Congenital Anomalies, Kinship Systems and Pleistocene Demography
PLoS ONE 8(3): e59587. doi:10.1371/journal.pone.0059587
An Enlarged Parietal Foramen in the Late Archaic Xujiayao 11 Neurocranium from Northern China, and Rare Anomalies among Pleistocene Homo
Xiu-Jie Wu,Song Xing, and Erik Trinkaus.
We report here a neurocranial abnormality previously undescribed in Pleistocene human fossils, an enlarged parietal foramen (EPF) in the early Late Pleistocene Xujiayao 11 parietal bones from the Xujiayao (Houjiayao) site, northern China. Xujiayao 11 is a pair of partial posteromedial parietal bones from an adult. It exhibits thick cranial vault bones, arachnoid granulations, a deviated posterior sagittal suture, and a unilateral (right) parietal lacuna with a posteriorly-directed and enlarged endocranial vascular sulcus. Differential diagnosis indicates that the perforation is a congenital defect, an enlarged parietal foramen, commonly associated with cerebral venous and cranial vault anomalies. It was not lethal given the individual’s age-at-death, but it may have been associated with secondary neurological deficiencies. The fossil constitutes the oldest evidence in human evolution of this very rare condition (a single enlarged parietal foramen). In combination with developmental and degenerative abnormalities in other Pleistocene human remains, it suggests demographic and survival patterns among Pleistocene Homo that led to an elevated frequency of conditions unknown or rare among recent humans.
The anthropological theory of kinship evolution among modern humans postulates symmetric prescriptive marital exchange (“restricted exchange” in Claude Levi-Strauss’s Elementary Structures of Kinship) as the ancestral form of alliance. Under restricted exchange marriage with parents, siblings and parallel cousins are prohibited, while marriage with parents’ opposite-sex siblings’ children is prescribed. Among modern human populations, symmetric prescriptive marital alliance was, until recent times, practiced mostly in Amazonia, aboriginal Australia and Papua New Guinea and tribal India. Africa and Europe show only vestiges of this ancient matrimonial institution. These regions display high frequencies of another wide-spread form of marriage, namely “complex exchange” under which incest prohibition still holds but mating partners are not prescribed. Between restricted and complex exchange there is a number of transitional alliance forms (such as “generalized exchange” in which a man marries his mother’s brother’s daughter or his father’s sister’s daughter) which create durable relationships between various constituent units in the population (lineages, villages, etc.). From the demographic perspective, generations of repeated marriage with mother’s brother’s son or daughter (who’s also father’s sister’s son or daughter) will create a heavily inbred population. One of the phenotypical outcomes of high levels of inbreeding are elevated frequencies of congenital defects in the population. Wu et al. (2013) provide evidence that Mid-Pleistocene hominins indeed displayed a wide range of congenital anomalies that are rare in modern human populations. Deformities such as enlarged parietal foramen are so rare that their repeated detection in Pleistocene remains suggests that unusual demographic conditions must be at play here. Wu et al. (2013) conclude with a question:
“To the extent that these abnormalities can be considered congenital or cannot be securely diagnosed, these considerations raise questions regarding the population dynamics of Pleistocene humans. To what extent could this pattern reflect small, highly inbred populations, which were also demographically unstable, resulting in both the increased appearance of congenital deleterious conditions and in their subsequent disappearance through local population extinction?”
The finding of low intragroup genetic diversity among Denisovans and Neandertals (Lalueza-Fox et al. “Genetic Evidence for Patrilocal Mating Behaviour among Neandertal Groups,” PNAS 108 (2011): 250-253) supports the inbreeding hypothesis and bolsters the anthropological theory of kinship evolution. The presence of the best survivals of those ancient mating patterns among Amazonian Indians may therefore be not a regression to a primordial condition after a Beringian bottleneck but a true, unbroken line of descent that has remained virtually intact from Mid-Pleistocene times. A long-time student of Yanomamo Indians, geneticist James Neel, has a lot to say in his autobiography Physician to the Gene Pool: Genetic Lessons and Other Stories (New York, 1994, quoted here) about the role of inbreeding in early human evolution:
“With our long-established interests in inbreeding, it was inevitable that we should try to establish how frequent it was amongst Amerindians. The Yanomama recognize male-descent lineages; a man should marry outside his lineage. A highly preferred for of marriage is for men of two lineages to exchange younger sisters as brides. In the following generation, the female offspring of such an exchange must marry outside the lineage… Thus, the preferred marriage involves certain types of first cousins. When such a marriage is not possible, a man (or a woman) will try to marry within the village, which of course contains many of the man’s more remote kin. This marriage system, if observed, should result in a high level of inbreeding... Despite Chagnon’s best effort, he could only establish the identity of the 4 grandparents in 37 of the 124 marriages represented in the 4 villages where he new the genealogies best. Thirteen of these 34 marriages involved first cousins. This was a high frequency, but was it representative? Again, we resorted to computer simulation, to try to determine how rapidly inbreeding would build up under these circumstances. The answer was, quite rapidly, by our contemporary standards. The key was the small geographical extent of the marital quest and the differential fertility we have just discussed. For instance, the “grandchildren” of the more prolific headmen would all be first cousins, and they would be concentrated in several adjacent villages.
We believe that the level of inbreeding that we encountered in the Yanomama was not a recent development, but one that goes far back in time. Accordingly, aided by the computer program, we could ask the question, if this pattern of inbreeding was in place when the Indian entered the Americas, just how inbred had these populations become by now? Our best estimate was that the average marriage in an Indian village represented a level of inbreeding at least five times as large as the inbreeding in a first-cousin marriage. This is, in fact, greater than the inbreeding in a brother-sister union. This conclusion was so surprising that we have gone back to reexamine it from every possible vantage point, and from every possible vantage point it seems to hold…
A second obvious genetic departure of most of the civilized world from tribal societies is the relaxation of inbreeding. A discussion of the consequences of such relaxation rapidly becomes complex, and we will consider only the simplest case, involving diseases due to completely recessive genes with quite deleterious effects, incompatible with reproduction… When inbreeding is relaxed, as is now particularly the case for Christian communities, homozygosity for genes of this type decreases, and there should be a decrease in the diseases associated with these genes. This, however, is only temporary. Mutation pressure continues, and the gene frequency will very slowly build up, until finally the frequency of homozygotes will again come into balance with mutation pressure. However, the relative frequency of the heterozygotes in the population is now greater than before. Should this population ever revert to high levels of inbreeding, it would, so to speak, “pay the bill,” i.e., the gene frequency would have risen above the frequency consistent with the new level of inbreeding, and there would now temporarily be more of whatever disease is associated with the genes in question than would be the case had inbreeding continued at the original levels. Furthermore, there is evidence from experimental genetics that the heterozygotes for these recessive genes are sometimes themselves slightly disadvantaged, so that a relative increase in the frequency of the heterozygous carriers of a deleterious recessive gene is not to the advantage of the population.
What we have documented in the studies of the Yanomama is a population with much more genetic flux than we could have anticipated. We, of course, are not the first to recognize that human tribal populations are usually subdivided into small, semi-isolated breeding units. But, by a fortunate selection of a tribe to study, we have been able to show the genetic consequences of this population structure. Each time a new village comes into being, it represents a combination of genes (packaged into individuals), the exact likes of which has probably never existed before. A major cause of this microdifferentiation is the kinship system, leading to nonrandom village fissionings. Our species is unique in the way the kinship system determines population aggregation. We are therefore led to suspect that tribally organized human populations show more microdifferentiation than most other animal populations… I repeat again, the village is the unit of genetic competition. If a village prevailed over other villages, the genes of that village would increase disproportionately. However, at the time of the next split, this favorable gene combination would be disrupted. But even so, the daughter villages should retain some of the favorable gene combinations of the parent village as they began their competitive existence.
What I am suggesting is that the tribal gene pool of early man, however defined, was much more drastically and regularly reshuffled into genetically diverse, competing units than has previously been thought. Early human populations, if the Yanomama are any guide, were so structured that there was continuous change in the composition of the ultimate (the village) gene pool…Since, ultimately, tribes as well as villages are competing, we again see a process that ensures that the competition will involve very different gene sets…
Now, with massive population amalgamations under way, the current population structure resembles a large , increasingly homogeneous, quivering blob of jelly, which, though it may shake a bit, is unlikely to spawn a detached and unusual offshoot that will persist long enough to establish an identity…
The kinship system plus the role of chance ensured that human bands or groups of allied bands–the basic units of human competition-differed remarkably from one another. Kinship may create a sense of group coherence, which at the same time intensifies the competition with nonkin groups. The “kinship effect” may be stronger in human evolution than in the evolution of other animals and would, in a technical sense, represent an extensions of the Wright model as applied to human evolution. Earlier, I suggested that in the course of human evolution new tribes probably arose from old because a band became so detached from the parent tribe that it became the basis for a new tribe. Some of these tribes survived and some did not. Visualize this process repeated thousands of times, with the offshoot village each time being as nonrepresentative of the total tribe as any single Yanomama village would be of the whole Yanomama tribe. Given that natural selection favored the band-tribe with the best complex of genes, then we have the basis for what can be termed rapid step-wise evolution, although each step would be relatively small…
Throughout most of history, man has aggregated in very small groups, at most amounting to a few hundred individuals. I have presented each of these small pockets of humanity as an experiment in evolution. Because of the small size of the pockets and the kinship-dominated social structure, this structure carries the potential for relatively rapid genetic change. The reconstruction of human evolution requires that when a better adapted human type arose, it replaced or assimilated the existing types in, geologically speaking, relatively short order.
It is reasonable to surmise that humankind has disrupted the complex genetic structure that resulted in its rapid evolution no less than human kind has disrupted the ecosystem in which it functions…
It is rather strange that geneticists such as James Neel can easily use Amazonian Indians as the rare surviving models of Mid-Pleistocene demography and still believe that modern humans expanded out of Africa. The spell of a powerful myth is just impossible to shake off, I guess.
I offer a couple ‘blasts from the past’ and the utility of understanding population growth as a signature of movement, into the Old World, and yes not out of Africa, but into Africa.
HC Harpending Signature of Ancient Population Growth in a Low-Resolution Mitochondrial DNA Mismatch Distribution. in Human Biology, August, 1994, v. 66, no. 4, pp. 591-600
…the absence of recombination in pedigrees of mtDNA sequences does mean that history is preserved in mtDNA sequences in such a way that it may not be in sequences from the nuclear genome. In particular, episodes of population growth and decline leave signatures in the distribution of differences among individuals in a population because population decline causes loss of sequence diversity and population growth causes the retention of sequences that otherwise would have been lost. Thus DNA sequence diversity may provide an instrument for examining prehistoric demography. (pg. 591)
Vigilant, Linda, Mark Stoneking, Henry Harpending, Kristen Hawkes, and Allan C. Wilson 1991. African Populations and the Evolution of Human Mitochondrial DNA. Science, Vol. 253, pp. 1503-1507.
“Cann et al. (7) used the midpoint method of rooting their tree, assuming that the rate of evolution has been the same in all lineages. If, however, mtDNA evolution were faster in Africans, then the deep African lineages would actually be shallow lineages along which more mutations had accumulated. Hence, the tree might not yield any information regarding the geographic origin of the mtDNA ancestor (12)(p. 1504).”
NOTE Or that Africa was not the place from which H. s.s. began their colonization of the Old World. Many authors and geneticists have questioned the Out of Africa argument(s). Out of Asia would only follow an Amerindian inclusion into the debate concerning H. s. s. origins. Rebecca Cann, at one point, suggested up to 33 Eves in the Americas. AMH
This is an incredible website! Thank you,
Anyway, the general public’s, and indeed the scientific, understanding of consanguinity is wrapped up in much myth. Yes, inbreeding causes defects but that is not the whole story. In mating between strongly related persons (such as in “selfing”) numerous defects will occur for about 6 generations. After that, provided the consanguinity is maintained, the defects begin to taper off until finally they recede to background around 9 generations. And after that, favorable genetic traits are _enhanced_, not diminished. You can ask anyone who has done long-term horse breeding about this as it is a well-known phenomenon. It’s called breed-through.