Anthropology 105

The bones that make up the shoulder are the scapula, clavicle and humerus.

The humerus is the upper arm bone, with a ball-shaped head at the proximal end. The scapula is a flat, triangular bone in humans. The most prominent parts of the scapula are at its lateralmost angle where it articulates with the humerus. Here, the bone bears a shallow, bean-shaped depression called the glenoid fossa. Two projections, the acromial and coracoid processes, extend beyond the glenoid fossa providing attachments for some of the muscles and ligaments of the shoulder and upper arm. The clavicle articulates with the acromial process and extends toward the midline of the torso, with its medial end articulating with the superior part of the sternum.

What to do: Examine the scapulae of different kinds of primates. You'll find that primates with different locomotor patterns have rather different scapula morphology.

Monkeys and prosimians that are mainly quadrupeds have relatively long and narrow scapulae. Their shoulders are adapted for forelimb movement anteriorly and posteriorly, but not especially to the side or above the head.

By contrast, apes and humans have scapulae that are very triangular in shape. The shoulder joint is more mobile in these primates, with the arm able to move freely to the side and above the head.

The mobility of the scapula is also related to the shape of the trunk. Monkeys have a deep trunk that is relatively narrow from side to side, while apes and humans have a shallower trunk that is wider from side to side.

Ecology, diet, competition, and ease of movement all affect the size of primate groups. The structure of primate groups is primarily affected by the mating system. There are several elements of primate mating systems. In most species, individuals of either one sex or the other disperse from their natal group --- the one they were born in --- when they reach adulthood. This dispersal affects the structure of the groups by breaking some kinds of relationships and preserving others.

For example, in primate species where maturing females transfer to a new group, males are often left within the group where they are born. This means that males can form relationships as juveniles that last their entire lives. The long-lasting male coalitions in chimpanzees are a side-effect of female dispersal, conditioned by large group sizes and other social factors. In contrast, male savanna baboons transfer to new groups when they reach adulthood. In baboon groups, the female associations are highly structured by kin relations, since mothers and daughters live in the same group as adults.

Mating conflicts

Mating is essential to reproduction, and is the contest through which individuals pass their genes into future generations. From an evolutionary perspective, individuals do whatever they can to promote their own chances to reproduce. Sometimes, individuals can promote their own reproduction by inhibiting the chances of others. In other instances, it may be in their best interest to cooperate with other individuals, or to bide their time waiting for higher-ranking individuals to die or lose status.

The most basic conflict of interest in mating is between males and females. Because of their biological role in carrying and providing nutrition for their offspring, both before and after birth, females must make a large investment in reproduction. Considering the large cost of reproduction, an adaptive mating strategy for a female is to mate with the male whose genes will contribute to the best possible offspring. For this reason, females are typically choosy about which males they will mate with. This element of female choice can give rise to sexual selection, in which males are advantaged by the possession of features that females value.

In contrast, males may have extreme levels of competition for mates. A single male may be able, through fighting, threat, or intimidation, to prevent other males from having mating access to females, or even to expel all other adult males from the group. If he is successful, the reproductive opportunities for such a male are tremendous. On the other hand, the opportunities of other males fall to zero. This places a tremendous genetic payoff on social competition for mating.

The intensity and form of mating competition vary from species to species. Some kinds of primates have a sparse diet that is simply unable to sustain the caloric requirements of huge male body sizes. Other primates or may modify the conditions of combat through coordination of activity with other individuals, emphasis on advertising the risks of combat rather than pursuing combat itself, or other means.

Males and females within a species often differ in size or morphology. For example, male primates almost always have larger canine teeth than females. The canine teeth are important in male mating competition --- males can display their canines as a threat to other males, and at an extreme they can injure or kill other males with these teeth. One indication of the importance of the canines in displays is that they tend to be more dimorphic in species that are active during the day, as opposed to nocturnal species (Leutenegger and Cheverud 1982).

Sexual dimorphism in body size is very pronounced in many primate species. For example, orangutan males average around twice the body mass of females. The body mass dimorphism is even more extreme for gorillas than for orangutans. Many different factors influence the body size dimorphism in a primate species (Hedrick and Temeles 1989). One of these is mating competition between males --- intense male competition increases the value of male body size. Another factor can be food competition between the sexes --- when males are larger, they may be able to dominate a larger share of valued food resources. Additionally, males can take on important reproductive roles beyond mating, such as protecting young juveniles from predation or infanticide.

Mating competition in many primates involves territoriality, when males defend a home range against incursions from other males. Primate groups may be territorial as a result of a single male's action, or the coordinated activity of multiple males. For example, Males of some primate species dominate access to females by preventing other males from coming into their home range. These primate males are said to be territorial. Even small social groups, like the monogamous male-female pairs of gibbons, may be highly territorial. But chimpanzees provide one of the strongest instances of territoriality among primates. Groups of male chimpanzees walk the approximate perimeter of their territory, engaging in violent conflicts with any members of neighboring groups they might encounter (Wrangham 1999). As observed by Jane Goodall (1986) at Gombe in Tanzania, the males of one group of chimpanzees killed all of the adult males and several females and juveniles in a neighboring group over the course of several months.

Kinds of groups in primates

Group size, dispersal, and mating competition all contribute to the proportion of males and females found in any given group. Sometimes a single male and female form a group; sometimes a single male and multiple females; sometimes multiple males and females; and occasionally a single female and multiple males.

Gibbons tend to form long-lasting associations between a single adult male and a single adult female. These pair-bonded primates occupy territories that they defend against incursions from other individuals. Both males and females make long vocalizations, called songs, to establish their shared territory. They often vocalize together in duets, although in different contexts based on whether threats come from males or female intruders (Geissmann 2000, Mitani 1987). These groups of a single adult male and female and their offspring are called monogamous groups.

In many kinds of primates, a single male may dominate a group with multiple females. This is a polygynous group --- a multifemale, single-male group. Polygyny results from strong mating competition among males. Only if a single adult male can repel other males from the group can he reap the powerful reward of mating with many females.

A well-known species with polygynous groups is the gorilla. Gorilla groups generally have one adult male, up to eight or more females, and their dependent offspring. Solitary males live outside of these polygynous groups and sometimes manage extragroup matings with females. These groups are maintained by strong mating competition --- a dominant male in a group repels other males by threats, intimidation, or violence.

Even so, there is variability in gorilla societies. In mountain gorillas, multimale groups are common (Robbins 1999). In such groups, the dominant males have a majority of matings, and often harass subordinate males that attempt to mate. But subordinates do have many mating opportunities, demonstrating a social flexibility among gorillas.

Marmosets and tamarins, called callitrichids, are the smallest of the New World monkeys. These monkeys are among the few primates for which twin births --- and sometimes triplets --- are common. This means that females tend to have high energetic requirements in pregnancy, lactation, and caring for young. Callitrichids therefore face unique challenges compared to other primates.

One way that these monkeys adapt to caring for more young is that older offspring of a female may stay with her for a longer time instead of quickly going off on their own. These older offspring help to watch and sometimes provide food for their younger siblings (Bales et al. 2000).

Another behavioral adaptation is for a single female to mate with and coexist with multiple males. This kind of mating system is called polyandry. Mating with multiple males reduces the paternity certainty of the males --- a male cannot know if a female conceived her offspring with him or another male. As long as mating opportunities are limited, males may cooperate in a group with a single female on the chance of having offspring with her. These males help to provide food and defense for the young juveniles in polyandrous groups. Polyandry is not universal among callitrichids; it is adopted more when resources and mating opportunities are rare (Goldizen 1988).

Some primates coexist in large groups numbering 50 individuals or more. A group this large is always a multimale group --- there is no way for a single male to deter other males from twenty or more adult females. But multiple males sometimes coordinate their behavior to deter neighboring groups. A large multimale group may occupy and defend a large territory, especially where movement costs are relatively low.

Large primates who live in large groups have a problem: there are very few food patches large enough to feed them all. So even though a large multimale, multifemale group may occupy a substantial territory, it may not be possible for them to feed together much of the time. Chimpanzees live in such large multimale, multifemale groups. Even though members of the group share a dominance hierarchy, social interactions, and relationships, they spend much of their time apart. Smaller groups of individuals --- sometimes a single female and her young, sometimes male-female pairs, and sometimes small groups of either sex --- split apart in order to forage for food. These small groups recombine and split in different combinations, and sometimes all of them come together, especially when food is plentiful. This kind of social organization is called a fission-fusion society. Individuals divide into small foraging groups and come back together into the full community for social interactions.

The diversification of the first primates from other early mammals took place partly because the ancestors of the primates came to inhabit a unique environment --- the trees. These early primates developed many features to allow them to move quickly in this arboreal habitat. Early primates evolved the ability to direct and focus both eyes on objects, called binocular vision, which allowed them to accurately judge distances to branches and other objects. They also developed grasping hands and feet, with opposable digits --- thumbs and big toes. The fingertips were broader in these early primates, to apply greater grip strength to branches, and instead of claws primates developed wide nails. All of these features helped primates to succeed as arboreal specialists.

• Primate adaptations to arboreal environments include binocular vision, opposable digits, enlarged fingertips and nails.

Many primates today continue this arboreal existence, spending large proportions of their time off the ground and in the trees. Moving in an arboreal environment has the obvious risk of falling out of the tree if everything does not go exactly right. Yet primates are virtual trapeze artists, masters of the arboreal environment. Smaller monkeys and lemurs can rush headlong from branch to branch, seemingly mindless of any risk of falling, because of their unrivaled arboreal skills. These primates bridge immense gaps by leaping from one tree to another, limited only by the acceleration of gravity. Even large primates like chimpanzees and orangutans can rapidly scale trees and move effectively from one tree to another. These arboreal skills are made possible by a large suite of adaptations, many of which originated very early in primate evolution.

But even though all primates are climbers, some of them have developed more specialized adaptations to other kinds of movement, or locomotion. These specialized forms of movement are adapted to different kinds of environments. Some primates are excellent at moving terrestrially, on the ground. Others are good at climbing tall vertical trunks and branches, or at swinging from one branch to another. Species who use these special forms of locomotion have consequences in their skeletons and muscle configurations.

Vertical clinging and leaping

Many prosimians, including tarsiers and many lemurs, use a form of locomotion called vertical clinging and leaping. These kinds of primates live in habitats where they climb relatively small tree trunks or bamboo. Sometimes they leap between these vertical supports. Other times, especially for the larger lemurs like sifakas, they leap along the ground. Their legs are relatively long compared to their arms, so that terrestrial movement can be more effective by leaping than by running on all fours.

This form of locomotion gives their bodies a very distinctive shape --- especially tarsiers, who are masters of this pattern. Tarsier legs are longer than their bodies and forelimbs put together, and they especially have very long foot bones. The name for these bones are tarsals, giving these unique little primates their name.

Below-branch locomotion

Some monkeys and all apes are adapted more to hanging beneath branches than running atop them. This suspensory style of locomotion is essential for larger arboreal primates, which can move above only the largest branches. Hanging below branches enables large primates to climb into the forest canopy, often on smaller branches than could support them from above.

A skeletal adaptation to suspension includes relatively long arms with very mobile shoulder joints. In contrast to quadrupedal monkeys, whose arms are limited in their range of motion, apes can move their arms through nearly a complete 360 degree circle. Also, apes' trunks are relatively flat from front to back, with the shoulders mostly alongside rather than in front of the spine. Putting the arms at the side requires long and strong collarbones --- called clavicles --- that serve as a strut supporting the shoulder musculature. Also, apes have extremely long fingers, useful for hooking onto branches quickly. Their thumbs are quite small, as they do not usually grip with their thumbs onto branches while hanging from them.

• Brachiation is arm-over-arm swinging.

Sometimes apes swing arm over arm from one branch to the next, a locomotor pattern called brachiation. Gibbons and siamangs are a brachiation specialists, but all living hominoids have the skeletal anatomy to enable them to brachiate. Brachiation conserves the energy of forward movement by treating the body as a swinging pendulum. This is a very efficient way to travel for medium-sized primates, combining energetic conservation with speed, and working with gravity instead of against it.

• Quadrumanous locomotion uses all four hands and feet to move among branches.

Large-bodied hominoids brachate less than gibbons. Branches of sufficient size to support the entire weight of a large ape are rarely located close enough to brachiate between them. Also, the pendular motion is less efficient for larger primates, because their arms just cannot be as long in proportion to the size of their bodies. Instead, when in the trees, the living great apes grip branches with three or four of their hands and feet at once. This allows large apes to support their weight on relatively small branches in the canopy. The masters of this kind of locomotion are orangutans, who move through the forest canopy moving one hand or foot at a time to a new support branch. This kind of locomotion, as if an animal was using four hands equally, is called quadrumanous locomotion.

Knuckle-walking and fist-walking

• Knuckle-walking allows quadrupedal walking in chimpanzees and gorillas, whose hands are adapted to suspension.

Chimpanzees and gorillas, when they are on the ground, walk quadrupedally using the proximal finger joints of their hands instead of the palms of their hands. They use this style of locomotion, called knuckle-walking, because of their unique forelimbs. These apes have long forelimbs relative to their hindlimbs, and their hands are very long with strong tendons for curling the long fingers into a powerful hook. These hands are very well adapted to suspension in the trees, but they are not capable of being extended with the palms toward the ground, which is the way most other primates walk quadrupedally. So instead of walking palm-down, they use their knuckles.

A few skeletal features of living chimpanzees and gorillas appear to be adaptations to knuckle-walking. Because the arms are held in a locked position while supporting the body, unlike the somewhat flexed position usual in quadrupeds, the proximal end of the ulna is more U-shaped, built for supporting the humerus mainly from below. Likewise, the joints of the hands are more limited in motion, and relatively incapable of being extended backward at the wrist and knuckles. It is not clear whether these unique anatomical consequences of knuckle-walking evolved in parallel in chimpanzees and gorillas, or whether they represent homologies inherited from a knuckle-walking common ancestor of gorillas, chimpanzees, and humans.

Although many orangutans spend little time on the ground in their natural habitat, they can walk quadrupedally. But unlike chimpanzees and gorillas, orangutans do not walk on their knuckles when they are on the ground. Instead, they curl their hands inward, walking on the outside of their fists. This fist-walking accomplishes the same goal as knuckle-walking --- it allows walking on all fours without facing the palms of the hands toward the ground.

When talking about bones and teeth, we will need to use several terms to orient ourselves. Some of the terms are obvious, like right and left. Other intuitive terms can fail us, however. For example, we could use higher and lower to refer to parts of our arms, but these terms will be confusing if we lift our arms over our heads. Even left and right can cause confusion: sometimes we need to talk about the left surface of our right arm, for instance. For reasons like these, anthropologists use terms with specific anatomical meanings to talk about the
positions of bones and features on them.

Humans are special compared to many vertebrates in having a vertebral axis that runs roughly up and down, at least while we are standing up. For this reason, a long tradition in human anatomy uses these terms:

Superior: Higher. The nose is superior to the mouth.

Inferior: Lower. The nostrils are most visible on the inferior aspect of the nose.

These terms are always used when referring to directions on the head. For the postcranial skeleton, we may also use cranial and caudal, which orient along the axis of the spine. For animals that don't carry their spine in an upright or vertical position, cranial and caudal will always denote the same directions.

The vertebral axis is only one direction, and our bodies have two additional directions: front to back, and side to side. The terms for the front to back direction are:

Anterior: Toward the front. The nose is on the anterior side of the head.

Posterior: Toward the rear. The posterior side of the head is frequently covered in hair.

Dorsal: In humans, toward the back of the torso. The shoulder blades are dorsal to the ribs.

Ventral: In humans, toward the front of the torso. The navel is on the ventral aspect of the body.

In humans, dorsal and ventral are mostly synonymous with posterior and anterior, and the latter terms are often used. In animals with habitual postures that are different than ours, dorsal and ventral retain an anatomical meaning that is unchanged and thus prevent confusion.

Left and right are absolute terms instead of relative terms. These terms separate one half of the body from the other. The right arm will always be the right arm, and the right lung is right even though it is not as far right as the right arm.

To refer to the position of a feature relative to another, the following terms are used:

Medial: Closer to the midline, or dividing line between right and left halves, of the body. The neck is medial to the shoulder.

Lateral: Farther from the midline. The eye is lateral to the nose.

The limbs are special cases, because they can move a great deal relative to the spine. For the limbs, anterior, posterior, medial, and lateral are all relative terms used in reference to a particular limb position, called the anatomical position. For humans, the arms are in anatomical position when hanging at the sides of the body, palms forward, and the legs are in anatomical position in a normal standing posture, feet side by side. This means that the pinky side of the wrist is medial, and the thumb side is lateral. Superior and inferior are not used for the limbs at all. These terms are replaced by:

Proximal: Closer to the point of attachment with the torso. In other words, closer to the shoulder or the hip. The elbow is proximal to the wrist.

Distal: Farther from the point of attachment. The ankle is distal to the knee.

These terms can be somewhat confusing to learn, but they prevent a great deal of confusion in referring to bones and their features. The most common ones
in this course will be anterior, posterior, superior, inferior, medial, lateral, proximal, and distal. Teeth and the hands and feet each have a few special directional terms, which will be introduced along with these anatomical areas.