This guest post by Eric Michael Johnson is part of his Primate Diaries in Exile blog tour. You can follow other stops on this tour through his RSS feed, The Primate Diaries on Facebook, or by following him on Twitter. I'm honored to have him here today.
DNA evidence implicates polygyny for the disappearance of millions. But is it 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 represents a significant portion of our collective memory that is being passed on to future generations. However, last year researchers 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. By analyzing the vocabulary usage throughout her career Ian Lancashire and Graeme Hirst at the University of Toronto concluded that the sophistication of Agatha Christie's 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, polygyny, as well as polyamory. However only one can be the culprit and, like a detective interrogating multiple suspects, the solution ultimately depends on which account you're willing to believe. Last year 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, polygyny, 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 published their findings in the esteemed online 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.

Hugh Hefner and his polygynous "playmates."
Image: Denise Truscello/WireImage
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.
Hammer and his team therefore analyzed the chromosomes from six different societies: Biaka foragers from Central African Republic, Mandenka villagers from Senegal, San hunter-gatherers from Namibia, French Basque, Han Chinese, and Melanesian islanders from Papua New Guinea. 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 . . .

[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).]