Flipper bone distribution reveals flexible trailing edge in underwater flying marine tetrapods

Abstract

Hydrofoil-shaped limbs (flipper-hydrofoils) have evolved independently several times in secondarily marine tetrapods and generally fall into two functional categories:(1) those that produce the majority of thrust during locomotion (propulsive flipperhydrofoils); (2) those used primarily to steer and resist destabilizing movements such as yaw, pitch, and roll (controller flipper-hydrofoils). The morphological differences between these two types have been poorly understood. Theoretical and experimental studies on engineered hydrofoils suggest that flapping hydrofoils with a flexible trailing edge are more efficient at producing thrust whereas hydrofoils used in steering and stabilization benefit from a more rigid one. To investigate whether the trailing edge is generally more flexible in propulsive flipper-hydrofoils, we compared the bone distribution along the chord in both flipper types. The propulsive flipperhydrofoil group consists of the forelimbs of Chelonioidea, Spheniscidae, and Otariidae. The controller flipper-hydrofoil group consists of the forelimbs of Cetacea. We quantified bone distribution from radiographs of species representing more than 50% of all extant genera for each clade. Our results show that the proportion of bone in both groups is similar along the leading edge (0-40% of the chord) but is significantly less along the trailing edge for propulsive flipper-hydrofoils (40-80% of the chord). Both flipper-hydrofoil types have little to no bony tissue along the very edge of the trailing edge (80-100% of the chord). This suggests a relatively flexible trailing edge for propulsive flipper-hydrofoils compared to controller flipper-hydrofoils in line with findings from prior studies. This study presents a morphological correlate for inferring flipper-hydrofoil function in extinct taxa and highlights the importance of a flexible trailing edge in the evolution of propulsive flipper-hydrofoils in marine tetrapods. K E Y W O R D S flexible trailing edge, flipper functional morphology, secondarily marine tetrapods

Wing Musculature Reconstruction in Extinct Flightless Auks (PinguinusandMancalla) Reveals Incomplete Convergence with Penguins (Spheniscidae) Due to Differing Ancestral States

“…Dorsoventrally flattened limb bones are seen in the wings of various wing-propelled diving birds (penguins, volant auks, diving petrels and some shearwaters; Kuroda 1954 ; Storer 1960 ; Livezey 1988 , 1989 ), and are prevalent in the specialized limbs of many different groups of secondarily aquatic tetrapods (e.g., Thewissen and Taylor 2007 ; Kelley and Pyenson 2015 ). When limbs are employed as flapping hydrofoils, dorsoventrally flattened limb bones increase hydrofoil rigidity, enabling the production of increased thrust and improving propulsive efficiency (although hydrofoil flexibility is another crucial factor underlying propulsive efficiency; DeBlois and Motani 2019 ). Therefore, flattened wing bones in Mancallinae strongly indicate that they were structurally suited to aquatic flight in a manner presumably homologous with that in crown-group Alcidae, and analogous to that in other extant wing-propelled diving birds (as well as other aquatic tetrapods).…”

“…As such, both the elongated crista deltopectoralis and attachment site for the ligg. propatagiale et limitans cubiti appear to represent modifications to increase the rigidity of the leading edge of the wings, which would increase thrust production in aquatic flight ( DeBlois and Motani 2019 ). It is evident that these modifications were acquired independently in Pinguinus and Mancallinae ( Fig.…”

“…1988 ; Louw 1992 ). The specialized, rigid wings of penguins are often referred to as flippers, analogous to the modified limbs of other secondarily aquatic tetrapods (e.g., Thewissen and Taylor 2007 ; Kelley and Pyenson 2015 ; DeBlois and Motani 2019 ).…”

Wing musculature reconstruction in extinct flightless auks (PinguinusandMancalla) reveals incomplete convergence with penguins (Spheniscidae) due to differing ancestral states

“…Several morphological attributes have been ascribed to wing-propelled diving: relatively small wings characterized by shortened bones and flight feathers which induce less drag and provide increased rigidity (Pennycuick 1987;Livezey 1988Livezey , 1989Louw 1992); dorsoventrally flattened wing bones with thick cortices apparently providing hydrodynamic efficiency and resistance to bending stress (Stettenheim 1959;Habib and Ruff 2008;Habib 2010; Clarke 2014); well-developed wing elevator muscles presumably involved in active upstroke of the wings in a dense, viscous medium (Stettenheim 1959;Schreiweis 1982;Bannasch 1986bBannasch , 1994Kovacs and Meyers, 2000); and reduced mobility of the elbow, wrist, and digital joints providing increased rigidity to the wings (specifically noted in penguins, but absent in volant auks; Bannasch 1986aBannasch , 1994Raikow et al 1988;Louw 1992). The specialized, rigid wings of penguins are often referred to as flippers, analogous to the 6 modified limbs of other secondarily aquatic tetrapods (e.g., Thewissen and Taylor 2007;Kelley and Pyenson 2015;DeBlois and Motani 2019). 101…”

Fingers zipped up or baby mittens? Two main tetrapod strategies to return to the sea

“…Although they are not closely related, all these groups share something in common: their ancestors had fingers. Previous studies have suggested that the limb-to-forefin (to better distinguish it from pectoral fins) transition in aquatic tetrapods occurred several times and followed diverse strategies [6][7][8][9][10][11]. However, did that morphological shift influence their anatomical integration?…”