathed rectrix.

The slow post-natal growth results in a protracted period of vulnerability, which is reflected in the Enantiornithes by the large number of juveniles found in the fossil record, whereas young juveniles of other Cretaceous bird lineages are unknown.

 

References:

Lida Xing, Jingmai K. O’Connor, Ryan C. McKellar, Luis M. Chiappe, Kuowei Tseng, Gang Li, Ming Bai , A mid-Cretaceous enantiornithine (Aves) hatchling preserved in Burmese amber with unusual plumage, (2017), doi: 10.1016/j.gr.2017.06.001

Jianianhualong and the evolution of feathers.

Jianianhualong tengi holotype (From Xu, X. et al., 2017)

In recent years, several discovered fossils of theropods and early birds have filled the morphological, functional, and temporal gaps along the line to modern birds. Most of these fossils are from the Jehol Biota of northeastern China, dated between approximately 130.7 and 120 million years ago. Among them are many fossils of troodontids, which are considered as the closest relatives of birds. Previous reported troodontid species include Mei long, Sinovenator changii, Sinusonasus magnodens and Jinfengopteryx elegans. Now a new troodontid, Jianianhualong tengi gen. et sp. nov., has anatomical features that shed light on troodontid character evolution.

The holotype (DLXH 1218) is a nearly complete skeleton with associated feathers, and is inferred to be an adult. It is estimated to be 112 cm in total skeletal body length with a fully reconstructed tail, and its body mass is estimated to be 2.4 kg, similar to most other Jehol troodontids, such as Sinovenator. The skull and mandible are in general well preserved, and  has a relatively short snout and highly expanded skull roof. There are probably 21 maxillary teeth and 25 dentary teeth on each side of the jaw. The vertebral column is nearly completely represented and  the tail is 54 cm long. The furcula is poorly preserved, and the humerus is 70% of femoral length. The manus is typical of maniraptoran theropods, and measures 112 mm in length. The pelvis is in general similar to those of basal troodontids, with a proportionally small ilium, a posteroventrally oriented pubis, and a short ischium. A phylogenetic analysis places Jianianhualong in an intermediate position together with several species between the basalmost and derived troodontids.

Plumage of Jianianhualong tengi (Adapted from Xu, X.  et al, 2017)

The tail frond of Jianianhualong preserves an asymmetrical feather, the first example of feather asymmetry in troodontids. Feathers were once considered to be unique avialan structures. Since the discovery of the feathered Sinosauropteryx in 1996, numerous specimens of most theropod groups and even three ornithischian groups preserving feathers have been recovered from the Jurassic and Cretaceous beds of China, Russia, Germany, and Canada. These feathers fall into several major morphotypes, ranging from monofilamentous feathers to highly complex flight feathers.

Evidence indicates that the earliest feathers evolved in non-flying dinosaurs for display or thermoregulation, and later were co-opted into flight structures with the evolution of asymmetrical pennaceous feathers in Paraves, therefore, the discovery of tail feathers with asymmetrical vanes in a troodontid theropod indicates that feather asymmetry was ancestral to Paraves.

 

 

References:

Xu, X. et al. Mosaic evolution in an asymmetrically feathered troodontid dinosaur with transitional features. Nat. Commun. 8, 14972 doi: 10.1038/ncomms14972 (2017).

Xu, X. et al. An integrative approach to understanding bird origins, Science, Vol. 346 no. 6215 (2014). DOI: 10.1126/science.1253293

A brief introduction to the origin of Birds.

Archaeopteryx lithographica, specimen displayed at the Museum für Naturkunde in Berlin. (From Wikimedia Commons)

Archaeopteryx lithographica, specimen displayed at the Museum für Naturkunde in Berlin. (From Wikimedia Commons)

Birds originated from a theropod lineage more than 150 million years ago. Their evolutionary history is one of the most enduring and fascinating debates in paleontology. In recent years, several discovered fossils of theropods and early birds have filled the morphological, functional, and temporal gaps along the line to modern birds. The discovered fossils demonstrate that distinctive bird characteristics such as feathers, flight, endothermic physiology, unique strategies for reproduction and growth, and a novel pulmonary system have a sequential and stepwise transformational pattern, with many arising early in dinosaur evolution, like the unusually crouched hindlimb for bipedal locomotion,the furcula and the “semilunate” carpal that appeared early in the theropod lineage (Allen et al., 2013; Xu et al., 2014).  Also, the discovery of Mahakala – a basal dromaeosaurid dinosaur named for one of the eight protector deities in Tibetan Buddhism – suggests that extreme miniaturization and laterally movable arms necessary for flapping flight are ancestral for paravian theropods. In contrast, a number of basal birds resemble theropods in many features.

Sin título

Sciurumimus (A); the basal coelurosaur Sinosauropteryx (B) with filamentous feathers; the deinonychosaurs Anchiornis (C) and Microraptor (D). Adapted from Xu et al., 2014.

Anatomical features like aspects of egg shape, ornamentation, microstructure, and porosity of living birds trace their origin to the maniraptoran theropods, such as oviraptorosaurs and troodontids. In addition, some preserving brooding postures, are known for four oviraptorosaurs, two troodontids, a dromaeosaur, and one basal bird providing clear evidence for parental care of eggs.

In birds, particularly their forebrains, are expanded relative to body size. The volumetric expansion of the avian endocranium began relatively early in theropod evolution. Archaeopteryx lithographica is volumetrically intermediate between those of more basal theropods and crown birds (Balanoff et al., 2013). The digital brain cast of Archaeopteryx also present an indentation that could be from the wulst, a neurological structure present in living birds used in information processing and motor control with two primary inputs: somatosensory and visual. Birds also exhibit the most advanced vertebrate visual system, with a highly developed ability to distinguish colors over a wide range of wavelengths.

Reconstruction of pulmonary components [cervical air-sac system (green), lung (orange), and abdominal air-sac system (blue)] in the theropod Majungatholus (From Xu et al., 2014)

Reconstruction of pulmonary components [cervical air-sac system (green), lung (orange), and abdominal air-sac system (blue)] in the theropod Majungatholus (From Xu et al., 2014)

Feathers were once considered to be unique avialan structures. The megalosaurus Sciurumimus, the compsognathus Sinosauropteryx, and a few other dinosaurs, document the appearance of primitive feathers. More recent studies indicated that non avian dinosaurs, as part of Archosauria, possessed the entirety of the known non keratin protein-coding toolkit for making feathers (Lowe et al., 2015)

The evolution of flight involved a series of adaptive changes at the morphological and molecular levels,like the fusion and elimination of some bones and the pneumatization of the remaining ones. The extensive skeletal pneumaticity in theropods such as Majungasaurus demonstrates that a complex air-sac system and birdlike respiration evolved in birds’ theropod ancestors. The increased metabolism associated with homeothermy and powered flight requires an efficient gas exchange process during pulmonary ventilation. Moreover, recent anatomical and physiological studies show that alligators, and monitor lizards exhibit respiratory systems and unidirectional breathing akin to those of birds, which indicate that unidirectional breathing is a primitive characteristic of archosaurs or an even more inclusive group with the complex air-sac system evolving later within Archosauria.

The earliest diversification of extant birds (Neornithes) occurred during the Cretaceous period and after the mass extinction event at the Cretaceous-Paleogene (K-Pg) boundary, the Neoaves, the most diverse avian clade, suffered a rapid global expansion and radiation. Today, with more than 10500 living species, birds are the most species-rich class of tetrapod vertebrates.

 

References:

Xing Xu, Zhonghe Zhou, Robert Dudley, Susan Mackem, Cheng-Ming Chuong, Gregory M. Erickson, David J. Varricchio, An integrative approach to understanding bird origins, Science, Vol. 346 no. 6215, DOI: 10.1126/science.1253293.

Puttick, M. N., Thomas, G. H. and Benton, M. J. (2014), HIGH RATES OF EVOLUTION PRECEDED THE ORIGIN OF BIRDS. Evolution, 68: 1497–1510. doi: 10.1111/evo.12363 A.

H. Turner, D. Pol, J. A. Clarke, G. M. Erickson, M. A. Norell, A basal dromaeosaurid and size evolution preceding avian flight. Science 317, 1378–1381 (2007).pmid: 17823350.

V. Allen, K. T. Bates, Z. Li, J. R. Hutchinson, Linking the evolution of body shape and locomotor biomechanics in bird-line archosaurs. Nature 497, 104–107 (2013). doi: 10.1038/nature12059; pmid: 23615616

A. M. Balanoff, G. S. Bever, T. B. Rowe, M. A. Norell, Evolutionary origins of the avian brain. Nature 501, 93–96 (2013). doi: 10.1038/nature12424; pmid: 23903660

M. S. Y. Lee, A. Cau, D. Naish, G. J. Dyke, Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345, 562–566 (2014). doi: 10.1126/science.1252243; pmid: 25082702

Craig B. Lowe, Julia A. Clarke, Allan J. Baker, David Haussler and Scott V. Edwards, Feather Development Genes and Associated Regulatory Innovation Predate the Origin of Dinosauria, Mol Biol Evol (2015) 32 (1): 23-28. doi: 10.1093/molbev/msu309