The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedents

Background: Powered flight is implicated as a major driver for the success of birds. Here we examine the effectiveness of three hypothesized pathways for the evolution of the flight stroke, the forelimb motion that powers aerial locomotion, in a terrestrial setting across a range of stem and basal a...

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Main Authors: T. Alexander Dececchi, Hans C.E. Larsson, Michael B. Habib
Format: Article
Language:English
Published: PeerJ Inc. 2016-07-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/2159.pdf
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author T. Alexander Dececchi
Hans C.E. Larsson
Michael B. Habib
author_facet T. Alexander Dececchi
Hans C.E. Larsson
Michael B. Habib
author_sort T. Alexander Dececchi
collection DOAJ
description Background: Powered flight is implicated as a major driver for the success of birds. Here we examine the effectiveness of three hypothesized pathways for the evolution of the flight stroke, the forelimb motion that powers aerial locomotion, in a terrestrial setting across a range of stem and basal avians: flap running, Wing Assisted Incline Running (WAIR), and wing-assisted leaping. Methods: Using biomechanical mathematical models based on known aerodynamic principals and in vivo experiments and ground truthed using extant avians we seek to test if an incipient flight stroke may have contributed sufficient force to permit flap running, WAIR, or leaping takeoff along the phylogenetic lineage from Coelurosauria to birds. Results: None of these behaviours were found to meet the biomechanical threshold requirements before Paraves. Neither was there a continuous trend of refinement for any of these biomechanical performances across phylogeny nor a signal of universal applicability near the origin of birds. None of these flap-based locomotory models appear to have been a major influence on pre-flight character acquisition such as pennaceous feathers, suggesting non-locomotory behaviours, and less stringent locomotory behaviours such as balancing and braking, played a role in the evolution of the maniraptoran wing and nascent flight stroke. We find no support for widespread prevalence of WAIR in non-avian theropods, but can’t reject its presence in large winged, small-bodied taxa like Microraptor and Archaeopteryx. Discussion: Using our first principles approach we find that “near flight” locomotor behaviors are most sensitive to wing area, and that non-locomotory related selection regimes likely expanded wing area well before WAIR and other such behaviors were possible in derived avians. These results suggest that investigations of the drivers for wing expansion and feather elongation in theropods need not be intrinsically linked to locomotory adaptations, and this separation is critical for our understanding of the origin of powered flight and avian evolution.
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spelling doaj.art-1aaf049b136c410eb0342723bf048a9c2023-12-03T10:57:38ZengPeerJ Inc.PeerJ2167-83592016-07-014e215910.7717/peerj.2159The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedentsT. Alexander Dececchi0Hans C.E. Larsson1Michael B. Habib2Department of Geological Sciences, Queens University, Kingston, Ontario, CanadaRedpath Museum, McGill University, Montreal, Quebec, CanadaKeck School of Medicine of USC, Department of Cell and Neurobiology, University of Southern California, Los Angeles, California, United StatesBackground: Powered flight is implicated as a major driver for the success of birds. Here we examine the effectiveness of three hypothesized pathways for the evolution of the flight stroke, the forelimb motion that powers aerial locomotion, in a terrestrial setting across a range of stem and basal avians: flap running, Wing Assisted Incline Running (WAIR), and wing-assisted leaping. Methods: Using biomechanical mathematical models based on known aerodynamic principals and in vivo experiments and ground truthed using extant avians we seek to test if an incipient flight stroke may have contributed sufficient force to permit flap running, WAIR, or leaping takeoff along the phylogenetic lineage from Coelurosauria to birds. Results: None of these behaviours were found to meet the biomechanical threshold requirements before Paraves. Neither was there a continuous trend of refinement for any of these biomechanical performances across phylogeny nor a signal of universal applicability near the origin of birds. None of these flap-based locomotory models appear to have been a major influence on pre-flight character acquisition such as pennaceous feathers, suggesting non-locomotory behaviours, and less stringent locomotory behaviours such as balancing and braking, played a role in the evolution of the maniraptoran wing and nascent flight stroke. We find no support for widespread prevalence of WAIR in non-avian theropods, but can’t reject its presence in large winged, small-bodied taxa like Microraptor and Archaeopteryx. Discussion: Using our first principles approach we find that “near flight” locomotor behaviors are most sensitive to wing area, and that non-locomotory related selection regimes likely expanded wing area well before WAIR and other such behaviors were possible in derived avians. These results suggest that investigations of the drivers for wing expansion and feather elongation in theropods need not be intrinsically linked to locomotory adaptations, and this separation is critical for our understanding of the origin of powered flight and avian evolution.https://peerj.com/articles/2159.pdfFlightWAIRManiraptoraMacroevolutionTheropodaFlap running
spellingShingle T. Alexander Dececchi
Hans C.E. Larsson
Michael B. Habib
The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedents
PeerJ
Flight
WAIR
Maniraptora
Macroevolution
Theropoda
Flap running
title The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedents
title_full The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedents
title_fullStr The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedents
title_full_unstemmed The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedents
title_short The wings before the bird: an evaluation of flapping-based locomotory hypotheses in bird antecedents
title_sort wings before the bird an evaluation of flapping based locomotory hypotheses in bird antecedents
topic Flight
WAIR
Maniraptora
Macroevolution
Theropoda
Flap running
url https://peerj.com/articles/2159.pdf
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