The evolution of 'thunniform' body shapes in several different groups of vertebrates, including whales, ichthyosaurs and several species of large pelagic fishes supports the view that physical and hydromechanical demands provided important selection pressures to optimize body design for locomotion during vertebrate evolution. Recognition of morphological similarities between lamnid sharks (the most well known being the great white and the mako) and tunas has led to a general expectation that they also have converged in their functional design; however, no quantitative data exist on the mechanical performance of the locomotor system in lamnid sharks. Here we examine the swimming kinematics, in vivo muscle dynamics and functional morphology of the force-transmission system in a lamnid shark, and show that the evolutionary convergence in body shape and mechanical design between the distantly related lamnids and tunas is much more than skin deep; it extends to the depths of the myotendinous architecture and the mechanical basis for propulsive movements. We demonstrate that not only have lamnids and tunas converged to a much greater extent than previously known, but they have also developed morphological and functional adaptations in their locomotor systems that are unlike virtually all other fishes.

One of the most conspicuous features of the locomotor muscle in fish is the distinct segregation of two functionally different fiber types: red oxidative and white glycolytic. In most bony and cartilaginous fishes, the red muscle comprises a thin subcutaneous wedge or sheet of muscle that is located near the lateral line while the white muscle comprises the bulk of the body cross-section. Some of the earliest research on the function of muscle in swimming fish focused on identifying the role of the red and white fibers in various swimming behaviors in sharks. Using electromyography (EMG), Bone (1966) showed that in dogfish shark the red muscle fibers were active during slow, steady swimming whereas white fibers were active when high burst speeds were required. Given differences in mitochondrial content, fat and glycogen content, patterns of innervation, and EMG activity at various swimming speeds between the two fiber types, Bone (1966) concluded that the red and white muscle in dogfish represent two distinct motor systems which operate independently. Following this work, the focus of studies investigating the function of fish muscle during swimming shifted from sharks to bony fishes. Indeed, the same pattern of differential muscle function between red and white fibers was shown in teleosts. Only red muscle was found to be active at slow swimming speeds, whereas white muscle was shown to be active only at burst speeds (Rayner and Keenan, 1967), or at progressive levels of recruitment starting at the upper range of sustainable swimming speeds (Greer-Walker, 1970; Johnston and Goldspink, 1973a,b;Johnston et al., 1977;Bone et al., 1978;Hochachka et al., 1978).In addition to examining the roles of the two major muscle fiber types as a function of swimming speed, numerous studies have investigated the timing of red muscle activation at different positions along the body during steady swimming. When superficial red muscle is active it contracts to produce local bending of the body, and the wave of lateral motion that generates thrust is the summation of the sequential muscle contractions along the body. Common features of activation patterns during steady swimming among several teleost species are that the wave of red muscle activation travels (1) down the body in a rostrocaudal direction (Grillner and Kashin, 1976;Williams et al., 1989;He et al., 1990;van Leeuwen et al., 1990;Jayne and Lauder, 1993, 1995b;Gillis, 1998;Knower et al., 1999;Shadwick et al., 1999) and (2) faster than the propulsive wave of lateral displacement (Grillner and Kashin, 1976;Wardle et al., 1995;Katz and Shadwick, 1998

Effects of temperature on muscle contraction and powering movement are profound, outwardly obvious, and of great consequence to survival. To cope with the effects of environmental temperature fluctuations, endothermic birds and mammals maintain a relatively warm and constant body temperature, whereas most fishes and other vertebrates are ectothermic and conform to their thermal niche, compromising performance at colder temperatures. However, within the fishes the tunas and lamnid sharks deviate from the ectothermic strategy, maintaining elevated core body temperatures that presumably confer physiological advantages for their roles as fast and continuously swimming pelagic predators. Here we show that the salmon shark, a lamnid inhabiting cold, north Pacific waters, has become so specialized for endothermy that its red, aerobic, locomotor muscles, which power continuous swimming, seem mammal-like, functioning only within a markedly elevated temperature range (20-30 degrees C). These muscles are ineffectual if exposed to the cool water temperatures, and when warmed even 10 degrees C above ambient they still produce only 25-50% of the power produced at 26 degrees C. In contrast, the white muscles, powering burst swimming, do not show such a marked thermal dependence and work well across a wide range of temperatures.

In contrast to all other sharks, lamnid sharks perform a specialized fast and continuous "thunniform" type of locomotion, more similar to that of tunas than to any other known shark or bony fish. Within sharks, it has evolved from a subcarangiform mode. Experimental data show that the two swimming modes in sharks differ remarkably in kinematic patterns as well as in muscle activation patterns, but the morphology of the underlying musculotendinous system (red muscles and myosepta) that drives continuous locomotion remains largely unknown. The goal of this study was to identify differences in the musculotendinous system of the two swimming types and to evaluate these differences in an evolutionary context. Three subcarangiform sharks (the velvet belly lantern shark, Etmopterus spinax, the smallspotted catshark, Scyliorhinus canicula, and the blackmouth catshark, Galeus melanostomus) from the two major clades (two galeans, one squalean) and one lamnid shark, the shortfin mako, Isurus oxyrhinchus, were compared with respect to 1) the 3D shape of myomeres and myosepta of different body positions; 2) the tendinous architecture (collagenous fiber pathways) of myosepta from different body positions; and 3) the association of red muscles with myoseptal tendons. Results show that the three subcarangiform sharks are morphologically similar but differ remarkably from the lamnid condition. Moreover, the "subcarangiform" morphology is similar to the condition known from teleostomes. Thus, major features of the "subcarangiform" condition in sharks have evolved early in gnathostome history: Myosepta have one main anterior-pointing cone and two posterior-pointing cones that project into the musculature. Within a single myoseptum cones are connected by longitudinally oriented tendons (the hypaxial and epaxial lateral and myorhabdoid tendons). Mediolaterally oriented tendons (epineural and epipleural tendons; mediolateral fibers) connect vertebral axis and skin. An individual lateral tendon spans only a short distance along the body (a fraction between 0.05 and 0.075 of total length, L, of the shark). This span is similar in all tendons along the body. Red muscles insert into the midregion of the lateral tendons. The shortfin mako differs substantially from this condition in several respects: Red muscles are internalized and separated from white muscles by a sheath of lubricative connective tissue. They insert into the anterior part of the hypaxial lateral tendon. Rostrocaudally, this tendon becomes very distinct and its span increases threefold (0.06L anteriorly to 0.19L posteriorly). Mediolateral fibers do not form distinct epineural/epipleural tendons in the mako. Since our morphological findings are in good accordance with experimental data it seems likely that the thunniform swimming mode has evolved along with the described morphological specializations.