12.1 Introduction

In Chapter 11, we explored the microscopic structure of muscle as well as how muscles function at the cellular level to produce tension. In this chapter, we will zoom out and begin considering muscle at the gross anatomical level. We will explore muscle organization, muscle shapes, and muscle naming conventions. After establishing a foundation of gross anatomical muscle structure and function, we will explore muscle evolution and the diversity of the major muscle groups among vertebrates.

12.2 Hierarchical Anatomy of Muscle

As you know from the previous chapter, skeletal muscle is composed of elongated cells known as muscle fibers or myocytes. But each of these myocytes actually contributes to the formation of a larger organ structure called a muscle, and this muscle has a hierarchical organization pattern.

Each muscle fiber is surrounded by a thin layer of extracellular matrix called endomysium. Individual muscle cells and their endomysium are bundled together, and these bundles of fibers form structures called fascicles. Fascicles are bound by a layer of connective tissue called perimysium. These fascicles and their surrounding perimysium are grouped together into a discrete unit called a muscle, which is enclosed by yet another layer of connective tissue called epimysium. The fibrous connective tissue of a muscle then forms a tendon, which anchors the muscle to the bone and/or the structure that the muscle moves (Figure 12.1).

This multilayered, bundled arrangement ensures that a muscle pulls as a unit, even if some of the fibers that make up the muscle are weaker than others. As a result of the way muscles are organized, skeletal muscles have distinct attachments to skeletal elements or connective tissue septa. These attachments are called tendons, and they basically consist of an extension of the muscle’s connective tissue, as described above, that penetrates the periosteum of the bone. Tendons can take a variety of forms (Figure 12.2):

1. Sometimes tendons are really inconspicuous, so much so that it simply looks as if the muscle grows directly out of bone (e.g., gluteus medius tendon; Figure 12.2A).
2. Other times tendons form prominent cords. The Achilles tendon above our heel is an excellent example of this type of tendon (Figure 12.2B).
3. And still other times tendons form broad sheets called aponeuroses. An example of an aponeurosis can be observed on the abdomen (Figure 12.2C).

When we describe the attachments of a muscle, we describe them in reference to two ends (Figure 12.3): There’s (1) the end that remains fixed (the origin), which is typically more proximal, and (2) the end that moves when the muscle contracts (the insertion), typically more distal.

In addition to muscle fibers and connective tissue, we also find blood vessels in muscle, which supply muscle fibers with nutrients and remove metabolic waste. Nerves are also present in muscle, as these are critical structures for coordinating muscle contraction (see neuromuscular junction, Figure 11.8).

12.3 Muscle Shapes

Skeletal muscles vary quite a bit in their structures, and this is related to the pattern of arrangement of the fascicles, which affect the appearance and function of the muscles. We find muscles in the following shapes (Figure 12.4):

1. Parallel: evenly spaced fascicles that attach to a tendon of similar width to the muscle. Parallel muscles have a “straplike” appearance (e.g., sartorius muscle of the thigh).
2. Convergent: broad and uniformly taper into a single tendon. Convergent muscles tend to be triangular in shape (e.g., pectoralis major of the chest).
3. Pennate: fibers and fascicles attach to the tendon at an angle; there are three forms:
   1. Unipennate: fascicles angle out on one side only (e.g., flexor pollicis longus of the forearm)
   2. Bipennate: fascicles angle out from both sides (e.g., rectus femoris of the thigh)
   3. Multipennate: composed of several areas where fascicles angle out from connective tissue separators (e.g., deltoid of the shoulder)
4. Circular: encircle a structure. These muscles can be found in areas such as around the eyes and mouth.
5. Spiral: characterized by having a twisted appearance; these often wrap around a bone (e.g., supinator muscle of the forearm).
6. Fusiform: thick in the middle and taper at either end (e.g., biceps brachii muscle of the upper arm).

12.4 Muscle Names

Muscle names can stem from a number of origins, but oftentimes these names are really helpful in informing us about the muscle. Muscle names often include size descriptors such as major (big), minor (small), longus (long), or brevis (short), among others. Similarly, muscle names may also include location information through the use of directional terms such as superior, medial, profundus (deep), capitis (head), and so on. They may also include regional terms, like pectoral or oculi, indicating where in the body the muscle may be found. In some cases, muscle names indicate the structures to which they attach. For example, the sternocleidomastoid muscle attaches to the sternum (“sterno”), the clavicle (“cleido”), and the mastoid process of the temporal bone (“mastoid”). Muscle names can also give clues about a given muscle’s function, such as flexing or extending a limb or elevating or adducting a body part (e.g., flexor pollicis longus flexes the thumb).

12.5 Muscle Evolution and Diversity

Now that we’ve established a foundational understanding of muscle development, form, and function, we’re ready to begin examining muscle evolution and diversity. In an earlier chapter we introduced the distinction between visceral and somatic portions of the body. You’ll recall that visceral refers to tissue associated with the gut tube, and somatic refers to everything else. And we can use this same distinction to categorize the muscles of the vertebrate body.

Almost all muscles are derived from mesenchymal mesoderm, but the specific kind of mesoderm differs depending on whether you’re dealing with visceral versus somatic muscles. Visceral muscles—including those in the walls of the gut tube, blood vessels, and heart—are derived from the splanchnic layer of the lateral plate mesoderm. In contrast, somatic muscles—which include the remaining muscles of the body axis, appendages, and head—develop from the somites and somatic layer of the lateral plate mesoderm (see Figure 4.10).

Because the structure of the digestive tract (gut tube) and cardiovascular system (blood vessels and heart) (Chapter 15) will be discussed in detail in later chapters, the rest of this chapter will focus on the six major groups of somatic muscles (and—impressively, four of the six are all located in the head and innervated by cranial nerves). As we introduce these muscle groups below, I will include notes on their innervation (particularly for the head muscles). But—if the nervous system (Chapter 19) is covered elsewhere in this book, why take the time to highlight the specific cranial nerves associated with the head muscles now? Why is this important? Well, cranial nerve innervation patterns are highly conserved across vertebrates, which means that the specific muscles of vertebrates that are derived from these groups will continue to follow these patterns of innervation!

The six major muscle groups of the vertebrate body (Figure 12.5) are

1. Extrinsic ocular muscles
2. Epibranchial muscles
3. Hypobranchial muscles
4. Branchiomeric muscles
5. Axial muscles
6. Appendicular muscles

Extrinsic Ocular Muscles

Let’s begin with a look at the extrinsic ocular muscles. These muscles are the muscles that move the eyeball (note the term ocular, referring to the eye). The extrinsic oculars are derived from the first three somitomeres (precursors to vertebrate somites) of the head as well as somitomere 5, and they are supplied by the ventral root nerve of each of the first three head segments. The ventral root nerves for the first three somitomeres are the oculomotor (CN III) for segment 1, trochlear (CN IV) for segment 2, and abducens (CN VI) for segment 3 (these cranial nerves will be covered in greater detail in the chapters on the nervous system and senses). The extrinsic ocular muscles are incredibly conserved throughout the diversification of vertebrates—so the six muscles that move the eye in a shark are essentially the same six muscles that move your own eye (Figure 12.6)!

Epibranchial Muscles

The next group of muscles is the epibranchial muscles, which are positioned dorsal to the gill pouches. These muscles are derived from the dorsal parts of the four head somites and are supplied by CN X (vagus nerve). Epibranchial muscles are typically fairly reduced; however, in some fishes and amphibians they contribute to the elevation of the braincase and upper jaw during feeding.

Hypobranchial Muscles

The third group of muscles sits ventral to the gill pouches and are called the hypobranchial muscles. The hypobranchials form from myoblasts that migrate ventrally from the somites and are supplied by CN XII (hypoglossial nerve). The hypobranchial muscles are a little more elaborated compared to the epibranchials. These muscles span from the shoulder girdle and sternum to the first and second gill arches and help depress the jaw and open the mouth in fishes. Often, the hypobranchials are classified based on their position relative to the hyoid:

1. Prehyoid muscles: muscles anterior to the hyoid arch
2. Posthyoid muscles: muscles posterior to the hyoid arch

The hypobranchial muscles become far more complex in tetrapods, because once tetrapods move onto land, their food isn’t supported by the environment, and suction feeding is not possible (Table 12.1). As a result, food must be manipulated by muscles within the mouth to facilitate oral processing and transfer to the esophagus to continue through the digestive system (Chapter 13). One of these tetrapod hypobranchial muscles is a newly evolved structure: the muscular tongue. The geniohyoideus and genioglossus also contribute to moving the tongue within the oral cavity in amphibians. The amniotes further subdivide the hypobranchial muscles, adding hyoglossus, styloglossus, and lingualis to the tongue musculature. In fact, the lingualis contributes the bulk of the tongue structure in mammals. In addition, we also find in mammals the sternohyoideus, sternothyroideus, thyrohyoideus, and omohyoid muscles, which contribute to the complex actions of the jaws and throat during swallowing.

Table 12.1—Hypobranchial muscle differentiation across select vertebrate taxa

Branchiomeric Muscles

The fourth group of head muscles are the actual muscles of the gill pouches themselves: the branchiomeric muscles. The muscles associated with the first two gill arches are specifically referred to as the mandibular muscles and hyoid muscles, respectively; the muscles of the remaining gill arches are simply referred to as the branchiomeric muscles. The mandibular muscles develop from somitomere 4 and are supplied by CN V (trigeminal nerve), whereas the hyoid muscles develop from somitomere 6 and are supplied by CN VII (facial nerve). The branchial muscles of the third arch are derived from somitomere 7 and supplied by CN IX (glossopharyngeal nerve), and the muscles of the remaining gill arches are derived from head somites 1–4 and supplied by CN X (vagus nerve). Unlike some of the more conserved muscle groups we’ve already been introduced to, the branchiomeric muscles show tremendous diversification across vertebrate taxa (Table 12.2), and much of this diversification is related to changes in feeding and the loss of gills.

Table 12.2—Branchial muscle differentiation across select vertebrate taxa

So let’s begin by considering how these muscles work in gilled critters. The muscles that are directly associated with the gills are known as branchial muscles, and if you think about how gills work, there are two main things they need to do:

1. They need to be able to squeeze and expel water that comes in through the mouth (constrict). The function of constriction is accomplished by the superficial constrictor muscles, which are easily seen in the shark.
2. Then they need to reopen, so they can constrict again. This second function was ancestrally executed by a separate levator muscle for each arch. However, in modern taxa these separate levators have fused together to form a single muscle called the cucullaris. The cucullaris runs from the dorsal gill arches to the pectoral girdle, and this position is noteworthy because it shows that the branchiomeric muscles have attachments that reach all the way onto the appendages. In other words, even though these are “head muscles,” they are not restricted solely to the head.

And as we examine tetrapod lineages that have lost gills, we find that the cucullaris has migrated and now expands over the limb to form two major muscle groups:

1. the trapezius group in the dorsal shoulder and
2. the sternocleidomastoid group, ventrally.

The trapezius and sternocleidomastoid groups act to move the arm and head, and even though they span the pectoral girdle, they are in fact still innervated by CN XI (accessory nerve). CN XI is a discrete branch of CN X that innervated the cucullaris, thus revealing clues to the evolutionary history of this muscle group.

The muscles associated with the mandibular and hyoid arches also become specialized for jaw function in the gnathostomes, as these arches are incorporated into the jaw skeleton. Recall from Chapter 8 that one of the major transformations of the tetrapod skull was fenestration, which enabled the expansion of the jaw-closing muscles on the roof of the skull. Ancestrally, the mechanism for jaw closing was dominated by a single, large muscle called the adductor mandibulae. However, in mammals, the adductor mandibulae differentiates into several new, discrete muscles with different lines of action (i.e., they pull the jaw in different directions). These derivations include the temporalis muscle, which pulls the lower jaw dorsally and posteriorly; the masseter muscle, which pulls the lower jaw laterally; and the pterygoid muscle, which is deep to the others and pulls the lower jaw medially (Figure 12.7). Because all three of these muscles are associated with the mandibular arch, they’re all innervated by the cranial nerve of that arch, which is CN V (trigeminal nerve). Mandibular muscles also contribute to the floor of the mouth by forming the mylohyoid, which runs between the mandibles. The levator palatoquadrati of the shark differentiates to form the levator pterygoidei and the protractor pterygoidei in vertebrates with mobile crania (e.g., amphibians, reptiles, and some birds); however, these muscles are lost in animals that lack kinetic skulls (e.g., mammals).

Now jaw closing is certainly important, but in order to feed, the jaws have to open too. Ancestrally, jaw depression (which opens the mouth) was accomplished by hypobranchial muscles like the coracomandibular and coracohyoid. However, as noted above, throughout the course of evolution most of the hypobranchial muscles became involved with control of the tongue in tetrapods, especially mammals. Therefore, mammals needed a different jaw-opening mechanism and indeed evolved a new muscle called the digastric. The term digastric actually means “two bellies” (di = two; gastric = stomach) and this name reflects how the muscle is formed from two muscle bundles located between the dentary and mastoid process. The anterior portion of the digastric (anterior belly) is derived from the old intermandibularis muscle, which was located in the floor of the mouth of animals like sharks. The posterior belly is derived from the ancestral interhyoideus muscle, which was deep to the intermandibularis in the shark. The intermandibularis is associated with the mandibular arch, so like all the other mandibular arch muscles, it is innervated by the trigeminal nerve (CN V). But the interhyoideus is actually associated with the hyoid arch. And like other hyoid arch muscles, it is innervated by the facial nerve (CN VII). What this means is that the two parts of the digastric muscle are actually innervated by different cranial nerves: The anterior belly is innervated by CN V and the posterior belly by CN VII!

Other muscles of the hyoid arch are retained in mammals in the form of the stapedius and the stylohyoid. In fact, these are the only two hyoid muscles that retain a connection to the hyoid arch in this group! The remaining hyoid muscles lost their connection to the hyoid arch and instead spread out to become the muscles of the face and the platysma, which extends down the front of the neck.

Axial Muscles

The head muscles are considered muscles of the body axis and are therefore technically axial muscles. However, axial muscles are present along the entire length of the vertebrate body, so we must also consider the postcranial axial musculature. Ancestrally, the axial muscles were made up of segmental V-shaped myomeres; these myomeres were separated by myosepta and supplied by spinal nerves. The portions of the myomeres dorsal to the horizontal skeletogenous septum are referred to as epaxial muscles, and the portions positioned ventral to the horizontal skeletogenous septum are the hypaxial muscles. This myomeric organization is still seen in fishes today, in both the chondrichthyans and the osteichthyans. The muscles attach to the axial skeleton or the notochord, and contractions of axial muscles produce lateral undulations along the length. These undulations exert force on the surrounding water, and the resulting reaction forces produce thrust, resulting in forward swimming of the fish. In fishes, the majority of axial muscle mass is white muscle, which you’ll recall from Chapter 11 is composed of fast-glycolytic (FG) fibers (Chapter 11), which contract quickly (but also fatigue rapidly). These rapid-response muscles are excellent for generating propulsion quickly and hence used for escapes.

In tetrapods, however, the major evolutionary trend is toward a decrease in epaxial muscles and increase in hypaxial muscle differentiation (Table 12.3). For example, the hypaxial muscles of the tetrapod’s body wall show several distinct lateral layers of muscle. From superficial to deep, these layers form the external oblique, internal oblique, and transverse abdominis muscles, and each of these layers exhibits different fiber angles that bend the trunk in different directions (Figure 12.8). Furthermore, there’s also a ventral layer with fibers that run parallel to the body axis: This muscle is called the rectus abdominis. Over the course of tetrapod evolution, as animals shift from using sprawling to more upright postures, the hypaxial muscles came to play a reduced role in trunk stabilization and lateral bending. Instead, these muscles begin to play a greater role in changing the volume of the chest cavity, thus driving the inspiration and expiration of breathing. In fact, the major respiratory muscle of mammals, the diaphragm, is a derivative of the rectus abdominis muscle!

Table 12.3—Axial muscle differentiation across select vertebrate taxa

Appendicular Muscles

The last major portion of the muscular system includes the appendicular muscles. These are the muscles of the limbs and fins and are derived from extensions of myotomes called limb buds. These muscles can also be subdivided into two major groups: dorsal and ventral. As with the epaxial and hypaxial muscles of the body axis, the appendicular muscles are innervated by segmental spinal nerves.

We’ve already learned that some of the muscles that act on the forelimb are actually derived from the branchiomeric muscles (the trapezius group and the sternocleidomastoid group—see Table 12.2). However, there are also a large number of appendicular muscles that are intrinsic to the appendages themselves. The ancestral organization of the appendicular musculature was very simple, and this can still be observed in sharks and bony fishes. This organization basically consisted of a major dorsal muscle mass called the extensor or abductor and a ventral muscle mass called the flexor or adductor. Tetrapods, in contrast, show considerable differentiation of their limb muscles; nonetheless, the basic organization of these muscles can still be traced to the ancestral flexor/extensor groups seen in fishes (Table 12.4).

Many of the differences in the appendicular musculature that we observe in nonfishy vertebrates are related to postural changes in different taxonomic groups. With the shift from sprawling posture (common in amphibians and reptiles) to a more upright posture (common in birds and mammals), the ventral adductors tend to be reduced. In contrast, the dorsal extensors are usually enhanced. Across taxa, there is a general trend toward larger proximal muscles and smaller distal muscles. This pattern is largely related to energetic principles of locomotion. It costs more energy to carry a large mass farther from you than closer to you. Consider walking to class with your backpack—if you carried your bag in your hand, extended away from your body, this would be far more energetically taxing than carrying it slung over your shoulder. So as animals became more upright and longer limbed, there was a distinct energetic advantage to reducing the muscle mass of the distal limbs and shifting those heavy muscles as close to the trunk as possible. But if the muscles are all located close to the trunk, how are the distal limbs moved? Well, the muscles that control the movement of the distal limb are attached to the distal bones by long, light tendons; this allows the muscles to control the movement of these elements while also keeping the distal limb lightweight.

Table 12.4—Appendicular muscle differentiation across select vertebrate taxa

12.6 Human Muscles: A Bipedal Tetrapod

Given our shared evolutionary history as mammalian tetrapods, humans’ musculature very closely resembles the musculature of other mammals. This is one reason that animals like cats, rabbits, and minks can be used as dissection stand-ins for human cadavers during anatomy labs—even in strictly human-based anatomy courses. However, it is worth noting that most mammal species are quadrupeds (meaning they move about on all four limbs), whereas humans are bipedal tetrapods (walking about on only two limbs). As a result, human bodies do undergo some muscular reconfiguration in order to accommodate bipedal posture and locomotion; these changes are particularly noticeable in the pelvic region and can help explain some common human muscle pathologies (Figure 12.9).

The piriformis muscle is a deep muscle of the gluteal region that functions to laterally rotate the thigh in humans. It originates from the sacrum, passes through the greater sciatic foramen of the pelvis, and inserts on the greater trochanter of the femur. This muscle sits in very close proximity to the sciatic nerve, which also passes through the greater sciatic foramen (Figure 12.10). Hypertrophy or inflammation of the piriformis muscle can cause the muscle to compress the sciatic nerve and result in pain, tingling, or numbness in the gluteal region, in the posterior thigh, and sometimes even down the calf and to the foot. This condition is known as piriformis syndrome.

The iliopsoas is actually composed of two thigh muscles: psoas major and iliacus (Figure 12.11). Both of these muscles insert on the lesser trochanter of the femur, but they have different origins. Psoas major originates in the lower back (from the 12th thoracic vertebra to the 5th lumbar vertebra), whereas iliacus originates from the iliac fossa of the pelvis. These muscles function together as a unit to flex the thigh. Psoas major can also laterally flex the vertebral column when the hip joint is held stationary; this is an example of how a muscle’s action can change when its origin and insertion are swapped. However, overuse of the iliopsoas through excessive repetitive flexion can lead to injury or inflammation of the muscle and/or its inserting tendon, leading to iliopsoas syndrome. Because the condition is often associated with dancers and high jumpers, it is also sometimes called dancer’s hip or jumper’s hip. Iliopsoas syndrome can cause lower back pain as well as pain in the hip or groin region, depending on the specific part of the iliopsoas muscle affected.

If you have an interest in exercise or physical fitness, you may already be familiar with the rectus abdominis muscle. Rectus abdominis is a superficial muscle that runs the length of the ventral abdomen (Figure 12.9). This muscle originates from the xiphoid process of the sternum and the inferior surfaces of ribs 5–7; it inserts on the superior pubis. The rectus abdominis is the muscle that is activated when flexing the trunk anteriorly, such as during crunches or sit-ups. This muscle is characterized by having tendinous insertions along its length, which separate sections of the muscle into smaller “blocks” that are sometimes visible under the surface of the skin—these are what we commonly refer to as “six-pack abs”!

12.7 Summary

The muscular system really drives the movement of the vertebrate body—both in the sense of moving an animal through its environment and in moving materials through the animal’s body. The properties of muscle tissue, along with its structure at both the microanatomic and macroanatomic scales, are intimately tied to muscle function. Furthermore, the muscular system is intimately linked with both the skeletal system, as they work together to give the body structure and movement, and the nervous system, which generates the stimulus for muscle contraction. Vertebrate muscles can be organized into six functional groups, and although some of these groups are highly conserved across vertebrate taxa (e.g., extrinsic eye muscles), others show incredible diversification related to environmental and postural changes associated with tetrapod evolution (e.g., appendicular muscles). Nonetheless, muscle origins can be traced through evolutionary history through a combined examination of muscle development and innervation patterns.

12.8 Further Reading

1. Martin, James M., and Roland M. Bagby. “Temperature–frequency relationship of the rattlesnake rattle.” Copeia 1972 (1972): 482–485.
2. Nguyen, Allyn, Jordan P. Balaban, Emanuel Azizi, Robert J. Talmadge, and A. Kristopher Lappin, “Fatigue resistant jaw muscles facilitate long-lasting courtship behaviour in the southern alligator lizard (Elgaria multicarinata).” Proceedings of the Royal Society B 287 (2020): 20201578.
3. Powell, Anthony R. “Sustained force production by jaw muscles of specialized megalophagous frogs (Ceratophrys Spp.)” PhD diss. California State Polytechnic University, Pomona, 2022.
4. Schaeffer, Paul J., Kevin E. Conley, and Stan L. Lindstedt. “Structural correlates of speed and endurance in skeletal muscle: The rattlesnake tailshaker muscle.” Journal of Experimental Biology 199 (1996): 351–358.
5. van Ginneken, Vincent, Erik Antonissen, Ulrike K. Müller, Ronald Booms, Epp Eding, Johan Verreth, and Guido van den Thillart, G. “Eel migration to the Sargasso: Remarkably high swimming efficiency and low energy costs.” Journal of Experimental Biology 208 (2005): 1329–1335.

12.9 References

1. Amerman, Erin C. Human Anatomy and Physiology, 1st ed. Boston: Pearson, 2016.
2. Marieb, Elaine N., and Katja Hoehn. Human Anatomy and Physiology, 10th ed. Pearson: Boston: Pearson, 2016.
3. Martin, James M., and Roland M. Bagby. “Temperature–frequency relationship of the rattlesnake rattle.” Copeia 1972 (1972): 482–485.
4. McKinley, Michael P., Valerie D. O’Loughlin, and Elizabeth E. Pennefather-O’Brien. Human Anatomy, 5th ed. New York: McGraw Hill Education, 2015.
5. Nguyen, Allyn, Jordan P. Balaban, Emanuel Azizi, Robert J. Talmadge, and A. Kristopher Lappin, “Fatigue resistant jaw muscles facilitate long-lasting courtship behaviour in the southern alligator lizard (Elgaria multicarinata).” Proceedings of the Royal Society B 287 (2020): 20201578.
6. Powell, Anthony R. “Sustained force production by jaw muscles of specialized megalophagous frogs (Ceratophrys Spp.)” PhD diss. California State Polytechnic University, Pomona, 2022.
7. Schaeffer, Paul J., Kevin E. Conley, and Stan L. Lindstedt. “Structural correlates of speed and endurance in skeletal muscle: The rattlesnake tailshaker muscle.” Journal of Experimental Biology 199 (1996): 351–358.
8. van Ginneken, Vincent, Erik Antonissen, Ulrike K. Müller, Ronald Booms, Epp Eding, Johan Verreth, and Guido van den Thillart, G. “Eel migration to the Sargasso: Remarkably high swimming efficiency and low energy costs.” Journal of Experimental Biology 208 (2005): 1329–1335.