Shifts in stability and control effectiveness during evolution of Paraves support aerial maneuvering hypotheses for flight origins

The capacity for aerial maneuvering was likely a major influence on the evolution of flying animals. Here we evaluate consequences of paravian morphology for aerial performance by quantifying static stability and control effectiveness of physical models for numerous taxa sampled from within the lineage leading to birds (Paraves). Results of aerodynamic testing are mapped phylogenetically to examine how maneuvering characteristics correspond to tail shortening, forewing elaboration, and other morphological features. In the evolution of Paraves we observe shifts from static stability to inherently unstable aerial planforms; control effectiveness also migrated from tails to the forewings. These shifts suggest that a some degree of aerodynamic control and capacity for maneuvering preceded the evolution of a strong power stroke. The timing of shifts also suggests features normally considered in light of development of a power stroke may play important roles in control.

[1]  Xiaoting Zheng,et al.  Hind Wings in Basal Birds and the Evolution of Leg Feathers , 2013, Science.

[2]  Zhonghe Zhou,et al.  A beaked bird from the Jurassic of China , 1995, Nature.

[3]  Gareth J Dyke,et al.  Forelimb Posture in Dinosaurs and the Evolution of the Avian Flapping Flight-Stroke , 2009, Evolution; international journal of organic evolution.

[4]  R. Templin,et al.  Biplane wing planform and flight performance of the feathered dinosaur Microraptor gui , 2007, Proceedings of the National Academy of Sciences.

[5]  François Escuillié,et al.  A Jurassic avialan dinosaur from China resolves the early phylogenetic history of birds , 2013, Nature.

[6]  Matthew R Evans,et al.  Birds' tails do act like delta wings but delta-wing theory does not always predict the forces they generate , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[7]  L. Chiappe,et al.  A NEW BASAL LINEAGE OF EARLY CRETACEOUS BIRDS FROM CHINA AND ITS IMPLICATIONS ON THE EVOLUTION OF THE AVIAN TAIL , 2008 .

[8]  O. Rauhut,et al.  New specimen of Archaeopteryx provides insights into the evolution of pennaceous feathers , 2014, Nature.

[9]  M. Koehl,et al.  Using physical models to study the gliding performance of extinct animals. , 2011, Integrative and comparative biology.

[10]  N. Longrich,et al.  Structure and function of hindlimb feathers in Archaeopteryx lithographica , 2006, Paleobiology.

[11]  Zhonghe Zhou,et al.  Life history of a basal bird: morphometrics of the Early Cretaceous Confuciusornis , 2008, Biology Letters.

[12]  P. Tubaro,et al.  Unique caudal plumage of Jeholornis and complex tail evolution in early birds , 2013, Proceedings of the National Academy of Sciences.

[13]  J. Vinther,et al.  Plumage Color Patterns of an Extinct Dinosaur , 2010, Science.

[14]  M. Koehl,et al.  Aerodynamic Characteristics of a Feathered Dinosaur Measured Using Physical Models. Effects of Form on Static Stability and Control Effectiveness , 2013, bioRxiv.

[15]  Karel F. Liem,et al.  Functional Anatomy of the Vertebrates: An Evolutionary Perspective , 1994 .

[16]  L. Chiappe,et al.  The origin of birds and their flight. , 1998, Scientific American.

[17]  R. Dudley Mechanisms and Implications of Animal Flight Maneuverability1 , 2002, Integrative and comparative biology.

[18]  G. Taylor,et al.  Animal flight dynamics II. Longitudinal stability in flapping flight. , 2003, Journal of theoretical biology.

[19]  M. Koehl,et al.  Aerodynamic characteristics of a feathered dinosaur measured using physical models. Effects of form on static stability and control effectiveness , 2013, bioRxiv.

[20]  Xiaoting Zheng,et al.  On the absence of sternal elements in Anchiornis (Paraves) and Sapeornis (Aves) and the complex early evolution of the avian sternum , 2014, Proceedings of the National Academy of Sciences.

[21]  M. Norell,et al.  A Review of Dromaeosaurid Systematics and Paravian Phylogeny , 2012 .

[22]  Barnes W. McCormick,et al.  Aerodynamics, Aeronautics and Flight Mechanics , 1979 .

[23]  K. Padian Cross-Testing Adaptive Hypotheses: Phylogenetic Analysis and the Origin of Bird Flight1 , 2001 .

[24]  G. Nabuurs,et al.  Ecologically implausible carbon response? , 2008, Nature.

[25]  R. Dudley,et al.  Animal aloft: the origins of aerial behavior and flight. , 2011, Integrative and comparative biology.

[26]  Sara H Burch,et al.  Complete forelimb myology of the basal theropod dinosaur Tawa hallae based on a novel robust muscle reconstruction method , 2014, Journal of anatomy.

[27]  R. Dudley,et al.  Backward flight in hummingbirds employs unique kinematic adjustments and entails low metabolic cost , 2012, Journal of Experimental Biology.

[28]  J. O’Connor,et al.  Pre‐modern Birds: Avian Divergences in the Mesozoic , 2011 .

[29]  Stefan Gottschalk,et al.  Aerodynamics Aeronautics And Flight Mechanics , 2016 .

[30]  Xing Xu,et al.  An Archaeopteryx-like theropod from China and the origin of Avialae , 2011, Nature.

[31]  Gottfried Sachs,et al.  Yaw stability in gliding birds , 2005, Journal of Ornithology.

[32]  K. Dial,et al.  A fundamental avian wing-stroke provides a new perspective on the evolution of flight , 2008, Nature.

[33]  S. Gatesy,et al.  FROM FROND TO FAN: ARCHAEOPTERYX AND THE EVOLUTION OF SHORT‐TAILED BIRDS , 1996, Evolution; international journal of organic evolution.

[34]  Russ Tedrake,et al.  On the controllability of fixed-wing perching , 2009, 2009 American Control Conference.

[35]  Adrian L. R. Thomas On the Tails of Birds , 1997 .

[36]  Gottfried Sachs,et al.  Tail effects on yaw stability in birds. , 2007, Journal of theoretical biology.

[37]  John R. Hutchinson,et al.  Linking the evolution of body shape and locomotor biomechanics in bird-line archosaurs , 2013, Nature.

[39]  Zhonghe Zhou,et al.  A new species of Jeholornis with complete caudal integument , 2012 .

[40]  Zhonghe Zhou,et al.  Four-winged dinosaurs from China , 2003, Nature.

[41]  R. Dudley,et al.  Ontogeny of aerial righting and wing flapping in juvenile birds , 2014, bioRxiv.

[42]  S. Gatesy,et al.  Long-axis rotation: a missing degree of freedom in avian bipedal locomotion , 2014, Journal of Experimental Biology.

[43]  R. Blickhan,et al.  Dynamic and static stability in hexapedal runners. , 1994, The Journal of experimental biology.

[44]  Gareth J Dyke,et al.  Narrow Primary Feather Rachises in Confuciusornis and Archaeopteryx Suggest Poor Flight Ability , 2010, Science.

[45]  S. Levin,et al.  A long-tailed , seed-eating bird from the Early Cretaceous of China , 2022 .

[46]  M. Norell,et al.  Reconstruction of Microraptor and the Evolution of Iridescent Plumage , 2012, Science.

[47]  J. Maynard Smith,et al.  THE IMPORTANCE OF THE NERVOUS SYSTEM IN THE EVOLUTION OF ANIMAL FLIGHT , 1952 .

[48]  T. Teichmann,et al.  Dynamics of Flight: Stability and Control , 1959 .

[49]  J. Hutchinson,et al.  Shake a Tail Feather: The Evolution of the Theropod Tail into a Stiff Aerodynamic Surface , 2013, PloS one.

[50]  B. Tobalske,et al.  Ontogeny of lift and drag production in ground birds , 2011, Journal of Experimental Biology.

[51]  Zhonghe Zhou,et al.  Anatomy of the primitive bird Sapeornis chaoyangensis from the Early Cretaceous of Liaoning, China , 2003 .

[52]  Zhonghe Zhou,et al.  Palaeontology: Leg feathers in an Early Cretaceous bird , 2004, Nature.

[53]  B. Ganapathisubramani,et al.  Aerodynamic performance of the feathered dinosaur Microraptor and the evolution of feathered flight , 2013, Nature Communications.

[54]  Russ Tedrake,et al.  System Identification of Post Stall Aerodynamics for UAV Perching , 2009 .

[55]  Joel Cracraft,et al.  Assembling the tree of life , 2004 .

[56]  D. Evangelista Aerial Righting, Directed Aerial Descent, and Maneuvering in the Evolution of Flight in Birds , 2013 .

[57]  M. G. McCay,et al.  Aerodynamic stability and maneuverability of the gliding frog Polypedates dennysi. , 2001, The Journal of experimental biology.

[58]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[59]  Robert J Full,et al.  Aerial righting reflexes in flightless animals. , 2011, Integrative and comparative biology.

[60]  S. Olson Anatomy and Systematics of the Confuciusornithidae (Theropoda: Aves) from the Late Mesozoic of Northeastern China , 2000 .

[61]  C. J. Clark,et al.  The Evolution of Tail Shape in Hummingbirds , 2010 .

[62]  A Tetrapteryx stage in the ancestry of birds , 1915 .

[63]  D. B. Baier,et al.  The origin of the avian flight stroke: a kinematic and kinetic perspective , 2005, Paleobiology.

[64]  Xing Xu,et al.  A pre-Archaeopteryx troodontid theropod from China with long feathers on the metatarsus , 2009, Nature.

[65]  Jonathan Daniel Munk The Descent of Ant , 2011 .

[66]  D. Watson Vertebrate Paleontology , 1946, Nature.

[67]  K. Dial Wing-Assisted Incline Running and the Evolution of Flight , 2003, Science.

[68]  R. Full,et al.  Active tails enhance arboreal acrobatics in geckos , 2008, Proceedings of the National Academy of Sciences.

[69]  M. Koehl,et al.  FUNCTIONAL COMPLEXES AND ADDITIVITY IN PERFORMANCE: A TEST CASE WITH “FLYING” FROGS , 1990, Evolution; international journal of organic evolution.

[70]  B. Tobalske,et al.  From baby birds to feathered dinosaurs: incipient wings and the evolution of flight , 2014, Paleobiology.

[71]  James Tangler,et al.  Wind Turbine Post-Stall Airfoil Performance Characteristics Guidelines for Blade-Element Momentum Methods: Preprint , 2005 .

[72]  R. Full,et al.  The role of the mechanical system in control: a hypothesis of self-stabilization in hexapedal runners , 1999 .

[73]  G. Taylor,et al.  Animal flight dynamics I. Stability in gliding flight. , 2001, Journal of theoretical biology.

[74]  P. Christiansen,et al.  Body plumage in Archaeopteryx: a review, and new evidence from the Berlin specimen , 2004 .

[75]  Zhonghe Zhou,et al.  Jeholornis compared to Archaeopteryx, with a new understanding of the earliest avian evolution , 2003, Naturwissenschaften.

[76]  R. Full,et al.  Dynamic stabilization of rapid hexapedal locomotion. , 2002, The Journal of experimental biology.

[77]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[78]  J. Cracraft,et al.  Phylogenetic relationships among modern birds (Neornithes): towards an avian tree of life , 2004 .

[79]  Zhonghe Zhou,et al.  A new Lower Cretaceous bird from China and tooth reduction in early avian evolution , 2010, Proceedings of the Royal Society B: Biological Sciences.

[80]  John B. Peterson,et al.  of Aerodynamic Characteristics , 1980 .

[81]  Enpu Gong,et al.  Model tests of gliding with different hindwing configurations in the four-winged dromaeosaurid Microraptor gui , 2010, Proceedings of the National Academy of Sciences.

[82]  Fucheng Zhang,et al.  The Extent of the Preserved Feathers on the Four-Winged Dinosaur Microraptor gui under Ultraviolet Light , 2010, PloS one.