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. 2016 Jul 7:4:e2159.
doi: 10.7717/peerj.2159. eCollection 2016.

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

T Alexander Dececchi  1 , Hans C E Larsson  2 , Michael B Habib  3
Affiliations

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

T Alexander Dececchi et al. PeerJ. .

Abstract

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.

Keywords: Flap running; Flight; Flight stroke; Macroevolution; Maniraptora; Theropoda; WAIR.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Figure 1
Figure 1. Wing loading values in non-avian theropods.
Each open circle denotes the value per specimen for taxa with multiple specimens included in analysis. Note that only a minority of paravian specimens are below the lines denoting values pre WAIR quadruped crawling in Chukar (3 dph) and when fledging occurs (10 dph) as well as WAIR capable Brush Turkeys.
Figure 2
Figure 2. Evolution of WAIR performance.
Estimated evolutionary ranges of WAIR stages I and II (Dial, 2003; Heers & Dial, 2012; Heers, Dial & Tobalske, 2014) are mapped over a phylogeny of selected Maniraptoriformes. Upper lines are for 90° flap angles and lower lines for 50° flap angles. Flight-stroke specific characters are mapped onto the phylogeny: 1, forelimb integument; 2, pennaceous feathers on forelimb; 3, L-shaped scapulocoracoid; 4, laterally facing glenoid; 5, asymmetrical remigies; 6, alula; 7, incipient ligament-based shoulder stabilization; 8, dorsolaterally facing glenoid; 9, full ligament-based shoulder stabilization. The bottom coloured lines denote 50° flap angles and upper coloured lines 90°. Silhouettes from PhyloPic images by B. McFeeters, T.M. Keesey, M. Martynuick, and original.
Figure 3
Figure 3. Evolution of flight stroke enhancements to flap running (orange) and vertical leaping (blue) performance.
Estimated ranges are mapped over a phylogeny of selected Maniraptoriformes. Averages are presented when multiple specimens are available. Upper lines are for 90° flap angles and lower lines for 50° flap angles. Flight-stroke specific characters are mapped onto the phylogeny: 1, forelimb integument; 2, pennaceous feathers on forelimb; L-shaped scapulocoracoid; 4, laterally facing glenoid; 5, asymmetrical remigies; 6, alula; 7, incipient ligament-based shoulder stabilization; 8, dorsolaterally facing glenoid; 9, full ligament-based shoulder stabilization. The bottom coloured lines denote 50° flap angles and upper coloured lines 90°. Silhouettes from PhyloPic images by B. McFeeters, T.M. Keesey, M. Martynuick, and original.
Figure 4
Figure 4. 3D scatterplot of values for Chukars modeled for the first 70 days of growth.
2D projections of the values are shown on each axis-pair plane with grey circles. Age, pectoral limb muscle mass, wing loading, and WAIR performance data are from Heers & Dial (2015). Maximum WAIR angle was limited to 100°. Regressions were neither linear nor unimodal suggesting a complex interaction between musculoskeleletal and aerofoil ontogeny and performance. Mass (g) was estimated from age by the quadratic equation 5.730818 + 3.472647 × x + −0.011605 × x2 + 0.000661 × x3 (R2 = 0.9902); only ages less than 100 days were used. Percent pectoral mass was estimated from mass by the quadratic equation 0.858022 + 0.231592 × x −0.000658 × x2 × 5.9340−7 × x3 (R2 = 0.92). Wing loading was estimated from mass by the quadratic equation 1.692164 + −0.018717 × x + 8.756264−5 × x2 + −9.483335−8 × x3 (R2 = 0.69). Maximum WAIR angle was estimated from mass by the quadratic equation 38.119489 + 1.137820 × x + −0.007969 × x2 + 1.925223e − 05 × x3 (R2 = 0.9575).
Figure 5
Figure 5. Regression of measured wing loading versus maximum.
WAIR angle in Chukar chicks aged 3–15 day post hatching and estimates for selected non-avian theropods. Chuckar data are from Heers & Dial (2015). Large circles denote Chukar values with their age given as the number inside. Regression for Chuckar data is 100.17 − 20.824x, R2 = 0.848. Small circles denote estimated paravian theropods. Only specimens with wing loading values comparable to those seen in Chukars (< 2.0 g/cm2 = 196 N/m2) were included. Demarcation of quadrupedal crawling to WAIR at 65° was based on Jackson, Segre & Dial (2009). Non-avian theropods are: f1, Anchiornis huxleyi BMNHCPH828; f2, Anchiornis huxleyi LPM B00169; f3, Aurornis xui YFGP-T5198; f4, Changyuanraptor yangi HG B016; f5, Eosinopteryx brevipenna YFGP-T5197; f6, Microraptor gui BMNHC PH 881; f7, M. gui IVPP V 13352; f8, M. hanqingi LVH 0026 (light mass estimate); f9, M. hanqingi LVH 0026 (heavy mass estimate).
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