Integrative and Comparative Biology Integrative and Comparative Biology, Pp

Integrative and Comparative Biology Integrative and Comparative Biology, pp. 1–16 doi:10.1093/icb/icab021 Society for Integrative and Comparative Biology SYMPOSIUM Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021 The Role of the Tail or Lack Thereof in the Evolution of Tetrapod Aquatic Propulsion Frank E. Fish,1,* Natalia Rybczynski,† George V. Lauder‡ and Christina M. Duff* *Department of Biology, West Chester University, West Chester, PA 19383, USA; †Department of Palaeobiology, Canadian Museum of Nature, Ottawa, ON, Canada K1P 6P4; ‡Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138, USA From the symposium “An evolutionary tail: Evo-Devo, structure, and function of post-anal appendages” presented at the virtual annual meeting of the Society for Integrative and Comparative Biology, January 3–7, 2020. 1E-mail: [email protected] Synopsis Secondary aquatic vertebrates exhibit a diversity of swimming modes that use paired limbs and/or the tail. Various secondarily aquatic tetrapod clades, including amphibians, reptiles, and mammals use transverse undulations or oscillations of the tail for swimming. These movements have often been classified according to a kinematic gradient that was established for fishes but may not be appropriate to describe the swimming motions of tetrapods. To understand the evolution of movements and design of the tail in aquatic tetrapods, we categorize the types of tails used for swimming and examine swimming kinematics and hydrodynamics. From a foundation of a narrow, elongate ancestral tail, the tails used for swimming by aquatic tetrapods are classified as tapered, keeled, paddle, and lunate. Tail undulations are associated with tapered, keeled, and paddle tails for a diversity of taxa. Propulsive undulatory waves move down the tail with increasing amplitude toward the tail tip, while moving posteriorly at a velocity faster than the anterior motion of the body indicating that the tail is used for thrust generation. Aquatic propulsion is associated with the transfer of momentum to the water from the swimming movements of the tail, particularly at the trailing edge. The addition of transverse extensions and flattening of the tail increases the mass of water accelerated posteriorly and affects vorticity shed into the wake for more aquatically adapted animals. Digital Particle Image Velocimetry reveals that the differences were exhibited in the vortex wake between the morphological and kinematic extremes of the alligator with a tapering undulating tail and the dolphin with oscillating wing-like flukes that generate thrust. In addition to exploring the relationship between the shape of undulating tails and the swimming performance across aquatic tetrapods, the role of tail reduction or loss of a tail in aquatic-tetrapod swimming was also explored. For aquatic tetrapods, the reduction would have been due to factors including locomotor and defensive specializations and phylogenetic and physiological constraints. Possession of a thrust-generating tail for swimming, or lack thereof, guided various lineages of secondarily aquatic vertebrates into different evolutionary trajectories for effective aquatic propulsion (i.e., speed, efficiency, and acceleration). Introduction 1999), anuran tadpoles (Wassersug and Hoff 1985; Tails are ubiquitous as propulsive organs among ver- Liu et al. 1996), urodele amphibians (Ashley-Ross tebrates for swimming. Animals using the tail to swim and Bechtel 2004), snakes (Jayne 1985; Brischoux are generally classified as undulatory. Undulatory and Shine 2011), lizards (Ringma and Salisbury swimmers pass a series of waves that can be generated 2014), crocodilians (Manter 1940; Fish 1984), dino- in the body and move posteriorly down the tail. saurs (Ibrahim et al. 2020), mosasaurs (Lindgren et al. Undulatory swimming vertebrates include bony and 2010), ichthyosaurs (Riess 1986; Motani et al. 1996; cartilaginous fishes (Lindsey 1978; Sfakiotakis et al. Motani 2000; Buchholtz 2001), various semiaquatic ß The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved. For permissions please email: [email protected]. 2 F. E. Fish et al. mammals (Howell 1930), sirenians (Hartman 1979; quintessential example of evolutionary convergence Kojeszewski and Fish 2007), and cetaceans (Fish displayed by lamnid sharks, ichthyosaurs of the 1998a). Thunnosauria, and oceanic dolphins of the Downloaded from https://academic.oup.com/icb/advance-article/doi/10.1093/icb/icab021/6244185 by Harvard College Library, Cabot Science Library user on 10 May 2021 One of the definitive chordate characteristics is the Delphinidae (Howell 1930; Hildebrand 1995; post-anal tail. The legacy of this caudal appendage Motani 1999; Liem et al. 2001; Kardong 2019; from the early chordates is its use as a propulsive Moon 2019; Fish submitted for publication). All apparatus in many vertebrate clades to move these groups independently developed a high- through the aquatic medium. Swimming by basal performance wing-like, lunate caudal fin. Even semi- chordates originated with serial activation of myo- aquatic mammals (e.g., Castor, Castorocauda, meres to produce a wriggling movement of the body Ornithorhynchus, and Pteronura) display parallelism and tail for swimming (Webb 1973; Stokes 1997; in the flattening of their tails (Howell 1937; Duff and Lacalli 2012). From the basal chordates, movement Fish 2002; Ji et al. 2006). Between terrestrial forms through water by the majority of fishes used body making limited forays into water and these highly and caudal fin (BCF) swimming (Breder 1926; Webb derived aquatic morphologies are a diversity of tail 1975, 1982, 1984; Lindsey 1978; Sfakiotakis et al. designs with varying degrees of performance in re- 1999). Given the importance of speed, long- gard to thrust production and propulsive efficiency. distance swimming, acceleration, and efficiency, the This article examines the evolution of the tail as elaboration of a tail including the development of an aquatic propulsive structure in tetrapods. the caudal fin allowed greater propulsive diversity Although not a comprehensive review, the tails ex- in early vertebrates (Webb 1980). amined are drawn from vertebrate groups that were The majority of research on swimming move- historically terrestrial but became secondarily ments associated with a propulsive tail has focused aquatic. Gutmann (1994) provided a series of illus- on the undulatory-oscillatory gradient displayed by trations indicating the transition of body forms and fishes (see reviews by Breder 1926; Webb 1975, 1978; propulsive modes for secondarily aquatic vertebrates, Lindsey 1978; Blake 1983; Videler 1993; Sfakiotakis but without grounding these alterations in modern et al. 1999). However, the evolution of propulsive hydrodynamic theory. Here, we categorize and ad- tails has occurred independently multiple times in dress the changes in tail morphology in the context a variety of vertebrate clades that went through a of thrust production and propulsive efficiency. The terrestrial phase. interaction of the physical properties of the aqueous In one of the “Great Transformations” in evolu- medium with the hydrodynamics of propulsion most tion, vertebrates moved from an obligate aquatic ex- likely placed high selective pressures on animals istence to terrestrial habits (Dial et al. 2015). The tail attempting to move through the water with speed took on a non-propulsive role with the development and high-energy economy. In addition, we consider of legged locomotion on land (Inger 1962), although lineages with reduced tails and the relationship be- the tail served as the origin for some muscles asso- tween tail reduction/loss and the evolution of limb- ciated with the hind legs. This decreased reliance on based mechanisms for aquatic propulsion. the tail as a propulsive surface by terrestrial species meant that as multiple linages of vertebrates returned Reinventing the water wheel to the water a finned tail would have had to be reinvented. It is the secondary evolution of aquatic Undulatory categories habits by tetrapods that fostered the development of Undulatory propulsive motions are cyclical with tails similar to the earlier fish evolutionary lineages. symmetrically repeating flexion of the body and With the trends to larger body sizes and increased tail, generating a traveling wave during steady swim- need for speed and efficiency in the aquatic realm, ming. In fishes, the traveling wave is generated by the evolution of propulsive tails in secondarily sequential activation of the myomeres that are ar- aquatic tetrapods has culminated in the development ranged serially along the trunk and caudal vertebrae of high performance caudally derived propulsors modified from the original chordate swimming (Flower 1883; Lighthill 1969; Webb and De mechanism. Undulatory swimming has been best de- Buffrenil 1990; Fish 1996). Dealing with the same scribed for BCF swimming in fishes along a kine- physical hurdles and strong selection criteria im- matic gradient that is categorized according to posed by the aquatic environment, secondarily wavelength and proportion of the posterior body aquatic tetrapods converged on similar solutions generating the traveling wave. Propulsive movements with fishes for effective swimming. This “aquatic of wavelengths shorter than an

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