Monday, November 11 -- Female Dominance

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Recap of last lecture:

Last time we looked at cooperative relationships and social bonds, such as in monogamous pairs who cooperate to defend a territory. We also looked at social bonds in some polygynous species, such as gorillas, where females are loyal to the silverback male and will help him repel invading males. In return, he protects them from other males and protects their kids from other females. We also saw in bonobos how females maintain strong bonds with their sons. We saw social bonds where you'd least expect them- in a promiscuous mating system where males and females nevertheless form strong social bonds and females are able to express mate choice even though there's strong sexual dimorphism. We talked about Barb Smuts' work on friendships in baboons, defined in terms of physical proximity and grooming, and how females do most of the work in relationship maintenance. Females gain protection and males gain by increasing mating success. Also he didn't mention but we probably already know all the stuff in the coursepack article by Barb Smuts, "What are Friends For?"

Continuing on male-female relations, we're going to see two extremes; today we'll see female dominance, and next time male coercion. This is building on the theme developed in ch. 8 in Krebs and Davies.

Predictions from sexual selection theory

The basic rule is male dominance. Males usually win conflicts and have priority of access to food, etc. Why? This goes back to sexual selection. Because of sexual selection, you get sexual dimorphism; males are bigger and have more weaponry. When they come into conflict with females, it's usually the male who wins. In this sense, male dominance is kind of a byproduct of competition between males. Sexual selection shapes males physically but also mentally- they tend to be more aggressive and more competitive. There are cases where males and females are equal but there are very few instances where females are dominant.

Examples of species with male dominance: brown capuchins, baboons, langurs, orangutans, chimps.

All early studies in primatology focused on male dominance. One reason is that it's more visible and exciting. Also, they were all men and probably had a cultural bias that made it easier for them to see the male dominance. After a while, though, they began to see that females formed social bonds and could gang up on males. Through the 80's all serious work on female dominance was done by women primatologists.

Female dominance in primates

"To a greater or lesser extent, females in these species take priority at feeding sites and control social access to other group members. An offending male who comes too close to a female or her infant is cuffed in the face or chased away, and in some cases males are relegated tot eh outskirts of the troops. These species stand in contrast to television narratives about 'central male hierarchies' and 'dominant male leaders' - Sarah Hrdy 1981, pg 59, describing female dominance

Most female dominance species are in the prosimians, especially the prosimians of Madagascar. Ring-tailed lemur, sifakas (propithecus), and the indriis who are monogamous.

There are also a few cases outside of Madagascar; squirrel monkey (evidence not quite so clear cut), and the talapon which is a small cercopithecus. In apes, some newer research on bonobos shows that by forming alliances with each other, the females are able to socially dominate the males.

Female dominance in prosimians

Who? Mostly prosimian primates: mouse lemur (microcebus); dwarf lemur (cheirogaleidaes); mongoose lemur (lemuridae).

For a while it looked like the whole lemuridae family was female dominant, but it turned out that that's not the case- a 1990 comparative study of ring-tailed lemurs, crowned lemurs, and brown lemurs found that females were dominant in the ring tailed and the crowned lemur, but not in the brown lemur. Therefore, we can't just write it off as a characteristic of lemurs.


Female feeding priority
Most research has involved conflict over food, mainly because it's more dramatic and easier to collect data on. If you look at % of encounters between males and females, in the sifaka about 70% are over food, but in the ring-tailed lemur only about half are over food.

More than feeding?
If you look at % of encounters where females win in ring-tails, olfactory disputes, sexual disputes, and grooming disputes are all 100% female-won. Feeding and spatial (supplanting) disputes are won over 90% by the female, and agonistic disputes are won by the female about 60% of the time.

Correlates of female dominance
These are the main cues that people have used in trying to come up with hypotheses on why these species are special.

Why? Two Hypotheses...

We're going to give these but bear in mind we don't have a very convincing theory yet. Maybe someone would like to take it on for their final paper?

The male perspective
Males defer to females in order to conserve energy for the brief, but energetically costly, annual mating season.
Think about it- male competition is all about mating access, but if for most of the time there are no receptive females since the breeding system is so short, then what's the point of wasting energy being dominant?

The female perspective
Environmental or metabolic factors combine to increase the costs of reproduction for females. Given these circumstances, females win competitive interactions because the benefits they gain are greater than those derived by males. Basically, females are harder-pressed to get enough food.

Data that supports or harms these theories:

Prediction: Female dominance should go with shorter breeding seasons.
Female dominant systems indeed have much shorter breeding systems than male dominant systems. Female dominant species' breeding season is about 50 days, while male dominant species' breeding season is about 220 days- like 2/3 of the year. However, the correlation is not perfect: brown lemurs have a very short mating system, about 14 days, so they should be female dominant but they're not.

Prediction: Female costs of reproduction should be high in female-dominant species.
Food scarcity during gestation and lactation
Madagascar is more seasonal than most primate habitats. It's also got a pretty short season of plenty and they can't complete their whole reproductive cycle during the season, so the food goes away before they're done gestating and lactating. Note that there's no good data to back up this theory; no one has gone out and measured food availability and energy costs etc.

Small body size and therefore high metabolic rates
Smaller animals have higher metabolic rates. Are female dominant species unusually small? Yeah, they're smaller but it's not so dramatic. It's not statistically significant. The standards of deviations are pretty large.

Large litter sizes
If some species are producing more or larger infants, then that's going to increase the nutritional stress on the moms. Data? Female dominant species' neonate:mom weight ratio is .12, while in regular primates it's .72. So, indeed, female dominant species are having bigger kids. (This is total litter weight; may be because they have more kids or may be because they have heavier kids.)

Rapid infant growth
After they're born do the kids grow up faster? If they do, then their nutritional needs are greater. The rate of infant growth shows how great the stress is on the mom. Data for this is weaning data compared to female weight; you look at whether they're being weaned early or late for their moms size. You see that female dominant species fall below the line- they're weaning before you'd expect; so their babies are growing up faster. This is definitely a trend, but it's not super dramatic.

Demographic patterns that suggest that costs of reproduction are higher
Live fast, die young
If you plot life span vs birthrate, species that reproduce at higher rates tend to be those who die younger- this may have to do with the costs of reproduction. When you control for the lifespan of species, you find that female dominant species are above the line- they're reproducing offspring at a higher rate and they're dying earlier. All of which suggests their costs of reproduction are higher.

Propithecus mortality and lemur catta sex ratios
Propithecines show higher mortality rates for females than males for all age classes- life is harder on them for some reason, so they're more nutritionally stressed, so they die more.

Also, the lemur catta shows skewed male-female sex ratio in adults- which shows that females are dying faster than males.

To sum up;

There's some evidence that tends to support both hypotheses but no one is really super convinced yet. People have been interested in this because the idea of male or female dominance has a lot of social and political interest and many people are interested in the evolution of these trends.

Wednesday, November 13 -- Male Coercion

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Guest speaker; Barb Smuts

Wrote the book on baboon friendships. Edited our textbook. Is working now on male coercion.


She first became interested in male coercion when doing her dissertation on friendships. Although most interactions between males and females were affilitative or neutral, there was some aggression, too. This hadn't even gotten much attention. Males weigh twice as much as females and have huge sharp canines- the biggest, sharpest canines on the african savannah-- So there is potential for males to inflict serious injury to females. She began to wonder how often aggression took place.

She collected data over 2 year period based on focal samples of females who were pregnant or lactating- in other words, not attractive to males. She found that the non-estrous female was attacked once a week. This usually didn't involve biting, but there is always that potential. A female typically got a serious wound once a year- including a slash with canines that will draw blood. A slash is generally not too awful, but it does interfere with foraging and mothering. Only once did she see a fatal attack and she doesn't think the male intended to kill the female.

So why are the males attacking the females?

Immediate context- What were they doing right before the attacks?
20% of the time, the aggression occurred in context of feeding competition; the female got in the way of the male's food. 20% of the time was when the male was involved in aggression with another male and redirected his anger at the female. The remainder was in various 5 or 6% sized contexts. However, 25% of the attacks were classified as unprovoked; Smuts couldn't figure out any reason for the attack.

She thinks that in some cases the male was punishing the female for something she did several hours or several days earlier. Why does she think this? Once she saw a female attack another female who was a friend of a male. Smuts watched the male, and when the attacking female returned, he attacked her. So many of these 'unprovoked' cases might involve earlier incidents which hadn't been seen by the observer. In other cases, she thinks that it's just the male displaying his superiority over the female and reminding her of his power over her so when he tried to mate later, she would be more likely to submit to him.

Functional terms- what can the males potentially gain in fitness?
The data we've been discussing was from a study on non-estrous females, but most species for which we have data are from estrous females because most attacks happen to estrous females. This leads us to believe that male attacks must be related to mating or to mating access.

Review on male-male competition and female mate choice
The main way males can increase their mating success is by fighting with each for mating. Fighting establishes a mating hierarchy where the higher-ranking males have more access to females when the females are likely to be fertile. When you think about it, the outcome of male-male competition doesn't guarantee mating access- one way it does is if females prefer to mate with dominant males. This is apparent in many species including savannah baboons. They might pick dominant males 'cause they have better genes or because they can protect them better, being stronger.

When the dominant male protects females, he offers them benefits, but he can also offer them other benefits like in friendships; grooming, and long-term affiliative relationships with the infants. So males are increasing their access to mates by providing females with benefits- they do something good for females, making them more likely to chose them for mates.

Another way for the males to increase their mating success is by inflicting costs onto the females if they don't cooperate- this is an alternative to providing benefits. A primary way to inflict costs is by threats or actual aggression.

Sexual coercion

Definition: Any use of force or threatened use of force by a male against a female that functions to increase that male's mating access to the female, or that functions to decrease the probability that she will mate with another male, or both.

This is a functional definition- when we see aggression by a male, we can't say it's sexual aggression unless we see that it actually had the result of increasing his mating success or decreasing other male's success.

A gamut of examples

Please remember that this is a continuum- a male might threaten a female when she looks at another male or he might force copulation when she is screaming. We emphasize that forced copulation is not common among nonhuman primates.

Rhesus macaques- Joe Manson did a study on their mating behavior and found a high incidence of male aggression. When a female is mating with a low-ranking male, a high-ranking male is likely to come along and attack and chase the female, not the other male. Smuts spent a few weeks with this population when she was thinking about this subject, and was really struck by how much violence there was. What Manson points out is that even though females pay this cost, they continue to solicit low-ranking males. So here, female choice is coming into conflict with male mating strategies.

Chimps- Jane Goodall has provided data on how often male aggression occurs in chimps. It's most common against estrous females- for instance a picture shown in lecture which shows a male who has lifted a female up and is biting her on the back of the leg.

Goodall has a detailed analysis with good data and she noted a few things- a lot of male aggression against female chimps occurred in the first few days of their estrous cycle, before swelling. A female chimp swells for a few weeks and ovulates at the end, but most aggression is at beginning of swelling- it seems that males attack females repeatedly during their first phase to condition them to sexual submission so that as she reaches ovulation, she's more likely to submit to the advances of the male who attacked her. This is mostly based on circumstantial evidence. However, females usually don't reject sexual advances. The best strategy for male to get good mating success is to convince (read: coerce) a female to go away with him and mate in peace. The alpha male doesn't have to do this because he can keep the others away, but lower guys need to, otherwise they'll get interrupted. Some females go with guys they like but others are kept there by coercion. If she tries to leave, he bites her and things like that. So this aggression occurs hours or days before the actual mating- it's not as immediate as in the rhesus.

Hamadryas baboons- Female remain with males year after year throughout pregnancy lactation etc. This lack of association with any other males is maintained by the male hour by hour with instant reaction if the female strays too far away from the male. If a female moves too far off, the male gives the eyelid flash. If she doesn't come back, he rushes over and grabs her and gives her a ritualized bite on the back of the neck. Then she comes rushing back and presents to him (a form of ritualized submission). When she comes into estrous again, she is deeply conditioned to submit to this male after all these attacks.

Orangutans- As she said earlier, forced copulation is rare in nonhuman primates- the only species it's been documented in often in the wild is the orangutan. Remember that they're solitary females with ranges, and males who have larger ranges covering several females. When a female first comes into estrous, younger males who normally wouldn't have a chance later in the estrous cycle follow her around and force copulation. Observers know it's forced because the females scream and struggle.

(Chimps also force copulations infrequently, but it's just been seen in certain individuals in Gombe.)

Female Counter-strategies

Female-female coalitions
Vervet monkeys show the most widespread female counter-strategy. They form broad coalitions among female kin to defend each other against males. The size difference between males and females is 10-20% and two females can easily overwhelm a male. There is some male aggression against low-ranking females, but if a male tries anything with high-ranking female, she just turns around and whacks him one and he doesn't retaliate 'cause he knows she'll get all her relatives on him and make him feel it.

Female-female coalitions against males are not found only in primates. Lions form female bonded groups and if male lions show aggression, especially toward the infants when they've just joined a group, the females band together against him. They showed that the number of females in a pride affects the number of babies that are killed when a new male moves in.

Male-female affiliations
Another way to gain protection is by being in affilitative bond with another male who will come to your aid if you're attacked by another male. This is common in baboons 'cause female coalitions aren't too useful when dimorphism is as large as it is in baboons.

This strategy of affiliating with the male is most developed in the mountain gorilla. Females are not bonded or closely related. They don't bond with each other, but just with the male. Wrangham proposed that females do this to protect themselves against male harassment- more because of infanticide than sexual coercion but if you think about it, infanticide functions just like coercion because it brings the female into estrous sooner and increases the male's mating opportunity.

In 20 documented cases where the male gorilla died or disappeared and left females and babies, in every case all the babies were killed by another male.

Female dominance
Another way females can protect themselves is by dominating males. This occurs especially in lemurs. For example, in ring-tailed lemurs, male aggression is reduced or absent.

Variation across species on male aggression and sexual coercion-

Why is male coercion more common is some species than in others? The different female counter-strategies have a great deal to do with how vulnerable females are to male aggression and how often male aggression will happen.

Orangutans are good studies because they're the only nonhuman primate where forced copulations happen and also females travel alone- they have no other females to ally with, and no males to defend them. Smuts thinks this is why they're coerced; they have no protection.

Further evidence comes from a comparison of chimps and pygmy chimps, and exemplifies why social organization is an important factor.
Chimps are male-bonded. The males form coalitions against males from neighboring communities. Males groom frequently, and they reconcile one another after a fight much more than females do. The closest bond in chimps is males. Females are like 85% the size of males- large females are about the size of small males, and males' teeth aren't that much larger, so sexual dimorphism doesn't do much to explain male dominance over females. However, females invariably pant grunt to males and they don't fight back when males attack them. (Signs of submission)

Contrast with this the pygmy chimps. They also have a social system where males stay and females disperse. They show just as much sexual dimorphism. Within groups, however, social relations are really different. The closest bonds by far are among adult females who are unrelated. Not only do they spend more time together and groom each other, but they have frequent intense sexual interactions. This is called GG rubbing, and it's when females rub their sexual swellings together. Researchers are pretty sure that the females reach orgasm in these homosexual relations as well as their heterosexual ones. This behavior is common in the wild; when they find a tree, before they eat, they all have sex together and then eat. It has been hypothesized that this sex is to keep the bonds close so that females can dominate the males. It has been particularly documented by Amy Parrish, studying bonobos in captivity. In 100s of hours, she never saw male aggression on females, but repeatedly saw females attacking males or inflicting wounds on them. No one has ever seen male coercion in bonobos.

So, the bonding and coalitions between females function to shift the balance of power, protecting them against male coercion.

What evolutionary basis is there for rape and sexual assault in humans?

When she wondered about this and went to look at the literature, she found articles comparing insect behavior to humans... Not much help.

She has found some social variables that might correlate. The Yanamano people are some of the most aggressive primitive people. They are patrilineal and people have documented very severe incidents of male aggression against females, usually because of suspected adultery.

Contrast a society of pygmies in central Africa. They're traditional hunter/gatherers where men and women gather together and the males do a lot of child-care, more than in many 'advanced' societies. Anthropologists have never seen a man lift a hand against a woman in this culture.


There's a huge difference between cultures. Women are more vulnerable to coercion if they don't have close social bonds with female kin, or if they don't have female friends, or if they don't have the protection of a male.

This comparative perspective can help us think about such a difficult issue as sexual coercion in humans and it's not a case of 'oh it's built in and males are just going to do it.' We should pay attention instead to how social bonds affect things.

Friday, November 15 -- Social Relationships: Adults and Infants

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This is the theme for the next three lectures- including parent-offspring conflict and infanticide. See Primate Societies book in ch 27, 28 for more articles on this topic.

We've touched on some things about adult-infant contacts; remember Hamilton's rule: rB>C. This is the basic theoretical framework for understanding why an adult should ever take care of any infant. We've also seen how maximizing inclusive fitness explains males taking care of infants in cooperative polyandry, we've also seen male relations with infants in baboons- part of mating effort really, not parenting effort. We've also spoken of adult females and infants in the context of allomothers.

Adult females and infants

Most of the interaction that goes on between adults and infants and that is between infants and mothers. Any parental care by males is an exception to the general rule- in mammals, and particularly in primates, males don't take care of the kids. Remember that females spend a disproportional portion of their lives taking care of their infants. See the overhead about baboon lifecycles.

Variations in mother-infant relations: Maternal styles in baboons People really think it's interesting, the variation between individuals in this relationship between moms and infants. Some of the best studies are from savannah baboons. Especially the yellow baboon- mostly by Jean Altmann, who also wrote our coursepack article. She basically found that there were two types of mothers: permissive and restrictive mothers.

Permissive mothers stop restraining their infants at a younger age than restrictive mothers- when the infants are small, the mother is manly responsible for keeping the infant with her, grabbing him if he wanders off. At some point, the mom stops grabbing it and it's the infant's responsibility to keep up. Permissive mothers stop grabbing their wandering babies at about .5 months vs. 2.25 months for restrictive mothers.

Permissive mothers stop following their infants earlier than restrictive mothers. Early in life, mom is responsible for keeping the pair together, but later on the infant maintains responsibility. Permissive mothers stop following their kids at around 1mo vs. 3.25 months for the restrictive mothers. (This is using the Heinz index of approaches vs leaves to determine who is doing the work of maintaining the proximity.)

Anything else you look at, such as rejection of nursing or refusals to carry, happens earlier in permissive mothers than in restrictive mothers.

Relationship between maternal style and rank
It turns out that permissive mothers tend to be higher ranking than restrictive mothers. Permissive mother's rank in her group was an average of 6, while restrictive mothers' average rank was about 11- much lower. It's not too clear why this is- could it be that he high-ranking mothers are more secure that their kids'll be safe since they're high-ranking? But nothing people have come up with has seemed to work perfectly- for instance, in macaques it's the opposite.

Evolutionary consequences for mothers and infants
One result is that permissive moms wean their infants earlier. So, because permissive mothers stop lactating earlier, you might think they have a reproductive advantage because they could conceive sooner. However, this does not translate into a reproductive advantage, because permissive mothers do not show shorter birth cycles than restrictive mothers; the former take more cycles to conceive than the latter.

Some evidence suggests that restrictive motherhood increases infant survival. Ill health and infant death occurred at a slightly higher rate among infants of permissive mothers (5 of 7; 71%) than among those of restrictive mothers (2 of 5; 40%). Note from the small sample sizes that these aren't statistically significant.

So, given a choice of mothering style, why would mothers pick a more permissive mothering style if it increases their kids' mortality? We'll devote a whole lecture to this in the lecture on parent-offspring conflict, later on.

Adult males and infants

In a lot of species there 's a lot of interactions between males and infants in some species. These are categorized as:

Intensive caretaking
The male does a lot of parenting, such as in the callitrichids. In monogamous species, males are also doing a lot of carrying and protecting. Males should be sure of paternity to benefit from taking care of infants, so it's usually monogamous species like aotus, the night monkey. Most monogamous species have intensive care from the dads.

The male forms social bonds with the infant; they interact sometimes, playing together or maybe sharing food. You see these types of interactions in black howlers, baboons, and gorillas.

The male and infant don't have much interaction. This is most common in solitary species, such as orangutans. Males show no attractions to infants. They don't seek them out, but don't avoid them either.

A controversial aspect of male relations with infants- Triadic interactions

This is when there are three parties involved; two adult males and one baby. When there is a conflict between two males, sometimes one of them will pick up an infant.

This was first documented in barbary macaques. They're noted for males doing a lot of infant carrying and holding, but it was particularly Deag and Crook who noticed that males were particularly likely to pick up and carry a baby when they were in a conflict with another male. There are two hypotheses to explain this behavior.

Agonistic buffering hypothesis
The holder is using the baby to protect himself from the other male, who doesn't want to risk hurting the baby because then all the female baboons will get on his case.

Parental care hypothesis
This was suggested by Busse and Hamilton. When studying chacma baboons, they noticed that infants are most often picked up by a long-term resident male, while the male he's having the conflict with is usually a recent immigrant. They guessed that it might be a form of parental care- the holder could possibly be a father of the infant and he is protecting it from the other possibly infanticidal male; so it's a form of parental care by the males.

Evidence and predictions-- Agonistic buffering

Males who carry infants receive less aggression than males who don't carry infants.
  • Among the baboons at Gombe, a male was less likely to be threatened by another male when he was carrying an infant than when he was not carrying an infant. (20 of 22 dyads (91%))
  • In a study of captive bonnet macaques, 6 of 7 males were harassed by other males less often when holding an infant than when engaged in other activities. (Silk and Samuels did this study.)

Another prediction is that the male who is the recipient of the behavior (i.e. the one who is not carrying the infant) should be the father of the infant- the infant is being used like a hostage against him- but no one has found evidence of this.

So, a correlation has been shown, but causation has not. In other words, maybe because he is holding infant he is not attacked, but it also could be that when he is holding the infant, he is trying harder not to provoke an attack since he is supposed to be protecting it.

Evidence and predictions-- Parental care

Male carrier is a probable father, while recipient is not a probable father.
(Remember that males often carry their friend's babies- also remember that a lot of the time, males are likely to be the father of their friend's babies.)
  • Among chacma baboons, male carriers were high-ranking during the time at which the carried infants were conceived, and were therefore probable fathers.
  • In contrast, most recipient males were not in the group when carried infants were conceived (42 of 45 infant-recipient combinations). This is particularly interesting because recent immigrants or males who have just recently reached high rank are the ones who are the most likely to practice infanticide- so they are potentially threatening to the infants.
  • Male barbary macaques frequently care for infants. Recent genetic studies indicate that males do not show preferential treatment to their own infants. They found no particular correlation between care and paternity. This may indicate that the researchers knew more about paternity than the monkeys themselves did. Remember that mating is fairly promiscuous in barbary macaques so the males wouldn't have a lot of information available to guess which infants were their own.

Discussion --

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Today we turned in a paper, got back a paper, got a take-home quiz, and reviewed the previous three lectures.

Let me know your thoughts:
Last modified: November, 1996