The origins of our sexuality is the greatest mystery in human evolution. But could our prime suspect be a case of mistaken identity?

If reproductive success were applied to fiction the two billion copies of Agatha Christie's novels (only trailing behind Shakespeare and the Bible) would be considered a stunning example of evolutionary fitness. Her work, in such classics as Murder on the Orient Express, Death on the Nile, or Witness for the Prosecution represents a significant portion of our collective memory that is being passed on to future generations. However, researchers have recently uncovered evidence of a tragedy that befell the world's most popular mystery writer and, in so doing, provided a useful lesson when considering genetic evidence for the evolution of human sexuality.

Ian Lancashire and Graeme Hirst at the University of Toronto analyzed the vocabulary used throughout Christie's writing career and determined that the sophistication of her language underwent a significant decline in her final years. By looking at the number of different words used in her novels, as well as the number of repeated phrases, the researchers determined that her vocabulary dropped by almost 31% with the largest decline occurring in her last four books. This, in combination with her family's testimony about undiagnosed physical and mental decline, led the researchers to conclude that they were witnessing the effects of Alzheimer's disease on the world's best-selling author. As a result, Christie's final novels maintained echos of her former work, but they were of a substantially different character to most of her 54-year career as a writer.

Imagine for a moment that everything Agatha Christie had ever written was lost to history except for her last book. If you were to try and form conclusions about her work from this limited account it would result in significant distortions. It would represent the author after she had undergone a profound change and you would be hard pressed to understand why she had ever been so popular. But this kind of selection bias is essentially what we have when we look at the written record of our human past. All of written history, from the earliest accounts in 3,200 BCE to the present, is a mere fragment of human existence on this planet. It is the equivalent of only looking at Agatha Christie's final novel out of 85 published works during a long and distinguished career.

There is no greater mystery in human evolution than the origins of our sexuality. Following the trail of clues available researchers have independently concluded that humans evolved through systems of monogamy, polygamy, as well as polyamory. However, only one can be the culprit. Like a detective interrogating multiple suspects, the solution ultimately depends on which account you're willing to believe.

In 2009 Owen Lovejoy made the case for monogamy based on the fossil remains of the early human ancestor Ardipithecus ramidus. Meanwhile, Christopher Ryan and Cacilda Jethá have argued that polyamory (or, more precisely, a multimale-multifemale mating system) is the most likely scenario from an analysis that emphasized anthropology, behavioral biology, and physiology. To further complicate matters the third suspect in this mystery, polygamy, has been the conclusion from scientists conducting DNA analyses. These conflicting accounts therefore require careful detective work in order to determine which story is the most convincing.

Polygyny (the single male-multifemale version of polygamy) is most well known among primates such as baboons or gorillas. These are the species that have been (incorrectly) described as living in "harems," and are often easy to identify since the males can be up to twice the size of females. Many anthropological accounts, most famously George Murdock's Ethnographic Atlas, have suggested that the human species is "moderately polygynous" since the majority of studied societies practice polygynous marriage (982 out of 1157 according to Murdock's account).

To test whether these reports of polygyny are a local or species-wide phenomenon evolutionary biologist Michael F. Hammer and colleagues at the University of Arizona published their findings in the journal PLoS Genetics. By analyzing the clues left in our X-chromosomes and comparing their results to human autosomes (any of the additional 22 chromosome pairs that aren't sex-linked) the researchers sought to discover what they call male vs. female "effective population size," or the percentage of males compared to females who were effectively reproducing. If polygyny were indeed the norm it would mean that most men throughout human evolution never reproduced and, in strictly genetic terms, had mysteriously vanished without a trace.

Because women have two X-chromosomes they will always pass one of these to either their son or their daughter. Men, on the other hand, will either pass along an X-chromosome (in the case of a daughter) or a Y-chromosome (if they've had a son). But both men and women pass along the same number of autosomes. This means that by comparing the genetic differences between X-chromosomes and autosomes you can estimate the effective population size of men who successfully reproduced compared to women. In other words, the genetic evidence for effective population size is being used to determine the mating system. Skewed upwards and only a few men in any given population were having children with multiple women as in polygynous systems. However, if the ratio is closer to 1:1 it would be consistent with monogamy since an equal number of men as women were passing on their genes.

[caption id="attachment_1813" width="600" caption="Ratio of effective population sizes between X-chromosomes (Nx) and autosomes (Na) for each population. Points above the dotted line suggest greater variability in male reproductive success. Figure reproduced from Hammer et al. (2008)."][/caption]

Mike Hammer and his team of genetic detectives therefore analyzed the chromosomes from six different societies: French Basque, Han Chinese, Melanesian islanders from Papua New Guinea, Biaka foragers from Central African Republic, Mandenka villagers from Senegal, and San hunter-gatherers from Namibia. The researchers found evidence that there was greater variability on the X-chromosome than would be expected if monogamy had been the standard practice. Instead, the evidence suggested a male-female ratio of relatively few men and multiple women as would be expected in polygyny (ranging from 2.4-to-1 among the San and 8.7-to-1 among the Basque). This genetic evidence by Hammer and colleagues would seem to support Murdock's data on marriage systems and confirm that polygyny was the dominant mating system during human evolution.

But like every good detective mystery, just when you think the case is closed you're treated to a twist ending. Primatologist Sarah Blaffer Hrdy (author of The Woman That Never Evolved, Mother Nature, as well as her latest book Mothers and Others) is one of the leading experts on polygynous mating systems in primates. As she explained to me in our recent correspondence there are several important considerations that have been left out of this story. The most important is the kind of sample bias I referred to earlier if we were to make conclusions about Agatha Christie's work based only on her final novel. The DNA evidence may be a record of the human past, but how far into the past does it actually go? As Hrdy explained:

Keep in mind that in terms of interpreting such genetic evidence we are of necessity confined to a fairly recent time depth (and remember, by "recent" someone like me means the last 10,000 years or so). For this time period multiple lines of evidence do indeed suggest that humans were moderately to extremely polygynous and that women were moving between groups more than men were.

Humans have been around for far longer than 10,000 years and conservative estimates place the emergence of modern Homo sapiens at about 200,000 years ago. A genetic record extending back 10,000 years is remarkable, but it's essentially adding only three more novels to our existing timeline.

There is also something very important to consider that dramatically influenced human behavior within the last 10,000 years: the invention of agriculture. Prior to about 12,000 years ago all humans were hunter-gatherers and lived a migratory existence. With the advent of farming some human societies began to remain sedentary for the first time in our history. This change had serious impacts on human life and behavior. Just as Alzheimer's dramatically altered the content of Agatha Christie's work, so agriculture radically transformed human society and, by consequence, sexual behavior.

Hrdy argues that there was a major disruption in human residence patterns as a result of this "agricultural revolution." In small bands of modern day hunter-gatherers there is a mixture of what anthropologists call matrilocal and patrilocal residence, the practice of women or men to stay within the community they're born into while the other migrates between communities. However, recent research has shown that hunter-gatherer societies today emphasize matrilocal (or bilocal) residence while fewer than 25% are considered patrilocal. This is in stark contrast to the larger scale agricultural societies where an estimated 70% are patrilocal.

According to Hrdy, pre-agricultural human societies would likely have been similar to modern day hunter-gatherers, but the rise of agriculture changed this pattern dramatically. Over the past 10,000 years or so, Hrdy explained, "matrilocal societies gave way to pressures from more expansionist patrilocal societies." This simple change had serious repercussions for both human life and the genetic record. Patrilocal societies typically show increased hierarchies, greater male control over women's sexual choices, and more competition among men compared to matrilocal societies. Patrilocal societies are also usually polygynous. Therefore, the larger numbers of patrilocal (and polygynous) societies today is likely the consequence of agriculture and not a true reflection of the human past. Like Agatha Christie's writing, many human societies underwent a dramatic transformation and basing our conclusions on this period would distort our understanding of what came before.

But there is an even more basic problem in assuming a polygynous human mating system. Modern day bonobos and chimpanzees have a male vs. female effective population size of between 2-to-1 and 4-to-1. If we were using the same argument presented by Hammer and colleagues, these two species should be considered "moderately polygynous" as well. Two independent genetic studies found both bonobos and chimpanzees to be similar to humans on identical criteria. As one study (Erickson et al., 2006) concluded, "the male effective population size in bonobos is small and similar to that suggested from comparable data in humans," while, in the second study (Langergraber et al., 2007), the "data indicate that the sex difference in effective population size is similar in chimpanzees and humans." It turns out that our would-be perpetrator has two reliable alibis.

Despite Pan's moderately polygynous genetics, the bonobo and chimpanzee mating system is most accurately described as multimale-multifemale because males and females each mate with multiple individuals. Of course, this isn't random or indiscriminate mating since females are making careful decisions about who they choose to mate with, and when. The effective population size in bonobos and chimps shows up looking genetically similar to humans because females choose to preferentially mate with high-ranking males during their peak of ovulation. Females still choose to mate with additional males at other times of their cycle, but since these don't produce offspring the end result is that relatively few males are passing on their genes. As Hrdy has demonstrated, something very similar has been shown among humans. This makes a multimale-multifemale mating system the prime suspect in our evolutionary whodunit.

In humans, bonobos, and many other primates, there is a great deal more non-conceptive sexual behavior going on than most people -- from Saint Augustine to contemporary biologists - realize. For example, in South American partible paternity societies, the woman's official mate or husband is still statistically more likely to be the progenitor of offspring she produces, even though other men can and do have some probability of paternity, or at the very least, perceive that they do.

Because of this, Hrdy notes, in a large number of human societies women may be having multiple sexual partners at any given time, but there will usually be a relatively small number of men who are the actual fathers of their children. In this way the missing persons in our evolutionary mystery would be the result of sample bias. It's not because our genes don't reveal the full story, it's because women have only chosen some men whose genetic tale they wanted future generations to remember. In the evolution of human sexuality, as it was in Agatha Christie's life and work, such stories can be subject to dramatic alterations depending on the circumstances and care must be taken lest we misinterpret and obscure the very mystery we're trying to solve.

This post originally appeared at Psychology Today.

References:

Hammer, M., Mendez, F., Cox, M., Woerner, A., & Wall, J. (2008). Sex-Biased Evolutionary Forces Shape Genomic Patterns of Human Diversity PLoS Genetics, 4 (9) DOI: 10.1371/journal.pgen.1000202

Burton, M.L., Moore, C.C., Whiting, J.W.M., & Romney, A.K. (1996) Regions Based on Social Structure. Current Anthropology, 37(1), 87-123.

Eriksson, J., Siedel, H., Lukas, D., Kayser, M., Erler, A., Hashimoto, C., Hohmann, G., Boesch, C., & Vigilant, L. (2006) Y-chromosome analysis confirms highly sex-biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus). Molecular Ecology, 15(4), 939-949. DOI: 10.1111/j.1365-294X.2006.02845.x

Hrdy, S.B. (2005) Cooperative Breeders With an Ace in the Hold. In Voland, E., Chasiotis, A., and Schiefenhövel, W. (Eds.), Grandmotherhood: The Evolutionary Significance of the Second Half of Female Life. New York: Rutgers University Press.

Hrdy, S.B. (2000) The Optimal Number of Fathers. Evolution, demography, and history in the shaping of female mate preferences. Annals of the New York Academy of Sciences, 75-96. PMID: 10818622

Langergraber, K., Siedel, H., Mitani, J., Wrangham, R., Reynolds, V., Hunt, K., & Vigilant, L. (2007) The Genetic Signature of Sex-Biased Migration in Patrilocal Chimpanzees and Humans. PLoS ONE, 2(10), e973. DOI: 10.1371/journal.pone.0000973

Marlowe, F.W. (2004) Marital Residence Among Foragers, Current Anthropology 45(2): 277-284.