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Functional Design of Cranial Muscles: Comparative and Physiological Studies in Pigs1

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Functional Design of Cranial Muscles: Comparative and Physiological Studies in Pigs1 AMER. ZOOL., 20:283-293 (1980) Functional Design of Cranial Muscles: Comparative and Physiological Studies in Pigs1 SUSAN W. HERRING Department of Oral Anatomy, University of Illinois at the Medical Center, Chicago, Illinois 60680 Downloaded from https://academic.oup.com/icb/article-abstract/20/1/283/1992384 by UNICAMP user on 16 September 2018 SYNOPSIS. The adaptive significance and evolutionary history of the internal architecture of the masseter muscle in suid artiodactyls are investigated. Hypotheses are developed on the basis of anatomical and physiological studies in the pig, Sits scrofa, and used to make predictions about the expected anatomy in the giant forest hog, Hylochoerus meinertzhageni and the warthog, Phacochoerus aethiopicus. The hypotheses are then tested by anatomical examination of these animals. In the pig, pinnation of the masseter serves to increase masticatory force and to partition the muscle into three semi-independent parts: vertical anterior fibers, which are used especially to close from wide gape; a central pinnate por- tion, which is used for all activities; and horizontal fibers covering the jaw joint, which are used especially for anterior translation of the condyle. In the giant forest hog and warthog the structure of the masseter is more uniform and the physiological cross section is larger than in the pig. These changes are interpreted as correlates of decreased emphasis on gape and increased emphasis on masticatory force in the African suids. In order to clarify the evolutionary sequence, masseteric architecture in the suids is compared with that of tayassuids and the hippopotamus. INTRODUCTION length-tension curve, and nonsynchro- In mammalian anatomy, truly parallel- nous contraction of fibers, all of which fibered muscles exist mainly in textbooks. could have major biomechanical effects. In fact, muscle fibers almost never run di- The problem is at its worst in the case of rectly from bony origin to bony insertion; multipinnate muscles, where even the sim- they normally attach at one or both ends ple procedure of determining a line of ac- to tendinous tissue and are at least slightly tion is probably not valid. Since the func- angled to the long axis of the muscle. tional significance of complex muscular Sometimes the pattern of internal tendons architecture is not understood, it is diffi- is amazingly complicated. The concern of cult to progress to the mechanical analysis; this paper is to examine the architecture a physiological analysis of the muscle must of complex muscles in terms of function, come first. and to use this information in arriving at Providing that the function of a trait an evolutionary explanation for species- such as complex muscle structure can be specific differences in pinnation pattern. clarified, it becomes possible to construct The analysis of musculoskeletal anatomy hypotheses about its selective value, i.e., its has been one of the most successful en- status as an adaptation. The most direct deavors of functional morphology, and way to test such hypotheses is by detailed has led to great insights into the evolution field observations that assess not only the of vertebrate feeding and locomotor ad- operation of the trait but also its value in aptations. The traditional muscle-bone differential reproduction, as exemplified analysis generally proceeds by determin- by Sherman's (1977) study on the evolu- ing muscular lines of action and moment tion of alarm calls in ground squirrels. A arms and using these in free-body dia- less direct test can be made by tampering grams. It is well-known to the practitioners with the trait involved and studying sur- of this art that the technique does not ad- vival, as has been done for rodent ears by dress some important points of muscle Webster and Webster (1971). Unfortu- function, such as fiber type, position along nately, the assessment of adaptive value of specific internal architecture in muscles re- sists either of these approaches, since the 1 From the Symposium on Morphology and Analysis operation of the architecture is not readily of Adaptation presented at the Annual Meeting of the observable in the wild nor modifiable by American Society of Zoologists, 27-30 December 1978, at Richmond, Virginia. surgical procedures. A third, even less di- 283 284 SUSAN W. HERRING trait in one animal can be used to generate predictions about the anatomy of the trait in another animal where the function is known. Of necessity, such investigations are conducted on taxa, rather than indi- viduals, which means that the trait's value Downloaded from https://academic.oup.com/icb/article-abstract/20/1/283/1992384 by UNICAMP user on 16 September 2018 in differential reproduction can never be measured. Nonetheless, correct predic- tions can be taken as evidence that the hy- pothesized adaptive role of the trait is in- deed something which has been selected for, although not necessarily related to taxonomic evolution in the animals. This latter method of testing hypotheses is what is usually called "comparative" and has been used implicitly for years by functional morphologists. An important consider- ation in the comparative method is the se- lection of animals to be used. Comparisons based on anatomical details cannot be made if the animals are wildly dissimilar, because it will be impossible to sort out all the factors influencing the trait. On the other hand, a certain amount of diversity is necessary for an adequate test of the pre- diction. In this paper I have employed a com- parative approach to the study of internal design of the masseter muscle in three H genera of pigs (Suidae, Artiodactyla). The following stages were involved: (1) ana- tomical description of the masseter of the pig, Sus scrofa; (2) physiological studies, mainly electromyography, to elucidate the function of the pig masseter; (3) formula- tion of a hypothesis of the adaptive signif- icance of the anatomy of the masseter; (4) predictions of masseteric anatomy in two other suids, the warthog Phacochoerus ae- thiopicus and the giant forest hog Hylochoe- rus meinertzhageni, based mainly on field descriptions of diet and jaw movements; and (5) testing these predictions by ana- tomical investigation of the masseters of these species. FIG. 1. Lateral views of the left masseters of Sus (S), STUDIES ON SUS SCROFA with parts of the skull shown for reference; Hylochoe- rus (H), and Phacochaerus (P). One-half actual size. The pig masseter is a large muscle which originates from the zygomatic arch and in- rect method for testing hypotheses of ad- serts on the lateral surface of the mandib- aptation remains, however, and this is by ular angle (Fig. 1). Most fasciculi arise and prediction. A hypothesis constructed by insert on a branching system of internal analysis of the anatomy and function of a tendons (Fig. 2S). Although the masseter CRANIAL MUSCLES IN PIGS 285 Downloaded from https://academic.oup.com/icb/article-abstract/20/1/283/1992384 by UNICAMP user on 16 September 2018 FIG. 2. Internal aponeuroses of the left masseter, oriented as in Figure 1. S—Stis (modified from Herring and Scapino, 1973); H—Hylochoerus; P—Phacochoerus. Aponeuroses of origin are shown in the left column, and the attachments to the zygomatic arch are filled in. Aponeuroses of insertion are shown in the right column, and the attachments to the mandibular angle are hatched. Origin and insertion systems interdigitate. is an indivisible mass with all fibers run- ing septa oriented in an oblique plane, but ning inferiorly, posteriorly and medially, these give way in the posterior part to there are several gradual changes along an broad parasagittal aponeuroses. Third, the anteroposterior axis. First, the muscle is anterior fasciculi are comparatively long thickest anteriorly and tapers posteriorly and vertical (with respect to the tooth row) to a thin edge. Second, the internal ten- but the posterior fasciculi are short and dons of the anterior part are interdigitat- near-horizontal (anteroposteriorly) (Fig. 286 SUSAN VV. HERRING Downloaded from https://academic.oup.com/icb/article-abstract/20/1/283/1992384 by UNICAMP user on 16 September 2018 FIG. 3. Lateral views of the left masseters of Sus (S), Hylochoenis (H) and Phacochoerus (P). Upper row— orientation of fasciculi in the sagittal plane, measured clockwise from the tooth row. Large dots: 70°-90°; medium dots: 50°-69°; small dots: 40°-49°; white: less than 40°. Lower row—Fasciculus length, expressed as a percentage of the longest fasciculus (about 40 mm in each case). Large dots: 80%-100%; medium dots: 55%- 75%; small dots: 40%-50%; white: 25%-30%. 3S). Sarcomere lengths also differ between The anatomical differences between an- anterior and posterior fasciculi (Herring el terior and posterior fasciculi have several al., 1979). With the jaws near occlusion, functional implications. Assuming that one sarcomeres near the anterior border of the or both jaw joints serve as the fulcrum for muscle are short, 2.4-2.5 /x,m, but from the jaw movement, the most anterior fibers middle of the muscle to the posterior bor- will have the longest moment arm. For a der, sarcomere length ranges between 2.9 given point of origin, verticality of fiber and 3.0 (im. With the jaws near maximum orientation is also associated with in- gape (25° angle between upper and lower creased moment arm. At the same time, toothrows), sarcomeres are longest ante- features that promote mechanical advan- riorly (3.7 /xm) and progressively shorter tage have a deleterious effect on the de- posteriorly, reaching 3.3 /urn at the poste- gree of stretch required when the jaw is rior border. The sarcomeres in the opened (Herring and Herring, 1974). posterosuperior corner (the fibers which Thus we see the bulk of masseteric volume cover the jaw joint) are even shorter, be- oriented relatively vertically in the anterior coming as small as 2.6 /i,m.
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