Matrilineal networks may be the key to understanding Neanderthal mixture
A new study focusing on the X chromosome finds repeated maternal dispersal bias in Neanderthal and modern evolution.
News sources this week tell us that “modern human women preferred Neanderthal men”. One story added, “the results do not indicate whether mating was consensual”. AI-painted images of star-crossed Pleistocene lovers are making eyes at each other up and down my social feeds.
As usual headline writers have tried to make the research sexy. The actual result is less titillating but even more interesting. In the center of these stories is the strongest genetic test yet showing that Neanderthals and the African ancestors of modern people were the same biological species.
The results may also give one of our best opportunities to understand the social factors that helped modern human populations expand and disperse throughout the world.
Did Neanderthals find human traits hotter in women than men?—Canadian Broadcasting Company
Introgression one way
The new research comes from Alexander Platt, Daniel Harris, and Sarah Tishkoff, published this week in Science. Building on earlier work by their team, these authors looked closely at the Neanderthal ancestry on the X chromosome compared to the autosomes.
This is well-worn ground. In 2014, Sriram Sankararaman and coworkers showed that X chromosomes of today’s people have a lot less Neanderthal ancestry than the 22 pairs of autosomes. The X chromosome is also home to more large genomic segments that are almost devoid of Neanderthal ancestry—called “introgression deserts”.
One hypothesis proposed at the time was partial hybrid incompatibility between the expanding population of modern people and the Neanderthals they met. This could fall into a broader pattern known as Haldane’s Rule.
Haldane’s Rule explained: When two populations divide and are isolated for a long time, they may start to evolve reproductive incompatibilities—as these evolve, they are the basis of speciation. Hybrids of the two populations may exhibit sterility or reduced fertility. When such problems emerge, they are more likely to manifest in the sex with two different sex chromosomes—in humans, this is males with the XY genotype—than in the sex with two of the same sex chromosome—in humans, females with the XX genotype. This happens because males have the full phenotypic effect of any X chromosome allele—even when it causes sterility—while females have a second copy of the X that may mask or moderate some phenotypic effects. More generally, deleterious X chromosome alleles are more exposed to selection due to effects in XY individuals than XX individuals. This works in the opposite direction in birds, where males have a WZ genotype and females a ZZ genotype, and it was J.B.S. Haldane who generalized based on homogametic and heterogametic sex chromosome genotypes.
When Sankararaman and coworkers noticed the lower Neanderthal ancestry of the X chromosome, they suggested that this might be the result of reduced fertility of hybrid males. Such a reduction in fertility would be a strong sign that the process of speciation in modern humans and Neanderthals had come to the point where they should be considered distinct biological species.
This is the kind of result that I take very seriously. Speciation in sexual organisms is about reproduction. If hybrid offspring of two populations have reduced fertility or sterility, those populations are different species.
But as I noted at the time, there are other possible explanations for the reduced Neanderthal ancestry on the X chromosome. Neanderthals had a long-term smaller population size than African ancestors of modern people, resulting in a genetic load of weakly deleterious Neanderthal alleles. From today’s vantage point—more than 1500 generations after the populations mixed—slow, weak selection against many slightly deleterious X chromosome alleles is hard to tell apart from hybrid male reduced fertility across a single generation.
There’s also the positive selection on the X chromosome. Just as the X chromosome is more exposed to purifying selection against deleterious alleles, it can also more quickly register positive selection on beneficial alleles. This effect has transformed human X chromosomes, resulting in lower diversity than the autosomes and greater differentiation across living human populations. Work by Laurits Skov and collaborators in 2020 showed that the early modern dispersal into Eurasia was accompanied by strong selection on advantageous X chromosome alleles. That effect may have wiped out a lot of Neanderthal variation.
So, I’ve been a Haldane holdout. My feeling has been reinforced lately by the evidence that mixture with Neanderthals took place over a large geographic range as modern people dispersed. It’s hard to maintain the notion of hybrid incompatibility when the groups met and mixed continuously.
When we interbred with Neanderthals, they were usually the fathers—New Scientist
Introgression the other way
The new research by Platt, Harris, and Tishkoff adds a much older period of intermixture to the story. The paper builds on earlier work by this team, led in 2023 by Harris, that looked at the mixture of African people into the Neanderthal population around 250,000 years ago.
This 250,000-year-old period of African dispersal has been coming into focus for more than a decade. The first clue was a greater degree of genomic similarity of the “Altai Neanderthal” (Denisova 5) genome and African peoples, compared to the “Denisovan” (Denisovan 3) genome. Later, geneticists understood that when it comes to Neanderthal-modern differences, there is a large genomic discrepancy between the autosomes on the one hand and the mitochondrial DNA and Y chromosome on the other. Both these genetic systems were adopted wholesale by Neanderthals from African ancestors sometime around 250,000 years ago. Along with them came around 6% of the genome as a whole. Every Neanderthal after that time—roughly, the age of the Petralona skull and 200,000 years after Sima de los Huesos—was part African.
As data have grown, it has become possible to study this early episode of introgression in more detail. The new study asks quite a simple question: Did this early introgression of African DNA into Neanderthals have the same consequences for the X chromosome as the later introgression of Neanderthal DNA into modern humans?
The answer is no. In fact, the pattern was exactly the opposite. There was no reduction of X chromosome introgression into Neanderthals, there was a big increase.
It’s like the mirror image of the later contacts of Neanderthals and modern humans. Haldane’s Rule would predict a similar fate for the X chromosome in both cases of introgression. Instead, it seems that the X chromosomes of African ancestral groups had a big advantage in both these periods of population mixture, regardless of whether they expanded with the modern population or were absorbed by the Neanderthal population.
Platt and coworkers note that this is not what would be predicted by reduced fertility of male hybrids, nor is it what the selection hypotheses predict. I underline those conclusions: The early introgression pattern is absolutely not what you’d expect from two populations that had started the process of speciation.
The authors suggest that a long-term sex bias in mating between the populations might produce the effect they found. Introgression into modern groups was male-biased, and introgression into Neanderthal groups was female-biased. A single long-term mating bias, with pairings of Neanderthal men and modern women more likely than the opposite, would generate these observations.
Prehistoric human women had the hots for Neanderthal dudes—IFLScience
An unusual pattern
In both these periods of time, it was the African newcomer population that was expanding, and Neanderthals who had long resided in the regions. In both cases the women of the expanding group were more likely to mate with men of the resident group. That pattern cuts against the grain of most historic and prehistoric cases of human population contact.
In recent cases, geneticists have not generally traced the X chromosome but instead the mtDNA and Y chromosome due to the greater resolution of haplotype frequency data compared to X-single nucleotide polymorphisms (SNPs). Y chromosome haplotypes trace male-mediated migration and relationships; mtDNA traces female-mediated migration and relationships.
In historic and prehistoric population dispersals and contacts, the strongest pattern is often the arrival of new Y chromosome haplotypes. When Bronze Age populations from the Eurasian steppe entered central and western Europe, the Y chromosomes of some resident populations were almost entirely lost, while Y chromosome lineages of steppe origin became very common. The mitochondrial DNA variation was much less affected by newcomer lineages, reflecting a disproportionate impact of the incoming men and greater incorporation of resident women. The same pattern happened when Vikings arrived in Ireland, when European populations established colonies in the Americas, and when Bantu-speaking peoples dispersed into southern Africa and mixed with Khoesan-speaking hunter-gatherers and herders.
Still, the opposite pattern with female-mediated migration and gene flow has sometimes transpired. This was the pathway of early emergence of Polynesian peoples. People speaking Austronesian languages with Asian mitochondrial lineages expanded into near Oceania, meeting and combining with Melanesian peoples, whose Y chromosome haplotypes became common in the ancestral Polynesians. A similar case may be the growth and dispersal of Muskogean-speaking populations of the southeastern United States.
In cases like these, the political and economic organization of the expanding group is based in matrilineal clan or descent networks. The members of the culture reckon their kinship, loyalty, and affinity by their mothers and more distant maternal kin.
In anthropological theory, these different modes of organization and patterns of migration and dispersal are connected to subsistence and technology. Patrilineal migration and dispersal are often tied to mobile measures of wealth, like cattle and horses, as well as situations where technologies provide a warrior elite with mobility and the means of conquest. Expansion and dispersal of matrilineal networks is possible when fertility itself is of higher value, when the linguistic and cultural ties around community can be maintained by strong political consensus even as men from differing groups are integrated into the cultural group.
A matrilineal dispersal hypothesis
The X chromosome results are not an invitation to think in absolutes. Human societies—even small-scale human societies that hunt and gather wild foods—have always been varied in their residence patterns, kinship, and political structures. Neanderthal societies could not all have been cut from the same cloth, certainly not across thousands of miles and up to 200,000 years. As groups of these peoples came into contact with each other, some would have been culturally aligned, some ready for exchanges of communication and marriages, others less compatible or much more reticent for such contacts.
All this makes it unlikely that the same mating bias would carry across any very large geographic area, or that the same phenomena would unfold in a similar way 200,000 years apart. Yet, the data suggest that broadly similar patterns did unfold.
This is not a matter of cultural preference. But it may be a function of the kind of social organization that sometimes made growth and dispersal of early modern populations possible.
Around 50,000 years ago, a branch of the African ancestral population underwent a significant founder effect before dispersing north, west, and east from southwest Asia. This movement was a demic expansion characterized by continuous population growth along its entire trajectory. Marriage networks during this period occasionally incorporated Neanderthals, with unions between male Neanderthals and female modern humans being significantly more common.
An earlier period of contact, occurring more than 250,000 years ago, had a different demographic outcome. During this phase, the Neanderthal population did not suffer a global decline, and the expansion of modern human groups eventually stalled without population replacement. However, this contact was sufficient to cause a complete replacement of Neanderthal mitochondrial DNA and Y-chromosome variation with modern human lineages. The female-centered nature of this interaction is evidenced by a relative excess of African ancestry on the X chromosomes of all later Neanderthals compared to their autosomes.
In neither case was the pattern of gene flow exclusively female-mediated. If for no other reason, we know this because of what happened to their Y chromosomes: If either period of contact was exclusively female-mediated, then the African Y chromosome would not have replaced the indigenous Neanderthal Y chromosome variation.
These expansions could not have been exactly like recent expansions of matrilineal groups. But the circumstances of such recent expansions may provide some very useful insights. Consider:
Expansion of groups into the ranges of existing resident populations relies on cultural solidarity and high-fidelity cooperation along kinship networks. Matrilineal organization typically keeps cultural and genetic means of reckoning connections aligned across more generations than patrilineal systems.
Extra-group marriages likely enabled land-use rights and strategic alliances. A beneficial side-effect of these pairings is the introduction of locally adaptive genes, such as those related to immune response, environmental factors, or local foods.
Collective foraging strategies facilitate exploitation of a somewhat broader range of local resources, making it possible to grow into spaces that the resident population may find subsistence more marginal.
Disease and immunity—especially maintaining fertility rates in the presence of disease—may be an initial block to expansion and dispersal, but once local genes or cultural strategies are taken onboard, growth itself provides a snowballing advantage over other resident populations.
The newcomer and resident populations are never incompatible, but as the expanding population grows, their mixture has less and less impact on the subsequent gene pool. The genetic patterns most strongly reflect the earliest contacts.
The matrilineal expansion hypothesis may help explain why Neanderthal-modern contacts did not follow the same patterns as the male-mediated dispersals of later agricultural or pastoral peoples, which are typically associated with paternal networks and “elite dominance” models.
Many anthropologists over the years have thought that matrilineal organization may have been the ancestral mode for early humans. Right now there’s not much hard data to test this idea. But the increasing resolution of kinship studies from ancient DNA have shown some advances, including the identification of kin at Chagyrskaya Cave, which shows some evidence of female-biased migration. It will be a major advance if genomic data from African and Near Eastern sites such as Klasies River Mouth or Qafzeh may add information about early African ancestral humans.
References
Harris, D. N., Platt, A., Hansen, M. E. B., Fan, S., McQuillan, M. A., Nyambo, T., Mpoloka, S. W., Mokone, G. G., Belay, G., Fokunang, C., Njamnshi, A. K., & Tishkoff, S. A. (2023). Diverse African genomes reveal selection on ancient modern human introgressions in Neanderthals. Current Biology. https://doi.org/10.1016/j.cub.2023.09.066
Harris, K., & Nielsen, R. (2016). The Genetic Cost of Neanderthal Introgression. Genetics, 203(2), 881–891. https://doi.org/10.1534/genetics.116.186890
Platt, A., Harris, D. N., & Tishkoff, S. A. (2026). Interbreeding between Neanderthals and modern humans was strongly sex biased. Science, 391(6788), 922–925. https://doi.org/10.1126/science.aea6774
Sankararaman, S., Patterson, N., Li, H., Pääbo, S., & Reich, D. (2012). The Date of Interbreeding between Neandertals and Modern Humans. PLoS Genetics, 8(10), e1002947. https://doi.org/10.1371/journal.pgen.1002947
How sure are we that later Neanderthal uniparentals are introgressed from Africans and not the other way around? My understanding of that initial claim is that earliest Nean and Denisovan uniparentals are a clade, but that later Nean uniparentals are more similar to modern humans. What makes it impossible that those uniparentals originated in Neanderthals and introgressed into Africans?