Evolution of upper jaw protrusion mechanisms in elasmobranchs

Evolution of Upper Jaw Protrusion Mechanisms in Elasmobranchs1

SYNOPSIS. Upper jaw protrusion is a prominent component of the feeding mechanism in most elasmobranchs and has received considerable attention over the years. In this paper, we review what is known of muscle activity during prey capture in elasmobranchs, particularly that of upper jaw protrusion, and evaluate the extent to which functional modifications have evolved through changes in anatomy or patterns of muscle activity. To date, motor activity during feeding has been documented in only four species of elasmobranchs, although they represent the three major elasmobranch groups: Galea (typical sharks); Squalea (dogfish sharks); and Batoidea (skates and rays). Our efforts show that while muscles involved in cranial elevation and lower jaw depression and elevation show a conserved pattern of motor activity and function across species, other muscles show a more variable history. Our observations of elasmobranch upper jaw protrusion mechanisms suggest a mosaic of character changes over the course of evolution that involve anatomical changes in all cases and modifications of muscle activation patterns in some cases. During the evolution of feeding mechanisms of elasmobranchs, there have been two structural changes incorporating a pre-existing motor pattern to yield an unmodified kinematic profile, the original preorbitalis and the descendent preorbitalis. One additional instance of structural modification is accompanied by an alteration in the motor pattern leading to a change in movement pattern, the levator palatoquadrati.

INTRODUCTION

Understanding how musculoskeletal systems have been modified in the course of animal history is a central theme in functional morphology. Behaviors of interest to functional morphologists, such as feeding, can often be characterized by a common kinematic pattern. Evolutionary changes in a selected kinematic pattern may occur by several pathways: as a result of anatomical alterations in the structural elements that perform them, by changes in the activation pattern of muscles that operate the skeletal system, or by changes at both of these levels (Lauder, 1991; Reilly and Lauder, 1992; Lauder and Shaffer, 1993; Smith, 1994b; Wainwright and Turingan, 1997; Friel and Wainwright, 1998, 1999; Wilga et al., 2000). Functional studies on the head of bony fishes and salamanders suggest that differences in feeding behavior most frequently result from modifications in the musculoskeletal anatomy and that the general sequence of motor activity tends to be phylogenetically conserved (Shaffer and Lauder, 1985a, b; Wainwright and Lauder, 1986; Sanderson, 1988; Wainwright, 1989; Wainwright et al., 1989; Westneat and Wainwright, 1989; Lauder and Shaffer, 1993; Friel and Wainwright, 1998; Smith, 1994a; Wilga et al., 2000). However, other studies have shown that details of the motor pattern, such as intensity and specific timing of muscle activity, may differ among species and that these changes can be a central component of behavioral evolution (Liem, 1979, 1989; Lauder, 1983; Friel and Wainwright, 1998, 1999). Given these generalities from research on bony fishes and some salamanders, we review recent studies on the evolution of feeding systems in Chondrichthyes, the sister group to all other living gnathostome vertebrates.

Upper jaw protrusion in elasmobranchs provides an ideal system for studying the evolution and function of a musculoskeletal system because it is an important element of feeding behavior in most species (Motta and Wilga, 2001) and because the anatomy of the jaw musculature has a rich history. Physical subdivision and structural alteration have been implicated in the evolution of the muscles involved in protruding the upper jaw in elasmobranchs (Daniel, 1934; Moss, 1972; Compagno, 1988; Shirai, 1996). Upper jaw protrusion in elasmobranchs occurs when the palatoquadrate cartilage moves anteroventrally away from the cranium as the jaws close on the prey. Numerous functions for protrusion of the upper jaw in sharks have been proposed: more efficient biting and manipulation of the prey; gouging of the upper jaw into large prey; a versatile yet hydrodynamic subterminal mouth; reorienting of the teeth for increased grasping ability; nearly simultaneous closure of the upper and lower jaws; greater speed of jaw closure (Springer, 1961; Alexander, 1967; Moss, 1972, 1977; Tricas and McCosker, 1984; Frazzetta and Prange, 1987; Frazzetta, 1994; Motta et al., 1997; Wilga and Motta, 1998a, b, 2000; Pretlow-Edmonds, 1999).

Although the mechanics of feeding and upper jaw protrusion have been studied in only a few elasmobranch species, several different mechanisms have been described. These differences have been attributed (Moss, 1972, 1977; Motta and Wilga, 1995, 1999; Wilga and Motta, 1998a, b, 2000) to differences among taxa in cranial development and myology (Vetter, 1874, 1878; Tiesing, 1895; Marion, 1905; Luther, 1909; Allis 1917, 1923; Daniel, 1934; Edgeworth, 1935; Lightoller, 1939; Marinelli and Strenger, 1959; Nobiling, 1977; Compagno, 1988) and have had a profound effect on the mechanics of jaw protrusion in sharks. In this paper, we review what is known of muscle activity during feeding, particularly that associated with upper jaw protrusion, and evaluate the extent to which evolutionary modifications have come about through changes in anatomy or patterns of muscle activation.