Social change may explain decline in genetic diversity of the Y chromosome at the end of the Neolithic period | CNRS
The problem with having a childish superstition based on the campfire tales of primitive people who knew nothing of the world outside their own narrow horizons and folk memory is that it can cause you to believe the most ludicrous things that require you to maintain a pristine ignorance in order to retain your superstition.
This is especially true if an integral part of your irrational superstition is that there is a mind-reading bogeyman in the sky who will become angry if you have the slightest doubt or learn things that cause you to question your superstition. Your irrational phobia imposes a sort of information filter on your perception that doesn't allow anything to pass through that might cause you to change your mind.
This is why creationists will believe such absurdities as a global genocidal flood that left no geological evidence and reduced the human population to such a low number that the lack of genetic diversity would have guaranteed extinction within a handful of generations, yet this left no mark on human genetic diversity. Instead, what we see in the genetic record of human history in the Y chromosome is a change in the demographic profile just about the time when the Bronze Age story-tellers were setting their genocidal flood tale.
This shows that not only were there far more humans alive than the tales relate, but that there was a significant change in the form of society, probably as a result of technological change, to a more patrilineal society. This created the conditions for powerful male tribal leaders to inherit the powers to dominate other males and so to father many more children, resulting in a functional reduction in the male population, and fall in genetic diversity in the Y chromosome, while the female population continued to grow.
Some time ago I wrote about how gene-meme co-evolution can result in genetic changes which are not directly related to fitness of those genes, as this phenomenon illustrates. One of the examples I gave was that of Western Ireland where there is a cluster of Y chromosomes inherited from the legendary founder of the Uí Néill, Niall Noígíallach (Niall of the 9 hostages). In that part of Ireland an estimated 21% of males carry his Y chromosome and 8% in the rest of Ireland. I also cited another such cluster in China where an estimated 1.5 million males, mostly in Northern China and Mongolia have the same Y chromosome as descendants of Giocangga, a Qing emperor who died in 1582. These men were able to father many children because of the power they had in their societies, and their sons inherited both their Y chromosome and their power and authority. Because of their authority, they were able to command better resources in terms of food and shelter for their offspring, so improving their breeding success.
It was not necessary to use military power to dominate and exterminate neighbouring peoples to achieve the resulting reduction in genetic diversity in the Y chromosome.
Both these examples are cited in this paper.
This is the explanation proposed by a team of researchers from the French Centre national de la recherche scientifique (CNRS), the Muséum national d'Histoire naturelle (MNHN) and the Université Paris Cité, who have published their research findings, open access, in the journal Nature Communications. It is explained in a brief CNRS news item:
The emergence in the Neolithic of patrilineal1.1 social systems, in which children are affiliated with their father's lineage, may explain a spectacular decline in the genetic diversity of the Y chromosome2.1 observed worldwide between 3,000 and 5,000 years ago. In a study to be published on 24 April in Nature Communications, a team of scientists from the CNRS, MNHN and Université Paris Cité3.1 suggest that these patrilineal organisations had a greater impact on the Y chromosome than mortality during conflict. This conclusion was reached after analysing twenty years of anthropological field data – from contemporary non-warlike patrilineal groups, particularly from the scientists’ own fieldwork carried out in Asia – and modelling various socio-demographic scenarios. The team compared warrior and non-warrior scenarios and showed that two processes play a major role in genetic diversity: the splitting of clans into several sub-clans and differences in social status that lead to the expansion of certain lineages to the detriment of others. This study calls into question the previously proposed theory that violent clashes, supposedly due to competition between different clans, in which many men died, were at the origin of the loss of genetic diversity of the Y chromosome. The results of this study also provide new hypotheses on human social organisation in the Neolithic and Bronze Age.Ironically, the Bronze Age story-tellers recorded this patrilineal society in their tales, which are resolutely patriarchal with political power inherited by sons from fathers and women relegated to subservient status as commodities to be traded as sex slaves, with taboos on sexual activity with anyone other than an approved male in a marriage sanctioned by a male priesthood.
The researchers' open access paper in Nature Communications gives more technical and background information:
AbstractIt's very clear from this paper that not only did humans not go through a population bottleneck where the only surviving males all has the same Y chromosome, being sons of a single patriarch, but that the genetic diversity which had evolved at about the time went through a reduction in diversity (how can you reduce from 1?) because of cultural changes brought about by technological changes, which facilitated patriarchal and patrilineal societies where some male lines had achieved a dominance that increased their breeding success.
Studies have found a pronounced decline in male effective population sizes worldwide around 3000–5000 years ago. This bottleneck was not observed for female effective population sizes, which continued to increase over time. Until now, this remarkable genetic pattern was interpreted as the result of an ancient structuring of human populations into patrilineal groups (gathering closely related males) violently competing with each other. In this scenario, violence is responsible for the repeated extinctions of patrilineal groups, leading to a significant reduction in male effective population size. Here, we propose an alternative hypothesis by modelling a segmentary patrilineal system based on anthropological literature. We show that variance in reproductive success between patrilineal groups, combined with lineal fission (i.e., the splitting of a group into two new groups of patrilineally related individuals), can lead to a substantial reduction in the male effective population size without resorting to the violence hypothesis. Thus, a peaceful explanation involving ancient changes in social structures, linked to global changes in subsistence systems, may be sufficient to explain the reported decline in Y-chromosome diversity.
Introduction
By analysing mitochondrial and Y chromosome sequences in more than 300 contemporary human populations worldwide, Karmin et al.1 highlighted that the male effective population size of these populations (estimated from the paternally transmitted Y chromosome) underwent a severe bottleneck around 5000 years ago. This remarkable decrease was not observed for the female effective population size estimated from the maternally transmitted mitochondrial DNA (mtDNA). These results were further supported by a study on 26 human populations from the 1000 Genomes Project, which found evidence for a similar bottleneck of male effective population size2. Similarly, Batini et al. analysed genetic diversity from 17 populations from Europe and the Near East, and showed similar Y chromosome pattern3,4. The estimated timeframe of this bottleneck varies between world regions, ranging from 8300 BP in the Near East to 1400 BP in Siberia, and was estimated to 5000 BP in Europe according to Karmin et al.1 using a mutation rate of 0.74 × 10−9 mutations/bp/year for the Y chromosome. Using a slightly higher mutation rate (1.0 × 10−9 mutations/bp/year), Batini et al.3 estimated more recent dates for this bottleneck (ranging from 4200 to 2100 BP for the Near Eastern and European populations)3.
Several authors have pointed out that the interpretation of patterns in human genetic diversity needs to take into account fine-scale socio-cultural factors highlighted by archaeological and anthropological studies5,6,7,8. The first socio-cultural model proposed to explain the Y chromosome bottleneck involved violent competition between patrilineal kin groups and the killing of large numbers of men9. Thus, Zeng et al.9 simulated a human population structured into competing patrilineal kin groups. In this model, kin groups—referred to as descent groups in the present article, following Fox’s terminology10—are genetically homogeneous for the Y-chromosome because men in the same group share a recent common paternal ancestor. Violent competition between these different patrilineal groups results in the extinction of certain groups. By increasing the rate of loss of Y-chromosomal lineages and accelerating genetic drift, it induces a severe decrease of Y-chromosome diversity.
However, it is questionable whether violence is necessary to explain the genetic signal observed by Karmin et al.1 as the level of violence worldwide at these times remains uncertain (Zeng et al.’s model assumes that 15% of males were killed at each generation9). Using ethnographic and/or archaeological data, some authors have claimed that Pleistocene hunter-gatherers exhibited low levels of warfare11,12, while others came to the opposite conclusion13,14,15, fuelling the long-standing debate between Rousseauians and Hobbesians about human nature16. Furthermore, a study based on data from various archaeological sites in the Old World found that levels of violence remained stable from the time Homo sapiens diverged from other primates until the Bronze Age, but significantly increased during the Iron and the Middle Ages17. On the other hand, other studies have reported an increase in violence in more ancient periods, such as during the Early Neolithic in Central Europe18, and during the Copper Age and Late Bronze Age in the Middle East19. These inconsistencies likely result from the nature of the archaeological record, which suffers from numerous biases, including the particularly small sample sizes for the earliest periods. Moreover, although a large number of individuals have been found buried with weapons in the archaeological records of the Bronze Age, this does not coincide with an increase in interpersonal violence in either Europe or the Middle East, suggesting that the idealisation of the social persona of the warrior may not reflect an intensification of warfare19,20,21.
Previous studies have demonstrated that kinship systems, and particularly residence and descent rules, leave on their own a profound signature on uniparental genetic diversity without any need for violent competition22,23. For instance, patrilocality, a residence rule whereby a married couple settles in the house of the husband or his father, has been shown to reduce local Y-chromosome diversity compared to mtDNA, because men remain in their native village while women migrate between villages with their mtDNA upon marriage. This pattern was reported in various populations, such as hill tribes of Northern Thailand24,25,26, food-producers of Sub-Saharan Africa27, tribes of Western New Guinea28, and Sumatran populations29. On the other hand, matrilocality, the rule according to which the couple settles near the wife’s place of birth, is known to reduce diversity on mtDNA compared to the Y chromosome within groups (e.g. in the West Timor population30, Ngazidja of Comoros Islands31, and South-East Asian populations32).
The patrilineal descent rule, according to which individuals are affiliated with the descent group of their father, is also known to reduce Y-chromosome diversity. Indeed, within patrilineal lineages or clans, men are closely related on paternal genealogical lines and share similar Y chromosomes33,34,35,36. In Central Asia, present-day patrilineal populations were shown to have lower male than female effective population sizes37, along with reduced Y-chromosome diversity as compared to non-patrilineal (but patrilocal) populations36,38. These populations practice group exogamy, resulting in the migration of women between descent groups.
Here we test the hypothesis that the Y-chromosome bottleneck is the result of a global shift towards patrilineal systems, associated with the transition to new subsistence systems on all continents over the past 12,000 years. Supporting this hypothesis, previous work has shown that kinship systems covary with production systems. Marlowe12 showed that patrilocality is over-represented in contemporary non-forager populations (mainly farmers and herders) compared to forager populations (60% and 34% of populations, respectively). Similarly, patrilineal descent is over-represented in non-foragers compared to foragers (47% and 14%, respectively). This has been famously summarised by Aberle: ‘the cow is the enemy of matriliny’39. More recently, Holden and Mace confirmed that such relationships between subsistence and kinship systems exist in the Bantu populations even after correcting for the historical relationships between populations40. We can therefore assume that the emergence of agro-pastoralism was accompanied by a change in the kinship system through the practice of patrilineality and patrilocality. Two main hypotheses have been advanced to explain the relationship between subsistence strategies and kinship systems. According to structural functionalists, patrilocality and patrilineality arise when resources can be accumulated. Indeed, with movable property, prosperous men can offer a bride price to the parents of marriageable young women, rather than moving in with their in-laws for bride service. In this way, daughters are separated from their parents, while men remain in their place of birth after marriage. More generally, movable property is thought to empower men to resist matrilineal and matrilocal traditions41,42,43. According to evolutionary anthropologists, patriliny is more prevalent in wealth-accumulating societies because this inheritance rule is better suited to maximising reproductive success due to the higher reproductive potential of males compared to females40,44.
Two features of patrilineal systems may be particularly relevant for the evolution of uniparental genetic diversity. First, it was observed that in contemporary patrilineal populations not necessarily involved in violent conflict, demographic stochasticity cause some groups to grow over time as the number of descendants of the group founder increases, while other groups may die out by chance10. As Fox wrote, ‘it is the problem of all societies based on unilineal descent groups that these groups are subject to such fluctuations—some expanding and growing abnormally large, while others decline and become extinct’10 p.122. Differential access to resources and differences in social status between groups may reinforce this process, with the high-status groups having greater reproductive success than the low-status groups. This variance in reproductive success between descent groups has been observed, for example, in China, where high-status imperial lineages from the 18th to 19th centuries have higher growth rates and lower extinction rates compared to low-status patrilineages45. This has also been observed in north-west Ireland, where about one in five males is likely to be descended from a very powerful and long-lived early medieval dynasty: the Uí Neíll (see Supplementary Tables 1, 2 for a summary of the variance in growth rates and extinction rates reported for patrilineal lines and groups in the literature). In both cases, reproductive success is transmitted within descent groups, and groups with a high social status tend to have more children in each generation than groups with a low social status. Such variance in reproductive success between descent groups and its intergenerational transmission are expected to accelerate the growth of certain lineages and the extinction of others, at a faster rate than compared to a population with no difference in status.
Secondly, some patrilineal systems, known as segmentary patrilineal systems, are characterised not only by patrilineal descent but also by the segmentation (also called fission) of descent groups when they become too large10,46. These systems account for 14% of patrilineal systems according to ref. 39. Fissions are likely to occur in a lineal way, following paternal genealogical lines. In other words, paternally related men cluster together in the newly formed patrilineal groups47,48,49,50 (Supplementary Fig. 1). This type of fission has been shown to reduce genetic diversity within groups and to increase differentiation between groups more severely than random fission, where newly formed descent groups arise randomly without regard to paternal relatedness between men48. Although Zeng et al.’s model takes into account the fact that patrilineal descent groups experience fissions, these events are modelled as random fissions and not as lineal fissions9. Lineal fission, because it clusters paternally related men together, is expected to be more efficient than random fission at increasing Y chromosome similarity within groups. It accelerates the loss of Y-chromosome diversity as compared to random fission when groups become extinct.
In this study, we undertake a modelling approach to test our hypothesis that a transition to patrilineal organisations, linked to a worldwide change in subsistence strategies, may have triggered an important loss of Y-chromosome diversity and may be sufficient to explain the post-Neolithic Y-chromosome bottleneck reported by Karmin et al.1 without requiring a violent scenario. By simulating different socio-demographic models, we assess the effect of patrilocal residence and patrilineal descent on uniparental genetic diversity. We modelled both males and females and calibrated our mutation model for mtDNA and the Y chromosome using mutation rates from the literature, so that the relative levels of diversity in the simulated mtDNA and Y-chromosome data can be compared with those reported in the literature1,3,4. We integrated population structure by modelling a population structured into five villages. Fission was modelled as either lineal or random, with the former grouping males closely related on their paternal genealogical lines into new descent groups. We also accounted for the fact that different descent groups may have different growth rates, by calibrating such variance with data from studies of patrilineal lines or groups not mentioning warfare between them. Finally, we considered the possibility that descent groups may migrate to another village after a fission. To monitor the change in male and female effective population sizes in our model, we used two different methods that were previously reported in the literature. The first method, similar to the one used by Zeng et al.9, is to calculate uniparental genetic diversities at multiple time points. The second method, which was used in Karmin et al.1, is a Bayesian method based on coalescent, inferring the change in effective population size from contemporary individuals. We show that variance in reproductive success between patrilineal groups, combined with lineal fission, can lead to a substantial reduction in the male effective population size without resorting to the violence hypothesis. Thus, a peaceful explanation involving a shift in ancient social structures in relation with the rise of agro-pastoral subsistence strategies may be sufficient to explain the reported decline in Y-chromosome diversity.
Ironically, by the time the Bible tales were being made up, a patriarchal, patrilineal society was assumed to be the normal for human societies, so, not surprisingly, they wrote about a god who ordered such a society, just as they made up tales to explain everything else in their world, that they took for granted and assumed it had always been thus.
We now know better. It's just that a few people don't know what we now know.
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