This is the fourth part on the evolution of human mating behavior, comparing evidence for promiscuity and pair-bonding in our species. Please see the introduction here.
We left off with a list of eight traits in humans suggesting promiscuity in humans. Admittedly, the previous post was a little thick, as it dealt with imprinted genes and population genetics. The current one concerns human reproductive physiological and anatomical traits consistent with a multiple-partner mating structure, building on a couple of points addressed by Ryan and Jethá in their book. If you’re paying attention, that’s three posts concerning promiscuity and one (yet-to-be-written) on pair-bonding. Perhaps it seems I’m stacking the deck, but please reserve judgment. One reason more space is needed to make the case for the evolution of promiscuity is that the biology is less well known, and more effort is needed to bring it into the light. That single post on pair-bonding will be an important one, and quality matters just as much as quantity.
Continuing on with our list of traits hinting at promiscuity…
9. Sexual dimorphism in body size. This point remains somewhat contentious. In the majority of anthropoid species (monkeys, apes, and humans), males are the larger sex, with the degree of dimorphism ranging from slight to extreme (Plavcan 2001). This pattern correlates strongly with mating structure and male-male competition (Plavcan and van Schaik 1997). For monogamous species like gibbons, males and females tend to be roughly the same size. In species where females prefer larger males or where males compete for access to females, bigger males will leave behind more descendants. This is true for polygynous gorillas and dispersed, territorial orangutans, where males are physically about twice as large as females. A good non-primate example is elephant seals. On the other hand are horseshoe crabs, where smaller males cling to the backs of larger females and wait for the release of her eggs. This ‘reverse dimorphism’ is found in a few primates, but is slight and only in some prosimians such as lorises and lemurs.
In humans, the degree of dimorphism varies by population and whether one is looking at height, weight, or some other variable. For height, males are about 5 to 10% taller than females on average, though in populations where women contribute more to food production they tend to be closer in height to men, suggesting that social status and better nutrition are also critical factors (Holden and Mace 1999). Whether a population has a polygynous or monogamous marital system does not seem to predict height dimorphism. For weight, Turkana pastoralist men are only 5% heavier than women on average; in the United States, Netherlands, and Japan, that figure is about 20-25% (data from Little et al 1983; Bogin, 1999). It is tempting to think that because dimorphism in humans is nowhere near the extreme degree found in gorillas or orangutans, it points to generally monogamous mating in our evolution, with perhaps some slight polygyny. However, while a high degree of dimorphism is indicative of polygyny, it does not automatically follow that low dimorphism implies monogamy, polyandry or low male-male competition (Lawler 2009). And, as Ryan and Jethá remind us, the range of dimorphism seen in humans is within the range found in multi-male/multi-female chimpanzees and bonobos (15-20%).
They contend that this is overlooked for a couple of reasons. One is that it is often forgotten that reproductive competition among males is not limited to aggression, territoriality, or female mate preference, but may also take place post-copulation within the female reproductive tract through sperm competition. However, sperm competition can only occur if females copulate with more than one male in a relatively short time period, and that notion of female sexual assertiveness defies the culturally accepted view of females as demure and coy. To Ryan and Jethá, we have a cultural blind spot that predisposes us to consider monogamy or polygyny the only possible human mating strategies because they are more compatible with the image of males as sexually forward and females as reticent. This in turn causes us to overlook the possibility that we likely shared the more promiscuous behaviors found in both of our closest primate cousins.
It is also possible that this blind spot is partly attributable to parental investment theory and the (generally correct) observation that males have more to gain in terms of genetic fitness from having multiple partners due to differences between gametes and gestation. Here’s an example of this logic:
The fact that males produce numerous and cheap sperm, while females produce few and expensive eggs, has two important consequences. First, … a male may potentially fertilize many females, whereas females are limited by the number of eggs, and thus offspring, that they can produce and raise. Males, thus, will benefit by trying to fertilize as many females as possible, and will compete for access to reproductive females. In contrast, females will benefit by mating with the best mate possible.” (Mills et al, 2010: 544).
However, it can’t be that simple, or every sexually reproducing species would have the same basic reproductive behavior, and Dr. Tatiana would then be out of a job. Certainly, having multiple partners can benefit females too. In Meredith Small’s words: “the most striking feature of female primate sexuality is the consistent orientation toward novelty and variation, sometimes to the point of promiscuity” (1993:176). She cites several possible advantages of sexual novelty and promiscuity for female primates, including strengthening social bonds, being better able to evaluate male quality through experience, preventing infanticide by males by confusing paternity, and avoiding inbreeding. Another benefit might be potential paternal care from multiple males. Additionally, a female may mate with multiple males simply to increase the odds of conception because, as Small phrases it: “primate males, both human and nonhuman, can’t mate time and time again in succession. They need time off. And this vacation might be frustrating to a female monkey in heat” (p. 179). For a female primate, the window of opportunity for pregnancy may be brief, and an individual male might not be able to get the job done. Is any of this relevant to humans? Possibly.
10. Reproductive Physiology. Human sperm count averages somewhere between 280 and 480 million per ejaculate, and is closer to that of chimps and bonobos (603) than to orangutans (67) or gorillas (51) (Ryan and Jethá, p. 230)1. This is consistent with an evolutionary scenario of human multimale/multifemale mating, and selection for higher counts via sperm competition.2 Why should this be?
In species where females mate with a single male (i.e., monogamy, polygyny, or dispersed), the effect of natural selection on sperm counts is relaxed. This is seen most readily in the bizarre example of seahorses and pipefish, where a female leaves her eggs in the male’s brood pouch, and the chance of fertilization by another male is nil. As a result, sperm counts are “vanishingly low” in these species, as it would be a waste of resources to produce more than is necessary (Judson, 2002: 23). At the other extreme is the highly promiscuous Australian fairy-wren, where females copulate with many males, who in turn are able to produce 8.3 billion (yes, billion with a ‘B’) sperm per ejaculate (Tuttle et al 1996). It helps to have multiple lottery tickets if there are many players involved.
Obviously, we are not fairy-wrens or pipefish. But we probably have more in common with the former, as well as chimpanzees and bonobos, at least in this regard. Consistent with this is the large, true scrotum found in humans, chimps and bonobos, but not in orangutans or gorillas. This places testes in a position susceptible to injury, but also facilitates sperm longevity by keeping them at lower temperatures (also see Smith, 1984). As Plavcan (2001:39) wrote: “there is overwhelming evidence that testicular volume, density of seminiferous tubules, and seminal vesicle size are greater in species with multimale mating systems, where females mate with more than one male.”
It is difficult to conceive of another reason that human males should produce more sperm than is needed for fertilization in a monogamous mating structure other than some form of sperm competition. It is true that human testes size and sperm counts are not on the order of magnitude found in chimpanzees or bonobos (or possibly woolly spider monkeys- see Milton 1985). But in chimpanzees, females have been observed to copulate as many as 50 times a day with a dozen different males, putting a premium on sperm competition (cited in Smith 1984: 82). Still, human sperm counts are well above that found in primates where females mate with only one male. There could be another more proximate explanation for this, though I’m just not aware of it.
Ryan and Jethá address other traits in human biology consistent with an evolutionary scenario of promiscuity, which I can’t cover in depth here. These include: the chemical contents of semen in split ejaculates3, the potential for multiple female orgasms and copulatory vocalizations (maybe), and the conspicuous size of penes and breasts in humans (both larger than in any other primate species). As a counter-argument, C. Owen Lovejoy referred to humans as “the most epigamically adorned primate,” with our exaggerated genitalia and secondary sexual characteristics, unusual body and facial hair patterning, and sex differences in body shape and fat patterning (1981:346). However, he felt that this was consistent with monogamous mating, as a pair-bond would be strengthened if both sexes were ornate and attractive to each other, rather than only one sex, as seen in lions, mandrills, peacocks, etc. It’s an interesting idea, and he did cite some evidence for this in male and female herons which both have ‘elaborate display plumes.’
But in the big picture, I think it is impossible to ignore the many traits in our biology that suggest strongly that lifetime monogamy does not come easily to humans.4 Theodosius Dobzhansky famously wrote that “nothing in biology makes sense except in the light of evolution.” What do we make of imprinted genes, promiscuity in chimpanzees and bonobos, multiple lifetime partners and infidelities across cultures, high sperm counts, results from population genetics hinting at polygyny, et cetera? This is not to say that biology is destiny (I wouldn’t be a very good anthropologist to suggest otherwise). But these things are a part of our biology, passed down over millions of years, and they can’t be swept under the rug. We also have the ability to love very deeply, and that has its own biological correlates. What we need is a more complex synthesis, incorporating both of these facts. Somebody smarter than me should do it.
A Musical Interlude. (Link)
Part 5, Pair-Bonding and Romantic Love. (Link)
1. These figures are generally consistent with those reported in a summary by Smith (1984), but reported a lower figure for humans (175 million per ejaculate). I imagine that like just about everything else in human biology, there is a wide range in human sperm count across individuals and populations. For example, Kate Clancy explained why there is so much variation in the menstrual cycle.
2. There are other forms of sperm competition than sheer numbers. In promiscuous fruit flies, males have evolved sperm that contain toxins that kill that of other males, often to the detriment of the female’s health and life expectancy (sperm with frickin’ laser beams on their heads). Closer to home, humans also seem to genetically resemble chimpanzees and bonobos for semen coagulation or ‘mating plugs,’ which could slow any subsequent male’s sperm from traveling through the female reproductive tract (see Eric M. Johnson’s post on this). Finally, as Ryan and Jethá discuss, the shape of the human penis, in particular its rather large size – compared to other primates – and the mushroom shaped glans, makes it particularly effective at displacing semen left by other males from the vaginal tract. Yes, people have tested this (via Jesse Bering). All for science. You should see what they do with ducks. Unbelievable. (Ed Yong).
3. Note: despite its putative beneficial effects never suggest semen as a Valentine’s gift, especially if you are the editor of an academic journal.
4. I thought Shmuley Boteach, commenting on Dan Savage’s NYTimes article on non-monogamy, made an astounding admission for a rabbi when he wrote: “Let’s be clear. Yes, monogamy is challenging and does not come naturally.” He had other important points to say about choices and responsibility, but still.
Bogin B. 1999. Patterns of Human Growth. Cambridge. (Link)
Holden C, Mace R. 1999. Sexual dimorphism in stature and women’s work: A phylogenetic cross-cultural analysis. American Journal of Physical Anthropology 110: 27-45. (Link)
Judson O. 2002. Dr. Tatiana’s Sex Advice to All Creation: The Definitive Guide to the Evolutionary Biology of Sex. Metropolitan Books. (Link)
Lawler RR. 2009. Monomorphism, male-male competition, and mechanisms of sexual dimorphism. Journal of Human Evolution. 57: 321-5.
Little MA, Galvin K, Mugambi M. 1983. Cross-sectional growth of nomadic Turkana pastoralists. Human Biology 55: 811-30.
Lovejoy OC. 1981. The origin of man. Science. 211(4480): 341-50.
Mills DS, Marchant-Forde JN, McGreevy PD (Eds). 2010. The Encyclopedia of Applied Animal Behaviour and Welfare. Oxfordshire: CABI. (Link)
Milton K. 1985. Mating patterns of woolly spider monkeys, Brachyteles arachnoids: implications for female choice. Behavioral Ecology and Sociobiology 17: 53-9. (Link)
Plavcan MJ. 2001. Sexual dimorphism in primate evolution. Yearbook of Physical Anthropology. 44: 25-53. (Link)
Plavcan MJ, van Schaik CP. 1997. Intrasexual competition and body weight dimorphism in anthropoid primates. American Journal of Physical Anthropology. 103: 37-68. (Link)
Ryan C, Jethá C. 2010. Sex at Dawn: The Prehistoric Origins of Modern Sexuality. Harper. (Link)
Small M. 1993. Female Choices: Sexual Behavior of Female Primates. Cornell.
Tuttle EM, Pruett-Jones S, Webster MS. 1996. Cloacal protuberances and extreme sperm production in Australian fairy-wrens. Proceedings of the Royal Society of London B 263: 1359-64. (Link)
When we wonder about female promiscuity, has anyone thought to ask a healthy ovulating woman? Good grief it seems very obvious that women back in these times probably mated with several males. Our culture has just told us we are horrible sluts if we have any sort of sex drive. Let’s do some studies on women’s sex drive from a positive female point of view, this shouldn’t be threatening to men. We are in this together 🙂
And, as Ryan and Jethá remind us, the range of dimorphism seen in humans is within the range found in multi-male/multi-female chimpanzees and bonobos (15-20%).
David Puts has argued (see “Beauty and the beast: mechanisms of sexual selection in humans”) that the difference in body fat between men and women means that the actual level of dimorphism is underestimated.
Copulatory vocalizations occur most often and are loudest with high-ranking males (and high-ranking females, in the case of female-female bonobo pairings). They also rarely result in decreased time between copulations. Both of these findings contradict the theory that vocalizations encourage sperm competition.
conspicuous size of penes and breasts in humans
Yet breast size is not found to be important in female sexual attractiveness across cultures.
These figures are generally consistent with those reported in a summary by Smith (1984), but reported a lower figure for humans (175 million per ejaculate).
The absolute numbers are probably not important, but variations are important if, as is done here, one is going to argue that humans are closer to chimps. The same is true for EMJ’s post that you linked. He writes that humans are closer to chimps on two semenogelin genes, yet according to the papers he links, humans are closer to chimps in the study of semenogelin I and closer to gorillas in the study of semenogelin II.
Finally, as Ryan and Jethá discuss, the shape of the human penis, in particular its rather large size – compared to other primates – and the mushroom shaped glans, makes it particularly effective at displacing semen left by other males from the vaginal tract. Yes, people have tested this
It has been tested using sex toys; it has not been tested on real people. That leaves some fairly weak evidence. There’s nothing showing this actually affects reproduction in humans. There’s no information on the variation between men. There’s the issue of female behavior. If sperm remains viable in the vagina for one to three hours and a “scooping” penis is only effective at removing semen from the vagina, then females have to be interested (that’s assuming female interest is relevant) in multiple copulations in that time frame.
Thank you for your comments. These are valid critiques, but I think that overall they are not fatal to the notion that our biology has some features that are indicative of some level of ancestral promiscuity.
On the matter of dimorphism, as mentioned above, it will depend on the variable measured (height, weight, body fat, lean body mass, etc), so there are many ways to carve up the data. Still, we are neither gorillas nor gibbons.
The rationale why sperm count would not be important is unclear to me.
It’s true that male preference for breast size is not consistent across cultures, but that is somewhat expected in that we are culturally and biologically variable species with behavioral flexibility. On the other hand, there is some evidence that breast size (and waist size) is correlated with female reproductive potential, as estimated by estradiol and progesterone levels (Jasienska et al 2004).
Click to access 15306344.pdf
Also, I think the viability of sperm in the female reproductive tract is on the order of days, rather than hours. That would widen the window of opportunity for having more than one partner and increase the plausibility of a sperm competition scenario.
These are valid critiques, but I think that overall they are not fatal to the notion that our biology has some features that are indicative of some level of ancestral promiscuity.
They weren’t intended to be. The question seems to be in what contexts humans engage in multiple matings, not whether they occur at all.
On the matter of dimorphism, as mentioned above, it will depend on the variable measured (height, weight, body fat, lean body mass, etc), so there are many ways to carve up the data.
There are different ways to analyze the data, and each way has its strengths and weaknesses. It’s worth considering whether the difference is significant if humans have about a 10% difference in body fat on average between the sexes where chimps have little to none.
The rationale why sperm count would not be important is unclear to me.
My apologies for being unclear. You wrote that chimps and bonobos have a sperm count of 603 million and gorillas 51 million. The average of chimps and gorillas then is 327 million. If you use Ryan’s data, then humans have a sperm count around 380 million, which would be closer to chimps, but if you use Smith, then humans average 175 million, which is closer to gorillas.
Interestingly, both gorillas and chimps are capable of mating multiple times a day without depleting their sperm counts whereas humans show evidence of depletion sooner.
It’s true that male preference for breast size is not consistent across cultures, but that is somewhat expected in that we are culturally and biologically variable species with behavioral flexibility.
The difference isn’t just preference for breast size but also the perception of breasts as a sexual signal. If the American view of breasts as sexual or erotic is atypical of most societies, it challenges the theory that permanently enlarged breasts evolved (or exapted) as sexual attractants.
Also, I think the viability of sperm in the female reproductive tract is on the order of days, rather than hours.
My comment was specifically in reference to the “penis as scooper/plunger” theory. The penis presumably works as a scooper only in the vagina. The vagina is a highly acidic environment that tends to immobilize sperm; semen acts as a temporary buffer, but the vagina will usually restore significant acidity within a few hours after intercourse. Sperm that make it to the cervix, uterus and Fallopian tubes are viable for several days.
the potential for multiple female orgasms
This could also merely reflect the fact that women lack the refractory period that men experience. There doesn’t seem to be anything extraordinary about women’s orgasmic capacity.
What we need is a more complex synthesis, incorporating both of these facts.
It basically comes down to humans being cooperative breeders. People weigh the potential benefits of a new or additional relationship against the potential costs of losing or weakening existing relationships. So essentially our sociality has subsumed our sexuality. That’s my conclusion. I look forward to reading your synthesis whenever you get around to it.
Quinn, I’m leaning toward that as my conclusion as well. I’ve taken too long to write the conclusion because I’m hesitant to commit fully to something that I’m really not 100% certain about (that, and all the other things I’ve had on my plate). With a break from teaching, I hope to have some time this winter to read some more and write a tentative conclusion. As I said at the outset, this isn’t my specialty, but it’s been an interesting learning process.
I’d like to read some of your stuff as well, if you wouldn’t mind pointing me in that direction. Thanks for reading and commenting.
More layman feedback, I’m finding this very very interesting and quite understandable thanks to the clarity of your explanations.