An early juvenile enantiornithine specimen from the Early Cretaceous of Spain

The slab and counterslab of MPCM-LH-26189

Mesozoic remains of juvenile birds are rare. To date, the only records are from the Early Cretaceous of China and Spain, from the mid-Cretaceous of  Myanmar, and from the Late Cretaceous of Argentina and Mongolia. The most recent finding from the Early Cretaceous of Las Hoyas, Spain, provide an insight into the osteogenesis of the Enantiornithes, the most abundant clade of Mesozoic birds. Previous records of Enantiornithes from the Las Hoyas fossil site include: Eoalulavis hoyasi, Concornis lacustris, and Iberomesornis romerali.

The latest specimen, MPCM-LH-26189, a nearly complete and largely articulated skeleton (only the feet, most of its hands, and the tip of the tail are missing), is very small. The specimen died around the time of birth, a crucial moment to study the osteogenesis in birds. The skull, is partially crushed, and is large compared to the body size. The braincase is fractured. The frontals and the parietals form a uniformly curved cranial vault. The cerebrocast shows a very slight inflation, suggesting that the cerebral anatomy of MPCM-LH-26189 falls in between that of the Archaeopteryx, and the putative basal ornithurine Cerebavis, whose telencephalic expansion is close to most extant birds. The cervical series is composed of 9 vertebrae. There are 10  thoracic vertebrae, and the sacrum appears to be composed of 5–6 vertebrae. The prezygapophyses of the mid-thoracic vertebrae extend beyond the cranial articular surface. The thoracic ribs are joint to the thoracic vertebrae. The two coracoids, the furcula, and three sternal ossifications are preserved. The furcula is Y-shapped. Both humeri, ulnae, and radii are also preserved.

Reconstruction of MPCM-LH-26189 by Raúl Martín

The osteohistological analysis of the left humerus shows a dense pattern of longitudinal grooves. Those grooves correspond to primary cavities, which open onto the surface of the cortex in young and fast-growing bone. The shaft of the tibia and radius show very-thin cortices. In addition,  the primary nature of the vascularisation, the round shape of the osteocytes lacunae and the uneven peripheral margin of the medullary cavity (with no endosteal bone), strongly suggests that the bone was actively growing when the bird died.

Enantiornithines show a mosaic of characters, reflecting their intermediate phylogenetic position between the basal-pygostylians and modern bird. In this clade, the sternum adopts an elaborate morphology, and in adult Enantiornithes, no more than eight free caudal vertebrae precede the pygostyle. The differences observed in the ossification of the sternum and the number of free caudal vertebrae in MPCM-LH-26189, when it compared to other juvenile enantiornithines, reveal a clade-wide asynchrony in the sequence of ossification of the sternum and tail, suggesting that the developmental strategies of these basal birds may have been more diverse than previously thought.

References:

Fabien Knoll, et al., “A diminutive perinate European Enantiornithes reveals an asynchronous ossification pattern in early birds,” Nature Communications, volume 9, Article number: 937 (2018) doi:10.1038/s41467-018-03295-9

Chiappe, L. M., Ji, S. & Ji, Q. Juvenile birds from the Early Cretaceous of China: implications for enantiornithine ontogeny. Am. Mus. Novit. 3594, 1–46 (2007).

 

 

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The First 100 Million Years of Avian History.

The basal avian Sapeornis chaoyangensis (From Wikimedia Commons)

The basal avian Sapeornis chaoyangensis (From Wikimedia Commons)

Birds originated from a theropod lineage more than 150 million years ago. By the Early Cretaceous, they diversified, evolving into a number of groups of varying anatomy and ecology. 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. The Jehol Biota is formed from two formations: the Yixian Formation, and the Jiufotang Formation, and contain the most diversified avifauna known to date. Among them was the long bony-tailed Jeholornis, only slightly more derived than Archaeopteryx, that lived with Sapeornis, Confuciusornis, and the earliest members of Enantiornithes and Ornithuromorpha. The last two groups, form the clade Ornithothoraces, characterized by a keeled sternum, elongate coracoid, narrow furcula, and reduced hand.

Ornithuromorphs, include Gansus, Patagopteryx, Yixianornis, and Apsaravis, which form a grade on the line to Ornithurae, a derived subgroup that includes modern birds and their closest fossil relatives (Brusatte et al., 2015).

The single best record of a Cretaceous neornithine is the partial skeleton of Vegavis from the latest Cretaceous (around 68–66 million years ago) of Antarctica.

Zhenyuanlong suni (photo by Junchang Lu¨ ) from the Jehol Biota.

Zhenyuanlong suni (photo by Junchang Lu) from the Jehol Biota.

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. Birds also exhibit the most advanced vertebrate visual system, with a highly developed ability to distinguish colors over a wide range of wavelengths.

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. Zhenyuanlong suni, from the Yixian Formation, provides the first evidence of well-developed pennaceous feathers in a large, non-flying dromaeosaur. Evidence indicates that the earliest feathers evolved in non-flying dinosaurs, likely for display and/or thermoregulation, and later were co-opted into flight structures in the earliest birds (Brusatte et al., 2015).

The basal avian Jeholornis prima.

The basal avian Jeholornis prima.

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. Archaeopteryx lacked a bony sternum and a compensatory specialized gastral basket for anchoring large flight muscles (O’Connor et al., 2015), while Jelohornis had several derived flight-related features of modern birds like fused sacral vertebrae, an elongated coracoid with a procoracoid process, a complex sternum, a narrow furcula, and curved scapula. In Enantiornithines, their robust pygostyle appears to have been unable to support the muscles that control the flight feathers on the tail in modern birds. The increased metabolism associated with homeothermy and powered flight requires an efficient gas exchange process during pulmonary ventilation. 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. A genome-scale molecular phylogeny indicates that nearly all modern ordinal lineages were formed within 15 million years after the extinction, suggesting a particularly rapid period of both genetic evolution and the formation of new species. Today, with more than 10500 living species, birds are the most species-rich class of tetrapod vertebrates.

 

References:

Brusatte, S. L., O’Connor, J. K., and Jarvis, E. D. 2015. The origin and diversification of birds. Current Biology, 25, R888-R898

Padian, K., and Chiappe, L.M. (1998). The origin and early evolution of birds. Biol. Rev. 73, 1–42.

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.

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.