Sex, reproduction, parenting in the evolution of primates

Figure 1. Fundamentals in the evolution of primates

Each one of us is result of a complex synergy among these and other variables. Our differences result from differences in our genetic information, personal experiences, and importantly for these factors -- small differences in hormones and other biochemical factors.

1. Evolution: Variation and selection

the functions of sex

sex creates variation

immunity against microorganisms

Variation of course is necessary for the diversity of life; imagine the effect of a viral epidemic on a cloned population where everyone has identical genetic makeup.

new niches - new species

Similarly, variation enables occupation and creation of new niches and ultimately new species.

repair DNA

Another important function of sexual reproduction may be the redundancy of genetic material in each cell due to the two copies, one from each parent. Damage to DNA may not result in loss of crucial information.

non-reproductive functions of sex

This is certainly a recent development in primates but obviously important in bonobos and humans.

sexual selection

Darwin suggested there were actually at least two selective forces--natural selection and "sexual selection."
"This depends on the advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction. p.256...It is certain that with almost all animals there is a struggle between the males for the possession of the female...hence the females, supposing that their mental capacity sufficed for the exertion of a choice, could select one out of several males. 259."[1]
This can lead to a genetic contest among males to develop the most attractive behaviors, plumage, and whatever to attract the favor of females of their species --developments that may have no other virtue and even be potentially maladaptive on other dimensions, e.g. the peacocks tail.
This intra-sex competition is one aspect of sexual selection; the other is the basis for the "female choice" in selecting one male over another who is competing for her attention. This leads to a complex interacting process. As Small (1993) puts it: "males have a trait, females like it and mate with them. females then have sons with the trait and daughters with the preference. The trait and the preferences are inherited together over and over, coevolving with each other. p.93"

Figure 2

Figure 2

Genes survive by constructing phenotypes which reproduce those genes and are not "filtered" out by chance or inability to adapt to environmental circumstances. Any gene contributes positive and negative effects, depending on circumstances, to its phenotype's success in reproducing that gene.
See "evolution notes" for more details.

2. Sexual differentiation

differences in form suggest differences in function

Previously we have seen this the case for everything from neurons to forelimbs. Even sperm cells carrying male or female chromosomes look different; the females are larger and somewhat slower moving.

mammalian sexual differentiation

all primates are built on same basic plan

Keep in mind that all primates, both sexes, are built on the same basic body plan. Variations are largely due to differential timing of growth patterns, extending some dimensions, shortening or inhibiting others by genetically regulated hormones. These include androgens, estrogens and other female hormones, as well as the important human Growth Hormone (hGH).[2]
It is worth noting that these hormones are instrumental in body "construction" as well as mediating differences in behavior. Both sexes respond, although differently, to the same hormones.

so are females and males of the same species

Despite differences in function and anatomy; males and females share a common anatomical plan. Just as species are variants of that plan, so are the two sexes of each species variants of the species "plan."

two paths to sexual maturity: M & F

All mammals follow similar paths in developing the males and females of a species. The process starts with a male or female chromosome-bearing sperm cell fertilizing an egg cell, which triggers of a chain of events that builds a male or female body governed by hormone levels. The resulting body and its pre- and post-natal interactions determine the individual's behavior.
(See detailed notes.)

two questions: Species differences? Sex differences?

primate sexual dimorphism

How do male and female primates differ from each other? What significance should be attributed to differences in overall body size or breast, penis, and testicle size? Even more interesting perhaps, how do the behavioral differences between the sexes emerge and contribute to the evolution of the species?

contemporary apes

(review these differences in size, shape, and behaviors)

hominid dimorphism

Fossil remains indicate declining differences in body size and teeth and as brain size increased. This suggests, perhaps, that competition among males declined and closer interpersonal relationships between males and females developed. Both males and females were reduced in size; males more so than females. (Borgognini Tarli and Repetto (1997) in Morbeck et al (1997).
These differences are due to differing growth rates; males being slower and reaching maturity later.(Actually measuring these differences is not trivial due to allometry and subgroup variation.)

primate sexual differentiation

How do the male and female primates of the various species differ from one species to the next?


With the very important exceptions of humans and bonobos, female primates primarily mate when they are fertile, within a short period around ovulation.
(The female primate reproductive cycle is a pattern of ovulation, mating, and menstruation if fertilization does not occur. Only a few species -- including chimps and humans -- show traces of external bleeding during menstruation. Estrus refers to a short period, generally around ovulation, when the female is receptive to or even actively soliciting copulation.)

overt indicators of ovulation

Female NHPs typically signal when they might be interested in mating with visual, behavioral, and/or olfactory cues. While common chimps and to a lesser extent, bonobos have flamboyant pink swellings indicating estrus, most female primates have little or no swelling. Only 22 of over 200 species have these swellings --many of them macaques and baboons, as well as the chimpanzees. (Small, 1993).
Even in common chimps, some copulation may occur outside of the estrus period.

concealed ovulation

Gibbons, orangutans, and gorillas have only very marginal visual changes, unlikely to be of much significance. Humans have none and may engage in intercourse more or less anytime.


(hair, face, breasts, lips, behavior, etc.?)


genital size

(hair, face, muscles, height, etc.?)

function of differentiation

The obvious function is to better pass on the genes of the participants! Humans, while not greatly different in size, have specialized their reproductive processes for great efficiency, enabling reproductive rates two to four times that of our large ape cousins.
(Note here and below synergistic factors here of extreme neonatal immaturity, MPI and food provision, nursing and fertility, loss of hair, etc.)

3. Parental investment

the idea of "investment" and reproductive "strategies"

reproductive "strategies"

reproductive rates

The large apes are characterized by single births, slow weaning and maturation, with extensive maternal care invested in each offspring.

Primate life history data

(See table 8.1 overhead for apes).

the !kung

Group size of 40-60, 4.7 children, 44.1 birth interval, suckling frequent and an important part of diet until 3. Compared to urban women, they have 15 years suppressed ovulation while nursing vs little or none?, later menstuation and earlier menopause and fewer menstrual cycles -- compared with 35 years of menstrual cycling in urban females today.

maturation of offspring

Young apes in the wild may become sexually mature in eight to ten years. A female chimpanzee may have her first infant somewhere between 13 and 15 years; considerably sooner in captivity where diet and body weight may speed up maturation.

female parental investment

mate choice

Because females invest so much more in their offspring (see below) than males, it is usually argued that they must be extremely careful in mate selection if they are to succeed in passing on their genes[3]. They need to get both quality genes and when relevant, protection and resources for themselves and adequate male parental care.
(Males in contrast with many cheap sperm to spread around, have no need to exercise such care. Darwin seems not to have considered this specific point (Trivers, 1972)).
In primates females exercise varying degrees of choice including making sexual advances, responding to some males but not others, and in species like humans and bonobos, maintaining sexual relationships beyond their periods of fertility. Small (1993) suggests, however, that the reality may be somewhat different in that female NHPs may --like some human females -- mate simply for pleasure or other non-reproductive reasons.
She points out that female-female sexual interactions are somewhat common, especially among bonobos, and these cannot be reproductive in nature. Some serve a bonding function; others perhaps just a result of hormonal motivation. (p.146).
"the human female is encumbered to an extent not seen in other species. Because of the extremely dependent state in which young are born and because of their slow development.....the human mother must continue to invest high levels of parental care in several young simulataneously....she adds to her encumberment and goes farther and farther into "debt" in the sense as her dependents multiply, but her physical reservior of energies remains the same....nearly all human groups attempt to regulate access to the reproductive capabilities of women by designating a mate (husband) and making him and hiskin share in the work of rearing or defending the children. (p. 226 Draper (1997) in Morbeck et al, 1997)


The duration varies somewhat among the large primates, eg. 7 months for chimpanzees, 9 for humans.


Nutrition demands double when nursing.
A reduction in suckling is primarily responsible for the restoration of ovulation sometime after birth.

care of offspring

male parental investment

This is contribution of sperm and seeking a mate at the minimum -- providing protection, food, and child care resources at the maximum.

primate species overview

early maternal care

attachment and implications


acquiring appropriate behaviors & values

In most nonhuman primates this is largely a maternal function.

food, dangers, sexual/social behavior

infant care behavior for young females

learning basic skills

Language in humans, food skills in non-human primates are obvious examples.

4. Competition, aggression, and cooperation and dominance


Probably all primate groups, including humans, have "dominance" -- high status with certain privileges, e.g. preferential access to food, mates, etc. Dominance may be inherited or acquired due to size or other characteristics. Physical aggression may play a role but is not the driving force in primates.

dominance and fitness

Pusey, Williams, and Goodall (199x) show that female chimpanzees in Gombe National Park, Tanzania, vary in their fitness and that fitness is correlated with dominance. If it seems odd that it has taken 37 years for Jane Goodall's Gombe studies to yield data on female reproductive success, consider that the chimpanzee social community contains only 10 to 15 females at any one time, with a mean interbirth interval of 5 years between surviving offspring. Half of the breeding females are immigrants, often of unknown age. Many females meet each other rarely, and even then clear-cut dominance interactions are infrequent, so that it can take several years for observers to detect the dominance relationship of any given pair. But by indexing the dominance ranking of the females over 2-year periods, Pusey et al. found that status correlated with at least three measures of fitness for breeding females. (from the Wrangham, 1998 Science paper)
(See aggression notes)

5. Social structures and mating

(See Table 2.2 in Bard (1995 "Parenting...")

formation of groups and regulation of inbreeding

Each species has its own practices in forming groups. Generally either the females or the males of the species leave their birth group when they become sexually mature. Females gorillas and chimps leave "home" and fall in with another group. The males orangs and gorillas typically must establish their own group. All these practices function to increase genetic variability in the populations.

reproductive factors

In addition to the need to prevent excessive inbreeding, social structure of groups probably reflects individual species reproductive adaptations. Male gorillas, for example, may not compete like chimps in sperm production but do quite well in "hand to hand" combat!

role of food supply and preferences

Food resources are an important factor in group structure. For example, from one perspective orangs and gorillas have similar social structures except for the great distance between the individual females and the dominant male in orangs. This seems to be a result of availability of the preferred foods, easily obtained leaves and shoots for gorillas and widely dispersed fruits for orangs.

types of apparent mating systems

These may be reflected in the size differences between males and females.

monogamous (including serial monogamy)

one male -several female ("harem" )

many male-many females

the reality of mating systems

Despite the superficial structure observed in the various species, the actual breeding patterns remain somewhat unknown without an accurate account of paternity. This is only likely with DNA analysis or implausibly close and continuous observation. (See Small, 1993, for discussion.) Recent DNA studies of gibbons and monogamous birds have demonstrated a certain amount of infidelity exists. Very recent DNA studies of chimpanzee matings revealed that a certain percentage of offspring were fathered by males not in the group. See "Furtive matings.......")

the virtues of promiscuity

the "Coolidge effect" (Small, 1993, p.179)
"More than any other variables that stand out to our human eyes, novelty and variety, appear to be the preferences of female nonhuman primates...183"

chimpanzee consortships

There are varied opinions on the importance of these temporary pair-bonds between a female in estrous and a male of her group. They appear to increase chances of a male's fertilizing a female as he can more or less control access to her around ovulation. DNA studies are necessary to confirm this.

dominance and rank

Theoretically females might want to mate with high ranking males, both for their presumably "quality genes" as well as protection and in some cases, increased sharing of resources. However the evidence is mixed. (Small, 1993).

reflects needs of females and available resources

good fathering skills?

This seems like a good idea but there's not much evidence for any species.

male dominance and aggression

W&P summarize three patterns of male violence in each of orang, gorilla, and chimp societies. These are not random acts of violence, but specific patterns that make sense in the particular social context and further the genetic interests of the violent males.


Fertilization or dominance? "The life histories of gorillas - and bonobos that rape is not inevitable if you are an ape. (Wrangham & Peterson, 1996, p.142)

"safety in numbers"

Perhaps the best predictor of violence toward a primate is the number he or she is traveling with at the moment.

sexual coercion

"In a typical interaction, he (a young adult male chimp) might charge at the female, hit her, kick her, pull her.. jump on top of her huddled and screaming form, slap her, lift her and slam her to the ground, and charge off again. This never becomes the all-out sort of wild gang violence directed against ... other communities. The female is not killed, rarely injured. W&P 143"
Goodall notes that male chimps are not very "nice" to females and that unless he old or crippled, a male can always coerce a female in copulating with him.
There are some scenes of intimidation in the Family of Chimps video at the Arnhem Zoo.


Infantcide is a part of a number of species typical behavior --including humans in some cultures. In humans it occurs deliberately with unwanted children, often females. It may occur less obviously in extreme child abuse that may have more commonality with gorilla infantcide.
W&P estimate 1 of 7 gorilla infants is killed by adult males; most of these unprotected by a silverback (in all likelihood the infant's father). By killing infants, males that take over a group put the females into a new reproductive cycle and further their own genetic advantage by impregnating them.
More surprising, are cases where the father silverback successfully defends himself but the invading male kills one of the infants. W&P report that this may serve to draw the mother of the slain infant to the killer!
"When another male does break through the defenses and kills her infant, she responds in a way that violates all our assumptions about attachment, loss, and revenge. It may take a few days before the female leaves her troop, but the evidence is clear. Infantcide draws a female to a male. She leaves her old mate and joins the killer....The female's choice is imposed by the logic of violence, by the threat to her next infant. 151"

primate intelligence

"The hugs and kisses and embraces of the apes are as elaborate as their use of brute force...Intelligence turns affection into love and aggression into punishment and control. WP, p.152."

"why are human males given to vicious lethal aggression?"

WP answer their rhetorical question as follows:
"...the curse stems from our species own special party-gang[4] traits: coalitionary bonds among males, male domination over an expandable territory, and a variable party size. The combination of these traits means that killing a neighboring male is usually worthwhile, and can often be done safely. 167"

"Why are bonobos so different?"

Bonobos are only about 2 million years separated from the common chimps and bear a number of even closer morphological and behavioral similarities to humans. Yet they apparently have little of the violent aggression common to their other cousins: orangs, gorillas, chimps, and humans.

females and food supply

W&P offer a complex explanation for this unique species.
"Females form the core of bonobo parties, so that in small parties there are more females than males.. Females spend their time closer to each other than males do. Females are more likely to be in the center of the party, with males on the outside. And they form alliances that effectively protect them against male aggression. 227"
This development was made possible, in their theory, by a cool drought some 2.5 million years ago, driving gorillas out of a small region around the Zaire river. When the drought ended, the herbs that are the primary diet of gorillas returned and local chimps adapted to that diet. Without competition from gorillas, they prospered and no longer had to forage in small groups as did their recent ancestors and today's chimps. Traveling together in large parties, the arboreal bonobos, male and female, were able to protect themselves from violent aggression from their own males.
One might speculate that sexuality and neotenous characteristics of bonobos evolved in response to these circumstances, while the violent traits were submerged --perhaps a simple adjustment in hormones and neurotransmitters as the more violent males were filtered out. This would be quite an achievement, though, since aggression is such a successful reproductive strategy.

bonobos are relatively neotenous

Even though bonobos are not closer genetically to humans than chimpanzees, they may share more characteristics because of their neoteny which may influence everything from bipedal ability to face to face sexual intercourse. (See Gould, 1977 for characteristics of humans perhaps neotenous.)

human sexual behavior

sexual activity is more than reproductive

culture is extremely important

This may work in curious ways -- even modifying hormone levels.

interpersonal bonds and MPI are high

knowing paternity is very important

evolutionary background and relation to our primate relatives is largely speculative fantasy

no consistent patterns

Many cultures have been polygamous; many nominally monogamous. Yet fidelity is varied and alternatives are commonplace.

however, powerful males may father 100s of children

Polygamy was widespread in early historical times and probably before. Financial resources remain important considerations for both males and females in regard children.

What types of mates to humans prefer?

Buss' research

Males everywhere prefer "attractive" younger women and females prefer "older" men with resources. (No kidding!) (See his BBS article.)

Ask Beth! (5/02/97

"Why are tough guys popular? Most of the guys ..."

female choice?

"On theoretical grounds, it is clear that dominating mechanisms -- whether aggressive or non aggressive in form -- would have evolutionary advantage in helping an individual acquire valued resources, especially in competition for mates. This is not simply a matter of a dominant man taking what he wants; women regard men who look dominant as attractive (Townsend 1993). Teenage men rated by naive judges as having "dominant looking" faces (often with prominent chins, heavy brow ridges, muscular rather than fleshy or skinny faces) report copulating earlier than their submissive-looking peers, presumably in part because they have an easier time finding willing partners (Mazur et al. 1997). "
(Perhaps not coincidentally, these characteristics are also consequences of taking hGH to enhance athletic performance.)

It is not obvious why there would be selective advantage in aggressiveness per se, apart from its dominating function.

Random Sex-related life-style factoids

signalling ovulation and receptivity

Females of at least 20 of 200 primate species signal ovulation by rear-end swellings and skin color changes, oflactory cues, or specific behavioral gestures.
Only chimps, among apes, have obvious swellings. The bonobos are apparently permanently "swollen" and (continuously, 3 of 4 days? See de Waal plot.) receptive to sex unlike the common chimp female who may be receptive 10-15 days each cycle.
Small (1993) following Hrdy & Whitten, 1987) notes that chimps may NOT be such a good model for human female sexual behavior and that contrary to lots of conjecture, human ancestors may have NEVER had overt sexual swellings as do chimps. p. 129
Gorillas (1-4 days)
Orangutan (5-6 days)

resumption of cycle

This probably depends on nursing patterns and diet of both mother and infant. Chimps and gorillas may resume in 3-4 years; bonobos much sooner and orangs longer. See Eliason reading for humans where it clearly depends on nursing patterns.

differing fates of M and F

In many primate species, female infants stay with their mother and in her group, while males leave or are forced out. In others the reverse is true; chimp females for example, generally leave the natal (birth) group. Gorilla young of both sexes typically leave their natal group.

social-sexual arrangements vary by species

(see overhead from deWaal (1995) Sci. Am.)
The apes certainly illustrate this; each species has a different arrangement. Even among a given species there may be variation. For example gorillas are described as having a haren arrangement, yet in 40% another younger male--often the brother or son of the silverback-- may mate with the 6 to 8 females of the "harem."
Mating behavior itself is extremely variable; gorillas copulate infrequently with a copulation lasting 80 seconds while female bonobos mate continuously and engage in lots of sex activity, including homosexual, as a means of gaining food and forming alliances.
Orangs present another system altogether (though it may be seen as a wide-ranging harem in which the females are not in contact.)
Female chimpanzees come into estrus once a month. They have a 35-day menstrual cycle and can breed at anytime of the year. The gestation period is more than seven months long, and a single offspring is produced.

function of orgasm

Small (1993) argues "orgasm for human females is the necessary feature of our reproductive biology which evolved to to take the place of estrus...anticipated pleasure for BOTH sexes is most likely an initiator to begin mating behavior. p.148"

on what basis do female NHPs "choose" mates?

While size, dominance, fathering skills may play a role in a given species, the evidence is sparse that this really matters in general. Small (1993) summarizes research on rhesus monkeys--the best studied primate--and reports the females prefer a variety of mates, especially outsiders, new to their group. This of course is a natural protection against excessive inbreeding. "Their interest in novelty, therefore, might be a primitive urge to find mates lurking at the periphery of their group with genes different, but not completely different from their own. p.171" Thus choice on this basis increases the genetic diversity of the species, hence its overall fitness. (Of course this may not always be a virtue if successful adaptations are LOST; cf role of birdsong dialects)
A variety of mates with a promiscuous female also ensures that enough sperm are available at the moment of ovulation, since repeated matings with the same male will not provide the same number of sperm each mating.
Small says, while these are speculative explanations, they "pull these females out of the negative light of promiscuous sex-crazed harlots into the arena of strategizing creatures trying to improve their individual reproductive success. p.182"
Small suggests the wild orangs support her idea that in general female nonhuman primates show a preference for fully mature, sexually able males by resisting efforts by younger males to mate with them. p.155
"Status, hierarchies, and rank are certainly part of our primate heritage, but unlike ourselves, nonhuman female primates seem to focus less on status then we do. A fancy car won't do a male ape much good.....p.160"
Much of this fits with the recent findings based on DNA analysis of chimp infants (Furtive mating...1997). Females to a certain extent bear offspring of males NOT in the group, presumably of their "choice."

sex in our closest relatives--chimps & bonobos

Male chimps are usually unkind to females and Goodall suggests females prefer the "nicer" males.
"Bonobos have sex more often and in more combinations than most people of any culture, and most of the time bonobo sex has nothing to do with reproduction. p.175"
de Waal relates many instances of tension reduction apparently the primary function of a sexual encounter. Generally these involve genital stimulation but apparently no orgasm or ejaculation.

declining human sperm counts?

ideas (beliefs) as tools

(Another way to look at this is to treat ideas as shaping the brain along with other such factors as genes, nutrition, hormones, etc. Note the parallel with language.)

beliefs about sex differences

the dilemma: a self-fulfilling prophecy regarding differences

human sexual/social practice

prematurity, nursing and diet, MPI, and reproductive rates

These all act synergistically in human evolution; for example nutrition speeds up sexual maturity hence reproductive rate.

lactation demands

A normal 2000 calorie woman requires double that when nursing.

Fisher's "Anatomy of Love" Norton: 1992

Virtually all humans have a marriage ritual in which men tend to marry one woman at a time.
"Female humans, like chimpanzees, tend to initiate sexual activity", e.g. 2/3 of pickups in bars! Compare with studies of captive chimps showing 85% of sexual acts initiated by females.
Adultery is widespread.
"Marriage has a cross-cultural pattern of decay. 112"
"The human animal seems built to court, to fall in love, and to marry one person at a time; then, at the height of our reproductive years, often with a single child, we divorce; then a few years later, we remarry once again."
She attributes pair-bonding to need for successful raising of infants. "What made me think of this was a remarkable correlation between the length of human infancy in traditional societies, about four years, and the length of many marriages, about four years. .153" (high mobility, weaning of young).
(She gives a lot of caveats on the generality of these comments immediately afterward!)

Buss's "evolutionary psychology" of mating

David Buss has summarized cross-cultural evidence on human mate choice and preferences. Some (not surprising) findings are:

woman value resources in mates

infidelity in women major cause of divorce

selectivity increases for both in offspring context

males value younger attractive women

[1]Of course it can be that a certain trait like "size" is ambigous --possibly selected for by female choice or as result of male-male competition. Only observation can determine if there is extensive male competition. (See Boinsky, 1987).
[2]This hormone, hGH, has recently been synthesized and is used to enhance athletic performance, with some negative consequences. "The hormone of the moment, hGH, can cause disfigurement by encouraging growth not only of muscles but also of bones, especially in the feet, hands and face. Some hGH users develop jutting foreheads, prominent cheekbones and an elongated jaw. (In Olympic circles an athelete with a pronounced jaw is sometimes said to have a hGH jaw. (Sports Illustrated, p. 70, April 14, 1997).
[3]Obviously females have no direct way to assess genes other than indirectly through signs of health and relevant skills and possession of resources.
[4]Their definition of "party-gang" species are those species in which there are "parties"--as in war parties -- or temporary groups, from lone individuals to an entire community. Chimps probably are the prototype here, varying from 10 or less to 20 or more. The coalitionary bonds refer to the relationships among the same-sexed adults used in aggression against others of the same species, usually same sexed. See W&P p. 165.