Accepted Manuscript. News & Views. Primary feather vane asymmetry should not be used to predict the flight capabilities of feathered fossils

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1 Accepted Manuscript News & Views Primary feather vane asymmetry should not be used to predict the flight capabilities of feathered fossils Xia Wang, Robert L. Nudds, Colin Palmer, Gareth J. Dyke PII: S (17)30453-X DOI: Reference: SCIB 210 To appear in: Science Bulletin Please cite this article as: X. Wang, R.L. Nudds, C. Palmer, G.J. Dyke, Primary feather vane asymmetry should not be used to predict the flight capabilities of feathered fossils, Science Bulletin (2017), doi: j.scib This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

2 Primary feather vane asymmetry should not be used to predict the flight capabilities of feathered fossils Xia Wang 1*, Robert L. Nudds 2, Colin Palmer 3 & Gareth J. Dyke 4 1 School of Biological Science and Technology, University of Jinan, China 2 Faculty of Life Sciences, University of Manchester, Manchester, UK 3 Department of Earth Sciences, University of Bristol, Bristol, UK 4 Evolutionary Zoology, University of Debrecen, Hungary Author for correspondence: Xia Wang bio_wangx@ujn.edu.cn Reconstructing flight abilities of fossil birds from preserved wings and feathers is an important goal if we are to understand the evolution of flight. Wing-shape is known to correlate well with bird flight style [1], but functional wing-shape is almost impossible to reconstruct from fossils with a high degree of certainty. In contrast, however, individual primary feathers are often preserved with high fidelity and therefore, offer the possibility of a diagnostic tool for determining flight capabilities in fossil taxa. In living birds, the primary or flight feathers, which make up the distal section of the wing in birds are the most mechanically derived feathers and are typically asymmetric. Feather asymmetry (i.e. trailing edge vane width /leading edge vane width) affects the dynamic behaviour of the primary feathers[2], it is plausible to predict that feather vane asymmetry alone could be indicative of a bird s flight capabilities. The presence of primary feather vane asymmetry, and whether or not it is related to flight ability, has generated great deal of debate, particularly with regard to the interpretation of fossil bird flight capabilities, most notably for the Jurassic Archaeopteryx [3-5], the Cretaceous Confuciusornis [6] and more recently, non-avialan theropods with preserved feathers like Anchiornis [7]. Although a degree of division between flightless and volant extant bird primary feather vane asymmetry is evident [5], whether its diagnostic resolution is such as to differentiate different flight styles remains to be tested. Thus in this study we test the hypothesis that degree of primary feather vane asymmetry alone can be used to discern flight style in extant birds. Analysis of the dataset presented here (Table S1) shows that primary feather vane asymmetry may only be used to determine whether an extant bird is capable of flapping flight under limited circumstances (Figs. 1, S1; Table S3). Furthermore, our analyses show 1

3 that degree of primary feather vane asymmetry is not a good predictor of flight style within extant volant birds (Fig. 1, S1; Table S2). When phylogeny was controlled our data shows no significant relationship between wing-beat frequency and feather asymmetry (Fig.S3). However, the flight style groups used here are broad so it remains a possibility that a higher resolution definitions of these categories might prove more discerning. Although, again, overlap in the values for the categories used here would suggest otherwise, particularly as no consistent, nor strong relationship was found between a continuous variable proxy for flight style (wing-beat frequency) and vane asymmetry either. Certainly, for now at least, we argue that primary feather vane asymmetry data may only be used to predict flightlessness (asymmetry ratio 1.9) and flapping flight (asymmetry ratio >9.0) in extant birds and only then at 50% feather length (Fig. 1; Table S2, S3). This is consistent with the results of Speakman and Thomson [5] (and Feo et al. [10], which report a similar overlapping range of vane asymmetry ratios for flying and flightless species (Speakman and Thomson [5]: flightless species , flying species ; Feo et al [10]: flightless species , flying species ). Can the results from our extant sample usefully be applied to fossil birds? It is well-known that both the Berlin and London Archaeopteryx specimens possess primary feathers with vane asymmetry ratios of <2 [5]. Similarly, although quite clearly asymmetrical [6], at least some of the flight feathers of the basal pygostylian bird Confuciusornis have a ratio of 2. In addition, the primary feathers of the non-avialan dromaeosaur Microraptor all have vane asymmetry values <2 [8] while the feathers of the troodontid Anchiornis are symmetrical [7]. Thus based on feather vane asymmetry values alone we must conclude that all four of these fossil species were totally flightless, a conclusion, which is only likely to draw some consensus for Anchiornis and Microraptor. It is plausible, however, that feather vane asymmetry increased in tandem with the evolution of flight. Pertinently, it is also important to consider that there is currently no evidence to suggest that a wing constructed of flight feathers with symmetrical or moderately asymmetrical vanes is not capable of providing a useful flight surface. Furthermore, the wing feather arrangement on feathered fossils is different to extant birds. That of Anchiornis is constructed of multiple layers of coverts and the primaries of Archaeopteryx also appear layered [9]. Other features of Archaeopteryx flight feathers, for example, backward curvature and a longitudinal furrow on the ventral side of the rachis, are in common with extant birds, suggesting a flight function [4]. There are, of course, many other anatomical features that may be interpreted in terms of flight ability, but as already stated, this paper is concerned with feather vane asymmetry alone and as such, a lengthy discourse on other lines of evidence is not undertaken here. Thanks to new fossil discoveries, it is now known that feathered limbs are not unique to birds and, 2

4 indeed, that the presence of feathers does not necessarily imply flight ability. The possession of asymmetric primary feather vanes, however, has traditionally been linked with flapping flight, with a suggestion that the more asymmetric the feathers the more adept the flight capabilities [3,4]. It appears, however, that primary feather asymmetry can only be used to discern between some flightless and volant extant species, not among different flight style groups. There is also no clear trend for birds with more asymmetrical feathers to beat their wings less vigorously contra Feduccia and Tordoff [3], with the nature of the relationship between frequency and asymmetry depending upon where along the feather the measurement is taken. Again, the relationship between wing-beat frequency and vane asymmetry is not useful for determining flight ability. In conclusion, assuming that the relationship between fossil bird feather morphology and flight style mirrors that seen in extant birds, the diagnostic power of feather vane asymmetry measures is extremely limited. Furthermore, without evidence that feather vane asymmetry is a prerequisite for a fully functioning wing it should not be used to predict the flight capabilities or flight styles of fossil taxa. Our findings are consistent with the suggestion of Feo et al [10] that feather barb geometry (e.g. barb length, barb angles) might be better understood to draw confident conclusions about the aerodynamic capabilities of flight feathers in the fossil record. Acknowledgments We thank Matthew Parkes and Leona Leonard for collections access in NMNH Dublin. This work was supported by the Shandong Provincial Natural Science Foundation, China to X. W. (ZR2017QD013). Conflict of interest The authors declare that they have no conflict of interest. References 1. Rayner JMV (1988) Form and function in avian flight. In: Johnston RF. Current ornithology. New York: Plenum Press Ennos A, Hickson J, Roberts A (1995) Functional morphology of the vanes of the flight feathers of the pigeon columba livia. J Exp Biol 198: Feduccia A, Tordoff HB (1979) Feathers of Archaeopteryx - asymmetric vanes indicate aerodynamic function. Science 203: Norberg RA (1985) Function of vane asymmetry and shaft curvature in bird flight feathers; inference on flight ability of Archaeopteryx. The beginnings of birds: proceedings of the international Archaeopteryx conference, Eichstätt Speakman JR, Thomson SC (1994) Flight capabilities of Archaeopteryx. Nature 370: Chiappe LM, Ji S, Ji Q et al (1999) Anatomy and systematics of the confuciusornithidae (theropoda : Aves) from the late mesozoic of northeastern china. Bull Amer Mus Nat Hist Hu D, Hou L, Zhang L et al (2009) A pre-archaeopteryx troodontid theropod from china with long feathers on the metatarsus. Nature 461: Xu X, Zhou Z, Wang X et al (2003) Four-winged dinosaurs from china. Nature 421:

5 9. Longrich NR, Vinther J, Meng Q et al (2012) Primitive wing feather arrangement in Archaeopteryx lithographica and Anchiornis huxleyi. Curr Biol 22: Feo TJ, Field DJ, Prum RO (2015) Barb geometry of asymmetrical feathers reveals a transitional morphology in the evolution of avian flight. Proc. R. Soc. B 282: Figure legends Fig.1 Box plot showing feather vane asymmetry values for each flight style group (CF = continuous flapping, FG = flapping and gliding, FS = flapping and soaring, PT = passerine-type flight and NF = non-flight ) at the 50% position along the primary feather length (from calamus to tip). 4

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Deposited on: 16 November 2012

Deposited on: 16 November 2012 Wang, X., McGowan, A.J., and Dyke, G.J. (2011) Avian wing proportions and flight styles: first step towards predicting the flight modes of Mesozoic birds. PLoS ONE, 6 (12). e28672. ISSN 1932-6203 http://eprints.gla.ac.uk/71705

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