Effective Polygyny in Humans: Turns out it is for real

ResearchBlogging.orgHuman societies tend to be at least a little polygynous. This finding, recently reported in PLoS genetics, does not surprise us but is nonetheless important. This important in two ways: 1) This study uncovers numerical details of human genetic variation that are necessary to understand change across populations and over time; and 2) the variation across populations are interesting and, in fact, seem to conform to expectations (in a "we don't' really care about statistical significance" sort of way, for now) regarding human social organization.

Before examining the paper, we should mention four terms/concepts: Effective population size, Polygyny, and Operational Sex Ratio (OSR), and Variation in Reproductive Success (RS). The first two are used in the article, and the third I'm adding because it is a good one to know.

Polygyny is a term about mating systems, and unfortunately, mating system terms are usually used or understood incorrectly. Also, terms about mating systems should not be used as a substitute for terms about actual mating or population genetics. A mating system is a characteristic of a population, group, species, or some other collection of individuals, not a behavior of an individual or a pattern of genetic flow, though of course they are all related.

Briefly, "Monogamy" is the mating system where a male and female pair off, either serially (chaning mates over time) or life-long; "Polygamy" is a term we should never use in science, but technically it includes the two most common non-monogamous systems. Most of the time when you hear the word "Polygamy" used it is by lawyers or reporters and they are really talking about "Polygyny" which is a system in which one or more females may be mated with a single male. Like race horses, big horn sheep, mormons, and so on. "Polyandry" is where more than one male is mated to one female, as is seen in phalaropes (a kind of bird) and in a small number of human societies.

If there is a roughly fifty-fifty sex ratio at birth, then in Polygyny, one expects that some number of males are not mating at all, or at least not very often, with females, while some other number of different males are mating more often. But in fact, mating is not enough ... what really matters is the difference among males in paternity of the various offspring borne by the females.

Since this is the number that really matters, we like the term "Operational Sex Ratio" or "OSR." There are two ways to get a smaller number of males (relative to females) in the mating equation: One is if some of the males simply disappaer following this fifty-fifty birth ratio, so among adults, there are fewer males. The other is that these males are around perhaps wanting to mate, but they don't for some reason, and we simply ingore them. We ignore them numerically by defining the OSR which is the ratio between actual mating/fathering/paternitizing males (the 'operational' males) and the actual mating/mothering/materitizing females.

Of course we are also ignoring some females, but in most natural populations of mammals or birds, far more males than are ignored by the OSR.

"Variation/variance in RS" is one of the most difficult terms for people to become totally comfortable with, in part because there is a way to understand this that makes you think you've "got it" but you don't. Then you try to apply it and the world goes topsy-turvy on you and you have to start again.

The variation that is being measured here is simply the numerical variation among members of ONE SEX (totally ignoring the other sex) in reproductive output. So we look at, say females, totally ingoring the males, and we ask of a group of females "what was the average number of offspring these females had over a lifetime" and then we ask "Oh, and what was the variation in that number." So if every female has one offspring and that is all she wrote, then the variation is zero. If some females had three or four offspring, a small percentage had zero, but most had two, then the variation is greater than zero, but not to much.

Then, we look at the other sex. "How many offspring, on average, did the MALES in this same population have?" Of course, this will be the same number as we had calculated for the females in this population, right? Then we ask "What is the variation among the males?" In a typical mammal (and humans are not typical mammals, by the way) we will find that a smallish number of males have lots of offspring each, a moderate to largish number have zero, and the remaining males have something in between. In other words, there will often be a LOT OF VARIATION among males. More importantly, there will be more variation among males than in females in most mammals ... a lot more in some mammals. For birds, as a rule, there is more variation among males than in females, but not such a large difference.

This is important because any allele that affects mating will have an effect that is stronger where variation is greater. This is why we see exaggerated sexually selected traits (including large body size) in male mammals, but hardly ever in female mammals, while in birds we see sexually selected traits quite often in both sexes.

The final term to examine is "effective population size." This is one of the more important aspects of the present study, because they were looking at the difference between males vs. females in relation to population genetic change over time. In population genetics, size is everything (size of population, that is). So, if there is a skewed OSR then the effective population size of males will be different than for females.

Here is what the study found:

... the mating system of humans is considered to be moderately polygynous (i.e., males exhibit a higher variance in reproductive success than females). As a consequence, males are expected to have a lower effective population size (Ne) than females, and the proportion of neutral genetic variation on the X chromosome (relative to the autosomes) should be higher than expected under the assumption of strict neutrality and an equal breeding sex ratio. We test for the effects of polygyny [note: here I would prefer the term "OSR"] by measuring levels of neutral polymorphism at 40 independent loci on the X chromosome and autosomes in six human populations. To correct for mutation rate heterogeneity among loci, we divide our diversity estimates within human populations by divergence with orangutan at each locus. Consistent with expectations under a model of polygyny, we find elevated levels of X-linked versus autosomal diversity. While it is possible that multiple demographic processes may contribute to the observed patterns of genomic diversity (i.e., background selection, changes in population size, and sex-specific migration), we conclude that an historical excess of breeding females over the number of breeding males can by itself explain most of the observed increase in effective population size of the X chromosome.

Here is a chart showing the results:


Figure 2. Ratio of effective population sizes for the X chromosome (Nx) and autosomes (Na) for each population. The diamonds represent the point estimate, while the vertical bar shows the estimated 95% confidence interval. The dotted line represents the expected ratio (0.75) under a neutral model with breeding sex ratio of 1. Three letter population codes are as follows: Melanesians (Mel), Basque (Bas), Han Chinese (Han), Mandenka (Man), Biaka (Bia), San (San).

Behavioral biological theory would make the following two predictions regarding these data:

1) The degree of body size dimorphism (with males being a bit larger than females) should be greater in the populations with the highest OSR (the ones higher on the graph), assuming that there is some effect having to do with male-male competition (warning, in the absence of behavioral evidence of males fighting over females, this may be a weak hypothesis. This will depend on what you think about males fighting over females in each population. Do they? Do you know?); and

2) The populations with the lowest OSR (those lower on the graph) should be foragers or egalitarian societies, while those highest on the graph should be societies where variation in personal wealth is more likely to occur.

I quickly add that the 95% confidence intervals overlap all of these populations, so interpretations related to these predictions using these data would be mere arm waving. And, if arm waving is an adaptive trait, say, for males, in a certain society, then we should see longer arms in males in that society. Which brings us back to the orangutans.

Michael F. Hammer, Fernando L. Mendez, Murray P. Cox, August E. Woerner, Jeffrey D. Wall, Dmitri A. Petrov (2008). Sex-Biased Evolutionary Forces Shape Genomic Patterns of Human Diversity PLoS Genetics, 4 (9) DOI: 10.1371/journal.pgen.1000202



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Maybe. I've got a REALLY COOL post coming out in a few hours on a newly reported fossil creature. The article is embargoed, so it has to wait. I think that if that post is not anthologizable and in fact judgable to be included I'm going to slit my wrists. But don't fell bad or anything if that happens.

(At first I thought "anthologizable" was some awful typo I had made......!!!)

The one with the you know what that relates to the evolution of the whatchamacallits that fly?

The question is what does it mean? What does polygyny mean?

I can think of numerous conditions which will produce an effective breeding ratio lower than 1:1, but which do not involve what you would traditionally think of as polygyny - selective female "cheating" being the most obvious (and known from chimps). Polyandry can be consistent with polygyny.

Another question is the time-depth of polyandry - is it a derived trait, or a primitive one? On the graph, the most primitive society, the San, have the lowest OSR. Is polyandry simply an effect of warfare over the last few thousand years?

So many questions, so few answers.

frog: exactly. this is why it is incorrect to equate polygyny as a mathing system with OSR.

The San are definitely not a primitive society. But putting that aside, polygyny is going to vary with environmental conditions in vertebrates. Same with humans but obviously one has to understand "environment." I would say that traditional polynesian sea faring people and cattle keepers would be on the top of the list for high OSR (effective polygyny)

GL: The San are definitely not a primitive society.

Are you saying that the San are less like our ancestors 10kya than we are, or are you using primitive in some new-fangled way?

I would say that traditional polynesian sea faring people and cattle keepers would be on the top of the list for high OSR

In multiple ways - when the cat is away, as they say. Reminds me of the end of Sapolsky's memoir, where the old beta baboon is lying in the sun with his assemblage of girl-friends and possible descendants.

I find it funny to always be picking on mormons when talking about polygyny. Just look at the presidential race this year among the repubs. Which candidate had 'sired" offspring from only one female....Romney.

Frog: Primitive is almost always taken as a slur, even if not meant as a slur. If you want to call a group primitive, you have to understand that very simple and unavoidable fact. A phrase like "Group X are like..." is a statement with either no meaning at all or way way too much meaning. For instance, the following statement is true in my mind:

"The San and Americans are more similar than the San and almost any other cultural group."

But I'm only thinking of a handful of ways in which they are similar. When you say "The San are like our ancestors of 10,000 years ago" what do you mean? Who are "our ancestors?" Are "we" Native American? Asian? European? There was a tremendous amount of diversity 10,000 years ago. Were the San rice farmers 10,000 years ago? Buffalo hunders? Growing rye in the Jordon Valley? Are you suggesting that they are the same today (meaning the ethnographic present) as they were 10,000 years ago, and how do you know that? In respect to what features of their physical form, their society, etc?

And so on and so forth. You are probably getting the picture...

GL: Primitive is almost always taken as a slur, even if not meant as a slur. If you want to call a group primitive, you have to understand that very simple and unavoidable fact. A phrase like "Group X are like..." is a statement with either no meaning at all or way way too much meaning.

Yeah, we keep on running out of words because we have to kowtow to the lowest common denominator. We all know that in discussions like this primitive means exactly what it means - less derived. It's ridiculous to continuously add new euphemisms because dummies assume that change is inevitably an improvement in a context free manner.

In almost everyway the San are more similar to human societies of 10kya than we are. More similar in economic structure and social structure - since obviously the genetic differences are slight; but even there, the major evolutionary changes have been in digestion and immunology, which we know are epicentered in the ME.

Even the largest society of 10kya were on the scale of thousands of individuals. 10E3/10 (for traditional San society as of 20 years ago) is much, much smaller than 10E9/10E3, and scale is the defining characteristic of social systems (number of relationships per person, which grows exponentially).

Yes, it is important to be precise - but you can only get so much precision in a couple paragraph comment. It's also important not to tie ourselves so much that we can't say anything at all. Group X does have features, insofar as Group X exists at all. If Group X is useful at all, it has an internal structure, as shown by the OSR graph.

You understand that as someone who knows a number of hunter gatherers as close personal friends, I'm not going to let the word "primitive" into the discussion at all, and I'm going to force the discussion to address the nuances and complexities that (as you correctly state) can't fit into a couple of paragraphs. That is the only way that this discussion is going to happen here.

So, let's get back to your point, which was actually a good question, but I want to rephrase it.

You are asking if foragers have a greater or lower likelihood of being polygynous. Or, in other words, is polygyny the typical social element for humans generally with a shift happening recently with agriculture, etc.?

(By the way, most of the "san" we think of when invoking that term have ancestors who primarily kept cattle, who's ancestors in turn were foragers. But I digress)

Foraging usually is equated with egalitarian, low-resource variance societies, which would tend to be have very low polygyny rates. Among the Efe somewhat under one in ten married men are in a polygynous marriage, and never more than two wives as far as I know.

So, GL, what word do you suggest we use? Historically recent primary foragers? Maybe that won't be misunderstood - it's esoteric enough to not get picked up by the dummies? "Non-derivative" even has a positive sound about it -- even if it's confusing.

My question is a bit more sophisticated - how many different combinations of egalitarian systems would produce the OSR rates you see? How many different kinds of tribal, sheikdom and state level systems of mating would still produce the OSR rates you see? Do OSR rates map onto social systems at all at the marriage kinship level, or are they primarily determined by "extraneous" effects - warfare reducing the male population as a whole, differential fertility rates between males having a much more pronounced effect than in females and so forth?

My question was a rhetorical spur to questions - it's fairly well know that the "marriage ratio" among smaller scale societies only becomes significantly polygynous at the chiefdom level of organization. Band and tribal people have low polygyny rates because they have low levels of resource inequality - and when they do have it, it's often balanced out by polyandry as in most polynesian societies. But since they do have an unbalanced OSR, the safe assumption is that it has little to do with the obvious first-order "social kinship" patterns, and probably much more to do with more subtle second order effects.

As most things with human beings tend to be.

Please explain what an unbalanced OSR is.

People in the people business have dropped the word "primitive" in referring to groups of people some time ago. You simply have to get with that.

Where there are sufficient data, OSR maps with variance in resource holding across males. I think I already said that, but it is worth repeating. How that variance emerges is a function of ecological and cultural factors, etc. So you can have a very high variance group of foragers if there is a holdable dependable resources that is sometimes abundant. Traditional northwest Native Americans were foragers but had high rates of polygyny.

Please explain what an unbalanced OSR is. I meant skewed.

Where there are sufficient data, OSR maps with variance in resource holding across males.

That's interesting. It means the explanation is probably simpler - but it still doesn't, prima facie, eliminate differential effects of potential fertility. A female with fairly low fertility won't be knocked down from reproduction close to as much as a male -- even with pretty good mating opportunities. I'd expect that would be correlated with resource holding, at least in small-scale societies where resource holdings would map pretty closely to nutrition.

Traditional northwest Native Americans were foragers but had high rates of polygyny.

But they lived in chiefdoms! They weren't organized in bands, like most foragers.

There's the problem with throwing away the Bad Word without replacing it. NW Native Americans were more socially changed from the 30kya ancestral state than other foragers, and so just using the word "foragers" is misleading.

You have to summarize somehow -- and that requires a word or phrase; I don't care which one you use, but one is missing here, because there does exist a salient concept here. The Bad Word is kept in evolutionary biology because it is useful to summarize the essential change over time, without any implication of stasis or lack of sophistication.

Or are you saying that in the "People Business" the concept has been thrown away in the last decade? That there are no revolutionary changes as opposed to incremental changes in human societies?

So, GL, what word do you suggest we use?

How about "noble-savager"? As in the "the San are noble-savager than we are".

By El Christador (not verified) on 01 Oct 2008 #permalink

From the archaeological perspective, I see Europeans as being primitive in at least three respects:

General technology. European technology is mainly received from other regions over the last few centuries.

Language. Written language is received from other more advanced regions.

Math. Same.

I was thinking of a fourth one, but I can't remember what it was now. Oh, yes, food production. Europeans are primitive i this respect too.

Eureopeans = very very primitive.

Once we are all agreed on this indisputable set of facts then we can move back into this discussion of mating systems. Everybody read for that?

Of course, even in evolution (at least non-human-focused evolution) we've been trying to avoid use of the word "primitive" because it isn't necessarily apt. It irrevocably conjures not just the slur context, but the implication of greater simplicity/less sophistication -- because that is, after all, what it meant for years. But biologically, other organisms aren't necessarily "simpler" at all. They do not, to be sure, have complex social structures on the scale of humans, but measuring complexity purely by social structure is faintly sophistic. The biology and evolution of extant beings are all rather complex, and having some unitary axis to measure complexity doesn't make sense or faithfully represent reality.

The idea of primitive as only meaning "less derived" is actually, of course, a recent derivation. The ideas of the "Great Chain of Being" and other early hierarchies and evolutionary trees explicitly saw non-humans as "lesser," simpler, and farther from God -- and saw other races of humans as such as well. Yet bacteria have undergone millions of years of evolution like everything else -- and the reason they're still simpler organisms in many ways isn't because that's their place in the chain of being, it's because they've been wildly successful in what they do, and what they do is complex in a way wholly different than the way humans are complex. (They're the most successful organisms on Earth, if your standard is ubiquity or biomass.)

One can't simply deride as "dummies" those who don't glom on to the technical meaning of "primitive" when they are really just understanding it in the context it has been used in for hundreds of years. "Oh, no, ignore those hundreds of years everyone -- to still understand it in those freighted terms is to be backwards, and has nothing to do with being influenced by long-standing social cues and explicit condescension. It's just being PC to worry that hundreds of years of one usage will convey that meaning rather than the new and technical one we say it means."

In my biology circles at least, we use "Less derived" and "More derived." Not that hard at all.

J: In my biology circles at least, we use "Less derived" and "More derived." Not that hard at all.

Great answer. Regardless of the etymological history of the words, we just need someplace to hook-up time to evolution. Most scientific words that are fairly native to English have pretty absurd etymologies.

GL: Eureopeans = very very primitive.

Not at all - they have the exact same level of being "derived" as the Chinese, the Middle-East, India and the rest of Eurasia. At this point, of course, only a small percentage of the world population is still living with numerous "less derived" cultural traits - everywhere folks are significantly involved with states, literacy, math, and so on and so forth.

What you wanted to say is that Europeans are less creative - that the derived features in their cultures were horizontally rather than vertically transmitted. Of course, "creative" would be a Bad Word, for a good reason - creative applies to individuals and not to societies (just as less/more derived applies in this context to societies and not to individuals).

For example, the more derived feature is a general lack of curiosity and self-sufficiency; any small-scale society that rewarded a keep-your-nose-to-the-grindstone, country-first mindset would quickly be destroyed; while the opposite is true under contemporary conditions, where human beings are used as cannon fodder for an elite.

Another example is that in Polynesia, the lack of pottery is actually a derived characteristic, while the less derived characteristic was the sophisticated Lapita pottery complex. It's pretty obvious that less/more derived doesn't map onto any kind of simple-minded better/worse or advanced/retrograde gradient.

But to get back to my question: I'd expect that would be correlated with resource holding, at least in small-scale societies where resource holdings would map pretty closely to nutrition. Is that true, that biological fertility ~ nutritional status ~ resource holdings?

Regarding the body size dimorphism prediction:
In humans, since mating success rarely depends (anymore) on physical power, there should no longer be any evolutionary trend to increase body size dimorphism (although there might have been in the past). Modern human males tend to rely on political or economic power instead of physical power to achieve mating advantages. Perhaps a study on social standing or bank account dimorphism would be in order. Is there an evolutionary component to the "Glass Ceiling" for women?
(Constructive criticism encouraged-I'm not a pro at this.)

All you need is a study of what women prefer in men! This has been done countless times. Women on average prefer a man who is a little taller than they are, and it turns out that men are a little taller than women.

Now, why do women prefer this in study after study (on average)?

GL: All you need is a study of what women prefer in men!

But even that gets complicated. There's been studies that differentiate between what women prefer in men as partners, and what women prefer in men when they're fertile. Which strategy for males is more successful: the rugged bad-boy who only gets a chance once a month, or the nice-guy who gets a chance all month long --- but has to bring more resources to the table?

And of course those studies (referred above) were done with American and European women, which always brings up the question of whether they're globally applicable. Are the height studies done globally, or do they stick to Western or heavily Westernized societies?

Too many confounding variables every time. It's almost impossible to believe any human studies.

They always remind me of the chimp studies on mating patterns. Male biologists had assumed that females mated with the band they lived with; they never saw anything else. Bring in a few female biologists who bothered to actually do paternity tests - and voila, 50% of the infants were fathered by other bands. And chimps aren't nearly as sophisticated as we are at these games.

Frog ... Yes, and of course, there is also the occasional study done, say, in Canada or Japan, which allows the purveyors of the results to claim that they are cross-cultural...and thus represent humans as a species, and thus represent our evolutionary general-ness.

Modern human males tend to rely on political or economic power instead of physical power to achieve mating advantages.

But tall people have an economic advantage...

If you are referring to actually contracted marriages here, rather than looking at who the real biological parents of children are, then I would suggest that these may be cultural "mating systems" but hardly reproductive systems. Marriage is not guarantee of paternity; it is mostly a formal kinship-creation mechanism.

By Helga Vierich (not verified) on 21 Jul 2013 #permalink