An Intermediate in the evolution of superfast sonic muscles.

Hin-Kiu Mok,Pai-Ho Chiu,Kai-En Tsai,Michael L Fine,Eric Parmentier,Kuo-Hsun Chiu

doi:10.1186/1742-9994-8-31

Abstract

BackgroundIntermediate forms in the evolution of new adaptations such as transitions from water to land and the evolution of flight are often poorly understood. Similarly, the evolution of superfast sonic muscles in fishes, often considered the fastest muscles in vertebrates, has been a mystery because slow bladder movement does not generate sound. Slow muscles that stretch the swimbladder and then produce sound during recoil have recently been discovered in ophidiiform fishes. Here we describe the disturbance call (produced when fish are held) and sonic mechanism in an unrelated perciform pearl perch (Glaucosomatidae) that represents an intermediate condition in the evolution of super-fast sonic muscles.ResultsThe pearl perch disturbance call is a two-part sound produced by a fast sonic muscle that rapidly stretches the bladder and an antagonistic tendon-smooth muscle combination (part 1) causing the tendon and bladder to snap back (part 2) generating a higher-frequency and greater-amplitude pulse. The smooth muscle is confirmed by electron microscopy and protein analysis. To our knowledge smooth muscle attachment to a tendon is unknown in animals.ConclusionThe pearl perch, an advanced perciform teleost unrelated to ophidiiform fishes, uses a slow type mechanism to produce the major portion of the sound pulse during recoil, but the swimbladder is stretched by a fast muscle. Similarities between the two unrelated lineages, suggest independent and convergent evolution of sonic muscles and indicate intermediate forms in the evolution of superfast muscles.

Highlights

Intermediate forms in the evolution of new adaptations such as transitions from water to land and the evolution of flight are often poorly understood
In this study we investigate the anatomy of sound production including ultrastructure of sonic muscles and electrophoresis of muscle proteins, describe sound properties and relate them to sonic anatomy, and posit an evolutionary scheme that for the first time allows for intermediates in the evolution of super-fast sonic muscles
The disturbance call of the pearl perch is composed of two parts

Summary

Introduction

Intermediate forms in the evolution of new adaptations such as transitions from water to land and the evolution of flight are often poorly understood. Based on embryology [9] and parsimony, Fine and Ladich [10] speculated that extrinsic muscles preceded intrinsic ones because it would be simpler to move the insertion of an existing muscle to the swimbladder than to create a muscle de novo. In support of this idea, intrinsic sonic muscles and the sonic nerves in toadfish form in the occipital spinal cord, migrate and attach to the swimbladder [9]

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