Caudal Fin Locomotion in Ray-finned Fishes: Historical and Functional Analyses

Abstract

SYNOPSIS. Over the last 20 years, considerable progress has been made in quantifying the movement of the body during locomotion by aquatic vertebrates, and in defining the role of axial musculature in producing these kinematic patterns. Relatively little is known, however, about how specific internal structural features of the axial system in fishes affect body kinematics, and how such structural and functional features have changed during evolution. The major theme of this paper is that historical, phylogenetic patterns in the axial musculoskeletal system need to be integrated with experimental and functional data in order to understand the design of the locomotor apparatus in vertebrates. To illustrate this proposition, the evolution of the tail in ray-finned fishes is presented as a case study in phylogenetic and functional analysis of the vertebrate axial musculoskeletal system. Traditionally, the evolution of the tail in ray-finned fishes has been viewed as a transformation from a primitively heterocercal (functionally asymmetrical) tail to a homocercal tail in which the axis of rotation during locomotion was vertical, generating a symmetrical thrust. Both phylogenetic and functional approaches are used to examine this hypothesis. Major osteological and myological features of the tail in ray-finned fishes are mapped onto a phylogeny of ray-finned fishes to discern historical sequences of morphological change in the axial musculoskeletal system. A key event in locomotor evolution was the origin of the hypochordal longitudinalis muscle, the only intrinsic caudal muscle with a line of action at an appreciable angle to the body axis. This muscle originated prior to the origin of a caudal skeleton bearing both hypaxial and epaxial fin ray supports. The hypochordal muscle is proposed to be a key component of the axial musculoskeletal system that allows most fishes to modulate caudal function and decouples external morphological symmetry from functional symmetry. Experimental data (strain gauge recordings from tail bones, and electromyographic recordings from intrinsic and extrinsic caudal muscles) corroborate this interpretation and suggest that functional symmetry in the tail of ray-finned fishes is not predictable from skeletal morphology alone, but depends on the activity of the hypochordal longitudinalis muscle and on locomotor mode. The homocercal teleost tail may thus function asymmetrically.