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Convergent evolution in mechanical design of lamnid sharks and tunas

Abstract

The evolution of ‘thunniform’ body shapes in several different groups of vertebrates, including whales, ichthyosaurs1 and several species of large pelagic fishes2 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.

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Figure 1: Features of thunniform body shape and patterns of lateral undulation during steady swimming.
Figure 2: Simultaneous recordings of muscle strain (segment length change/mean length) of red (red trace) and adjacent white (grey trace) muscle during passive simulated swimming movements (a) and active steady swimming (0.5 l s-1) (b) in the mako shark.
Figure 3: Collagenous architecture of myosepta of I. oxyrinchus.

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Acknowledgements

We thank A. Biewener, J. Gosline, J. B. Graham, S. Vogel and N. Holland for discussion and reviews. Funding was provided by NSF and UC Regents.

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Correspondence to Jeanine M. Donley.

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Supplementary information

Supplementary Figure 1

Three-dimensional reconstruction of shape and tendinous architecture of myosepta (MS) and horizontal septum (HS) of gnathostome ancestor (A-C) and lateral views of selected MS of the shortfin mako (Isurus oxyrinchus) (D, E) showing differences from general gnathostome condition. (PDF 640 kb)

Supplementary Movie 1

This video clip shows a mako swimming in the swim tunnel. The dorsal view illustrates the degree of lateral displacement along the body during steady swimming. (MOV 1272 kb)

Supplementary Figure Legends

Figure legends for supplementary figures one and two (movie) and a list of cited references that accompany the legends. (DOC 23 kb)

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Donley, J., Sepulveda, C., Konstantinidis, P. et al. Convergent evolution in mechanical design of lamnid sharks and tunas. Nature 429, 61–65 (2004). https://doi.org/10.1038/nature02435

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