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Unique Caudal Plumage of Jeholornis and Complex Tail Evolution in Early Birds

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Unique Caudal Plumage of Jeholornis and Complex Tail Evolution in Early Birds Unique caudal plumage of Jeholornis and complex tail evolution in early birds Jingmai O’Connora,1, Xiaoli Wangb,c, Corwin Sullivana, Xiaoting Zhengb,c, Pablo Tubarod, Xiaomei Zhangc, and Zhonghe Zhoua,1 aKey Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China; bInstitute of Geology and Paleontology, Linyi University, Linyi City, Shandong 276005, China; cShandong Tianyu Museum of Nature, Pingyi, Shandong 273300, China; and dDivision Ornitologia, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia,” Consejo Nacional de Investigaciones Científicas y Técnicas, C1405DJR Buenos Aires, Argentina Contributed by Zhonghe Zhou, September 12, 2013 (sent for review July 2, 2013) The Early Cretaceous bird Jeholornis was previously only known to lift, and thus were interpreted as ornamental (8). Here, we have a distally restricted ornamental frond of tail feathers. We present a more complete description of the caudal plumage of describe a previously unrecognized fan-shaped tract of feathers Jeholornis based on a revised study of SDM 20090109 and several situated dorsal to the proximal caudal vertebrae. The position other published and unpublished specimens (Table 1), some of and morphology of these feathers is reminiscent of the specialized which preserve a previously undocumented pteryla (feather tract) upper tail coverts observed in males of some sexually dimorphic on the proximal tail. The new specimens indicate a previously neornithines. As in the neornithine tail, the unique “two-tail” unrecognized degree of diversity in the tail plumage config- plumage in Jeholornis probably evolved as the result of complex urations of Mesozoic birds and demonstrate that tail evolution interactions between natural and sexual selective pressures and did not follow a simple path from the “frond-like” arrangement served both aerodynamic and ornamental functions. We suggest seen in Archaeopteryx and some derived nonavian theropods to that the proximal fan would have helped to streamline the body the “fan-like” arrangement seen in ornithuromorphs. We de- and reduce drag whereas the distal frond was primarily ornamen- scribe the complete tail of Jeholornis, consider its possible func- tal. Jeholornis reveals that tail evolution was complex and not tions, and discuss trends in tail evolution in both Mesozoic and a simple progression from frond to fan. living birds. EVOLUTION Aves | Mesozoic | Jehol Description Several specimens of Jeholornis (Table 1) preserve elongate ail feathers are extraordinarily diverse in form and function pennaceous feathers that appear to project from an area dorsal Tin extant birds. A shallow forked tail is predicted by flight to the proximal caudal vertebrae (Figs. 1–3, Figs. S1 and S2). In models to be aerodynamically optimal in the sense of having the one specimen, these feathers were previously identified as dis- highest possible moment:drag ratio, but the rectrices (flight placed remiges (8), but new additional specimens clearly indicate feathers of the tail) and tectrices (upper tail coverts) that to- that the feathers represent a previously undescribed pteryla gether form the “tail” have been modified for other functions in forming a proximal tail fan. Most specimens preserve four clear many taxa (1). The elaborate ornamental tail feathers seen in the feathers, but these fans may well be incomplete. The feathers are males of some sexually dimorphic birds are the quintessential shorter than the remiges but slightly longer and much broader example of the power of sexual selection to dictate morphology than the distal tail feathers (Table 1). The feathers appear to (2). The Jehol Biota is recognized as the second oldest and most attach to the dorsal surface of the tail above the proximal caudal diverse Mesozoic avifauna but is most celebrated for its nu- vertebrae, close to the transition from short to elongate mor- merous specimens preserving integumentary structures and phology that occurs at the fifth to sixth caudal vertebra and were other soft tissues that are normally exceedingly rare in the fossil record. Preserved tail feathers are known for nearly every major Significance avian clade in the Jehol (3), revealing patterns that strongly parallel those observed in the tails of living birds. The Jehol Biota We describe the presence of essentially two functional tails in contains the earliest known members of both Ornithuromorpha, the Early Cretaceous Jeholornis (the second most primitive the derived clade that includes living birds (3), and Enantior- bird)—one like that of some modern birds with a fan-shaped nithes, the dominant avians of the Cretaceous. These relatively tract of feathers over the proximal tail vertebrae and another derived birds lived alongside an array of more primitive groups distal frond like that of feathered dinosaurs such as Cau- including the basalmost pygostylian clades, Sapeornithiformes and dipteryx and Microraptor. We suggest that the unique “two- Confuciusornithiformes, and the long boney-tailed Jeholornis.In tail” plumage in Jeholornis probably evolved as the result of the latter taxon, the tail was even longer (and contained more in- complex interactions between natural and sexual selective dividual vertebrae) than in Archaeopteryx, despite most phylogenetic pressures and served both aerodynamic (flight and balance, analyses resolving Jeholornis in a more derived position (4, 5). etc.) and ornamental functions (communication/display, etc.). The tails of enantiornithines and confuciusornithiforms com- Our aerodynamic analysis also provides a plausible functional monly preserve a pair of elongate racket plumes, modified pen- explanation for the elongation of the boney tail in Jeholornis naceous feathers that carry barbs only near their distal ends. relative to Archaeopteryx. These feathers are the earliest record of an ornamental tail morphology within Aves and has been suggested to indicate Author contributions: J.O., X. Zheng, and Z.Z. designed research; J.O., X.W., C.S., P.T., X. Zhang, and Z.Z. performed research; X. Zheng contributed new reagents/analytic tools; sexual dimorphism in these two clades (6, 7). A recently described J.O., X.W., C.S., and P.T. analyzed data; and J.O., C.S., and Z.Z. wrote the paper. Jeholornis specimen of (SDM, Shandong Museum, 20090109) The authors declare no conflict of interest. preserves the complete distal caudal integument, a palm-like 1 To whom correspondence may be addressed. E-mail: [email protected] or frond of feathers near the tip of the tail (8). Unlike in Archae- [email protected]. opteryx , the tail feathers are restricted to the distal end of the tail This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. and do not form a large cohesive surface capable of generating 1073/pnas.1316979110/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1316979110 PNAS Early Edition | 1of5 Table 1. A list of Jeholornis sp. specimens preserving tail plumage Femur Fan, no. of Preserved Frond, no. of Preserved Specimen length Remiges feathers length, fan feathers length, frond SDM 20090109.1 57.9 — 4 90 Complete - 11 90 STM2-18 53 Preserved 4–6103 —— STM2-8 68.8 Preserved 4 83.7 Incomplete (45.9) STM2-11 47.6 Preserved ——Ventral half, 6 72.6 STM2-23 73* Preserved (1–3) —— — STM2-37 68.4 Preserved 4–6113 — STM3-3 66 — 4105 —— STM3-4 58 — 6(53–57) Incomplete (45) STM3-30 56 — 4 72 Dorsal half, 6–7 (52) IVPP V13350 55.6 —— —Incomplete — IVPP V13353 64 Preserved —— — — All measurements are in millimeters. Parentheses indicate incomplete measurements. Preserved feather lengths were taken from the longest of the feathers forming the fan and frond respectively. *Estimates. presumably rooted in the soft tissues of this region. Based on comparable in rachis thickness with the remiges and proximal tail their appearance in one specimen that is preserved in dorsal view feathers (0.366–0.398 mm), their vanes are narrow and curved and (STM2-37; Fig. 1), the feathers are inferred to be arranged into taper sharply along their distal thirds. The vanes are preserved in a horizontal fan originating from a single area, a configuration only two specimens, and it is unclear whether they are symmetrical. broadly similar to the tail fans typical of living birds. However, in In STM2-11, only the caudal half of each vane is preserved most specimens, the skeleton is preserved in lateral view, and the whereas, in SDM 20090109, the feathers appear symmetrical on feathers are displaced and rotated so that their broad surfaces one side of the tail and asymmetrical on the other. are parallel to the surface of the slab (Fig. 2 A and D). The medial feathers are longer than the lateral feathers, giving the fan a graded morphology. The fan is consistently preserved as a unit, suggesting that the calami of the individual feathers were bound together by liga- ments. The absence of bending or distortion in any of the feathers indicates that the rachises were fairly stiff. The rachises are comparable in diameter with those of the remiges, rather than extremely wide as in the tail feathers of Confuciusornis and some enantiornithines (9). In STM2-37, the preserved rachises of the remiges range in diameter from 0.36 to 0.52 mm whereas those of the proximal tail feathers range from 0.32 to 0.44 mm, although poor preservation makes these values only approx- imations. In specimens preserved in lateral view, the vanes of the proximal tail feathers appear to be asymmetric and to taper distally (Fig. 2 A, B,andD). However, these characteristics probably result from distortion. In STM2-37, the feathers have symmetrical vanes, and one clearly preserved feather has a broad, rounded distal margin (Fig. 1). The amount of overlap between the feathers is unclear. In STM2-37, the preserved feathers are separated by small spaces, but the tail fan is probably incomplete. We interpret the feathers as having overlapped mediolaterally to some degree in life, forming a graded fan-shaped surface (Fig.
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    The remarkable fossils from the Early Cretaceous Jehol Biota of China and how they have changed our knowledge of Mesozoic life Presidential Address, delivered 2nd May 2008 Michael J. Benton1, Zhou Zhonghe2, Patrick J. Orr3, Zhang Fucheng2 & Stuart L. Kearns1 BENTON, M. J., ZHOU Z., ORR, P. J., ZHANG, F. & KEARNS, S. L. 2008. The remarkable fossils from the Early Cretaceous Jehol Biota of China and how they have changed our knowledge. Proceedings of the Geologists’ Association, 119, 209–228. Palaeontologists and others have been repeatedly amazed by reports of spectacularly well-preserved fossils from China, and one of the key sources has been the Jehol Biota of Liaoning, Hebei and Inner Mongolia in NE China. The Jehol Biota consists of three main horizons, the Dabeigou, Yixian and Jiufotang formations, spanning the late Hauterivian to early Aptian (131–120 Ma) of the Early Cretaceous and, collectively, these have produced thousands of essentially complete specimens of plants, insects, aquatic invertebrates, fishes, frogs, salamanders, turtles, lizards, choristoderes, pterosaurs, dinosaurs, birds and mammals. Most of the specimens show some aspect of exceptional preservation, ranging from clear impressions of the body outlines to traces of soft tissues (liver, teleost air sac, eye spots) and external body coverings (scales, feathers, hair). The claim was made that these discoveries have revolutionized our understanding of evolution through this critical part of the Cretaceous Terrestrial Revolution. Key insights have come from the numerous specimens of dinosaurs with feathers, but numerical study shows that only the finds of birds and mammals have substantially changed our views about global diversity and patterns of evolution through the Early Cretaceous.
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