Forelimb feathering, soft tissues, and skeleton of the flying dromaeosaurid Microraptor

Abstract

Background: Microraptor is an essential animal for understanding the evolution of flight in birds and their closest relatives. Recent studies have uncovered evidence of its powered flight potential and details of its diet and ecology. However, we are still missing a thorough description of the anatomy of Microraptor connecting feathers, soft tissues, and osteology together. Here we focus on the forelimbs of ten new Microraptor specimens from the Shandong Tianyu Museum of Nature studied under Laser-Stimulated Fluorescence. We compared our results with extensively studied existing specimens (e.g., IVPP V13352 and BMNHC PH881), other key early paravians (e.g., Anchiornis, Archaeopteryx and Confuciusornis), as well as modern birds to expand what we know about flight origins, and early diverging paravian theropods more generally.

Results: Plumage was previously only minimally known. Reconstruction of the forewings relied on brief descriptions of the primary and secondary feathers. With the new specimens studied here, we uncovered the whole shape of the wing from the tip of the digits to the proximal end of the ulna, the different layers of feathers, and the number as well as characteristics of each feather type. Skeletal features of the forelimb remain mostly unchanged from previous descriptions, but we bring new information regarding wrist bones and functional implications of humerus and radius features. The most significant advances have been recovered in preserved soft tissues including those of the shoulder, propatagium and postpatagium. In particular, the new specimens of Microraptor help us to understand the impact of the soft tissues on lift generation and cohesiveness of the forewing.

Conclusions: This study permitted us to recreate the most accurate forewing of Microraptor to date. Taken together, new information on the forelimb anatomy shows that Microraptor shares many of the forewing characteristics of early avialans and modern birds, and helps us to better understand the flight behaviour and ecology of this iconic and unique 'four-winged' animal along with its role in flight evolution. These results serve as a starting point to conduct more precise and integrative analyses (e.g., including hindwings and/or tail) on the locomotor behaviours of Microraptor.

Keywords: Microraptor; Feathered dinosaur; Feathering; Flight anatomy; Flight evolution; Forelimb; Theropod; Wing.

Fig. 1

Composite reconstruction of the forewing feathering of Microraptor based on 14 studied specimens. The wing has four to five layers of feathers: one of marginal coverts, possibly one of lesser coverts, one of ~ 35 median coverts, one of greater coverts (~ 10 primary coverts and ~ 17 secondary coverts) and one of flight feathers (~ 10 primary remiges plus ~ 17 secondary feathers). Secondary greater covert rachises are directly located on top of the secondary feather rachises, whereas the rachises of primary greater coverts are located offset compared to primary remex rachises, as seen in modern birds. Marginal coverts of Microraptor follow the same pattern as seen in modern birds. Scale bar is 50 mm

Fig. 2

Forelimbs of Microraptor IVPP V13352 showing a well-preserved secondary greater covert series. A Under LSF and B as an anatomical line drawing. Colour scheme is as follows: darker blues/purples (colours in large boxes), preserved feathers; pale blues/purples (colours in inset boxes), reconstructed feather outlines; white, preserved skeleton; grey, reconstructed skeletal sections; dark pink, preserved soft tissues; pale pink, reconstructed soft tissues. Short-dashed lines are reconstructed outlines. This colour scheme will be used in all figures in this study (Figs. 2, 3, 4, 5, 6, 7, 8, 9, and 10, and S1-4). D, digits with interpreted numbers; H, humerus; Mc, metacarpal; P, primary remiges; Ra, radius; Rc, radiale carpal; Se, semilunate carpal; U, ulna. This specimen preserves the best secondary greater covert series with an estimated count of ~ 17. It also preserves the crescent-shaped semilunate articulating with metacarpals I and II. Scale bar is 50 mm

Fig. 3

Forelimbs of Microraptor specimen STM 5–9 showcasing longest primary in P9 position. A LSF image and B as an anatomical line drawing. R, preserved rachis. This specimen has the most extended forelimb position of all the studied specimens, revealing the prominent biceps tuberosity of the radius. It is also the only specimen studied with remex P9 as the longest primary remex. See colour scheme key in Fig. 2. Scale bar is 50 mm

Fig. 4

Forelimbs of Microraptor BMNHC PH881 showcasing smallest primaries in P1 and P2 position. A Photo of BMNHC PH881 modified from Li et al. [11] and B as an anatomical line drawing. See colour scheme key in Fig. 2. Scale bar is 50 mm

Fig. 5

Forelimbs of Microraptor STM 5–93 showcasing the propatagium. A LSF image of the slab and B as an anatomical line drawing. Dc3, distal carpal 3; Pp, postpatagium; Ppt, propatagium. The specimen preserves the best propatagia and displays feather sheaths of the secondary feathers in the left postpatagium. See colour scheme key in Fig. 2. Scale bar is 50 mm

Fig. 6

Forelimbs of Microraptor STM 5–172 with marginal coverts in life position in the propatagium. A LSF image of the counterslab and B anatomical line drawing. The specimen displays the original arrangement of the marginal coverts. Instead of lying anterior to the forelimb, the marginal coverts are preserved in anatomical position: projecting perpendicular to the wing profile in the propatagium, as seen in modern birds. See colour scheme key in Fig. 2. Scale bar is 50 mm

Fig. 7

Forelimbs of Microraptor STM 5–4 showcasing the lesser and median coverts. A Under LSF and B as an anatomical line drawing. This specimen is the only one with distinguishable layers of lesser and median coverts, indicating that Microraptor potentially possessed five layers of feathers on its forewing. See colour scheme key in Fig. 2. Scale bar is 50 mm

Fig. 8

Forelimbs of Microraptor STM 5–75 showcasing distal carpal 3. A LSF image of the slab and B as an anatomical line drawing. This is the only studied specimen preserving a distal carpal 3 in anatomical position, completing the wrist of Microraptor (semilunate + radiale) with a third bone. See colour scheme key in Fig. 2. Scale bar is 50 mm

Fig. 9

Forelimbs of Microraptor STM 5–221 showcasing the soft tissues preserved alongside the bones. A Under LSF and B as an anatomical line drawing. The specimen preserves extensive soft tissues, including those of the shoulder. See colour scheme key in Fig. 2. Scale bar is 50 mm

Fig. 10

Forelimbs of Microraptor STM 5–109 showcasing upper arm feathering and the postpatagium. A LSF image of the counterslab and B as an anatomical line drawing. The specimen preserves the only feathers found from the upper arm of Microraptor. It also displays an exceptionally preserved postpatagium (manus section) with the feather sheaths of the primary remiges and primary greater coverts. See colour scheme key in Fig. 2. Scale bar is 50 mm