Ancient Africa may not have had as much deep structure as we think

A weakly structured stem for human origins in Africa:

While it is now broadly accepted that Homo sapiens originated within Africa, considerable uncertainty surrounds specific models of divergence and migration across the continent. Progress is hampered by a paucity of fossil and genomic data, as well as variability in prior divergence time estimates. Here we use linkage disequilibrium and diversity-based statistics, optimized for rapid, complex demographic inference to discriminate among such models. We infer detailed demographic models for populations across Africa, including representatives from eastern and western groups, as well as 44 newly whole-genome sequenced individuals from the Nama (Khoe-San). Despite the complexity of African population history, contemporary population structure dates back to Marine Isotope Stage (MIS) 5. The earliest population divergence among contemporary populations occurs 120-135ka, between the Khoe-San and other groups. Prior to the divergence of contemporary African groups, we infer long-lasting structure between two or more weakly differentiated ancestral Homo populations connected by gene flow over hundreds of thousands of years (i.e. a weakly structured stem). We find that weakly structured stem models provide more likely explanations of polymorphism that had previously been attributed to contributions from archaic hominins in Africa. In contrast to models with archaic introgression, we predict that fossil remains from coexisting ancestral populations should be morphologically similar. Despite genetic similarity between these populations, an inferred 1–4% of genetic differentiation among contemporary human populations can be attributed to genetic drift between stem populations. We show that model misspecification explains variation in previous divergence time estimates and argue that studying a suite of models is key to robust inferences about deep history.

Privately some people have been grumbling about models of deep structure between very differentiated populations for a while. They claim this is just a bias in the model specifications because it’s so easy to think of gene flow happening in periodic pulse admixtures. But the reality is that Africa doesn’t seem to have had the same barriers as across Eurasia or between Eurasia and Africa, so how are these deep lineages persisting?

The preprint here shows that the data can fit a different model, one that they find more biologically and paleoanthropologically more reasonable. The discussion has an “out of Africa with total replacement” flavor, but here it is within Africa:

Multiple studies have shown a correspondence between phenotypic differentiation, usually assessed with measurements of the cranium, and genetic differentiation among human populations and between humans and Neanderthals 36,37,38 (see also Section 5.3). This correspondence allows predictions of our model to be related to the fossil record. The fossil record of Africa is sparse during the time period of the stems, but of the available fossils, some are very similar in morphology to contemporary humans (e.g., from Omo Kibish, Ethiopia 39,40), others are similar in some morphological features but not others (e.g., from Jebel Irhoud, Morocco 1,41), and others are very different in morphology (e.g., from Dinaledi, South Africa 42,43). If, as our model predicts, the genetic differences between the stems were comparable to those among contemporary human populations, the most morphologically divergent fossils are unlikely to represent branches that contributed appreciably to contemporary human ancestries.

This result would recenter Omo Kibish from what I can tell.

Recent human origins in 2021

I wrote three long pieces for my Substack:

  1. Yo mama’s mama’s mama’s mama… etc.
  2. Our African origins: the more we understand, the less we know ($).
  3. What happens in Denisova Cave stays in Denisova Cave… until now ($).

I’m thinking about where I’m going to go in relation to this topic, and i think it may be in the direction of Eurasian back-migration to African and what we know now.

Also, I’m at nearly 60 podcasts after more than a year of the Substack. Please remember to rate it positively.

Through northern Arabia

Multiple hominin dispersals into Southwest Asia over the past 400,000 years:

We have identified at least five pulses of human dispersal into northern Arabia, each associated with a phase of decreased aridity. The differences in material culture between these phases—with two phases of Acheulean technology and then three distinct forms of Middle Palaeolithic—suggests that diverse hominin populations, and probably even species, were expanding into the region at different times…

From the supplements:

Little is known of the Pleistocene fauna of southern and eastern Arabia, but the repeatedly distinctive, localised, character of material culture suggests that crossing the Red Sea at the Bab al Mandeb was not a primarily dispersal route and that instead populations filtered through northern Arabia. In northern Arabia the growing fossil record suggests repeated connections to Africa across a contiguous grassland zone through the southern Levant which formed during repeated humid episodes (discussed in SI 10). To that we can add significant aspects of material culture which we have reported in this paper. The absence of Acheulo-Yabrudian assemblages in northern Arabia, and the southern Levant, suggests that the Late Acheulean in this area relates more to Africa than to areas to the north. Likewise, with the early Middle Palaeolithic at KAM-4 (Assemblage C of the Northwest Lake) both technological features (such as the methods of Levallois surface preparation, see SI 7) and quantitative characteristics in terms of PCA of Levallois flake shape situate the assemblage between the Levantine Early Middle Palaeolithic the early Middle Stone Age in East Africa (SI 9)…

…The possible MIS 3 presence of Neanderthals in Arabia may suggest that they expanded further south than previously thought, and highlights that there is currently little clarity on where the main pulse of admixture between Homo sapiens and Neanderthals occurred, beyond probably Southwest Asia broadly.

As a closing note, we emphasise that as well as our results being consistent with repeated pulses of hominin dispersal out of Africa into Southwest Asia, the possibility of movement in the reverse direction should be kept in mind. Given factors such as current uncertainty on the background to the earliest known Homo sapiens in Africae, and discussions on the possible
involvement of a hominin closely related to Homo antecessor as an ancestor of our species, currently only known from Eurasia, as a precursor to Homo sapiens, building reliable records for the later Quaternary in Southwest Asia is not only important for understanding ‘out of Africa’ dispersals, but also for ‘into Africa’ dispersals.

Was H. luzonensis Denisovan?

Philippine Ayta possess the highest level of Denisovan ancestry in the world:

Multiple lines of evidence show that modern humans interbred with archaic Denisovans. Here, we report an account of shared demographic history between Australasians and Denisovans distinctively in Island Southeast Asia. Our analyses are based on ∼2.3 million genotypes from 118 ethnic groups of the Philippines, including 25 diverse self-identified Negrito populations, along with high-coverage genomes of Australopapuans and Ayta Magbukon Negritos. We show that Ayta Magbukon possess the highest level of Denisovan ancestry in the world—∼30%–40% greater than that of Australians and Papuans—consistent with an independent admixture event into Negritos from Denisovans. Together with the recently described Homo luzonensis, we suggest that there were multiple archaic species that inhabited the Philippines prior to the arrival of modern humans and that these archaic groups may have been genetically related. Altogether, our findings unveil a complex intertwined history of modern and archaic humans in the Asia-Pacific region, where distinct Islander Denisovan populations differentially admixed with incoming Australasians across multiple locations and at various points in time.

T: The Story of Testosterone, the Hormone that Dominates and Divides Us

Carole Hooven has a new book, T: The Story of Testosterone, the Hormone that Dominates and Divides Us. I’ll be honest and admit I was only vaguely aware of the book until yesterday when a social media controversy erupted over her “transphobic comments” on Fox & Friends. You can watch the clip yourself, and see that she’s not transphobic at all.

I assume though the accusation will be enough to open some Title IX complaints. Unless her colleagues step up I assume she’ll be hounded out by the bureaucracy, though I hope I’m wrong.

Hooven has been all over the media, just see what she’s RTed on her Twitter account. She makes it pretty clear she’s not going to back down on the scientific questions and answers. Which is how it should be, but that sort of stance is far less common than groveling obeisance before the new red guards.

More and more evidence for ‘complex demography’ in archaic ancestry

An ancestral recombination graph of human, Neanderthal, and Denisovan genomes:

We note that our estimated TMRCA to Neanderthal within Neanderthal-introgressed segments in all non-African populations is recent, ~74 ka ago, and implies therefore that little genetic drift separates admixed humans from sequenced Neanderthals in these segments. This recent TMRCA suggests that the majority of Neanderthal ancestry in modern humans originated from Neanderthal gene flow into the ancestors of all non-Africans before populations diversified. It also suggests that at least one of the Neanderthal genomes used here is closely related to the Neanderthal(s) involved in this admixture event. The slightly elevated Neanderthal ancestry that others have described in Central and East Asian populations also appears to have originated in this first pulse, as Central and East Asian Neanderthal haplotypes are mostly shared with other, geographically distant populations. This observation favors the hypothesis that the increased Neanderthal ancestry in these populations relative to others is due to weaker selection against alleles that may be mildly deleterious (32), made possible because of smaller historical population sizes in this part of Eurasia, rather than to additional admixture events (22). Our evidence of many small-scale, population-specific admixture events, however, together with a simulation study that found a single-pulse admixture model followed by drift unable to explain the discrepancies in admixture proportions in European and Asian genomes (49), hints at a complex history of admixture throughout Eurasia not fully captured by either of these two hypotheses.

I don’t think that it’s weaker selection in East Asians. I think it’s complex demography.

Complex admixture of “Denisovans” in Southeast Asia and Sahul

A new paper, Genomic insights into population history and biological adaptation in Oceania, is worth reading. Read it along with Multiple migrations to the Philippines during the last 50,000 years and Multiple Deeply Divergent Denisovan Ancestries in Papuans.

I’m going to sidestep the new inference that Austronesian expansion may predate the movement out of Taiwan. I’ll revisit. Rather, let’s reflect on the Denisovans. There is strong evidence of more than one admixture from this lineage into modern humans. And, multiple papers now support a model where various Southeast Asian groups have several different pulses. Finally, the “Denisovans” have really deep divergence. Way deeper than anything in modern humans.  Some of them split right after the west-east Eurasian hominin split.

All this is curious in light of small hominins in the Philippines and Flores, as well as late ‘erectus.’ I think it is likely that some of the Denisovan lineages have ‘super-archaic’ admixture, while some of the gene flow is mediated by highly admixed moderns with high Denisovan load.

The great panmixia

Human inbreeding has decreased in time through the Holocene:

The history of human inbreeding is controversial. The development of sedentary agricultural societies may have had opposite influences on inbreeding levels. On the one hand, agriculture and food surplus may have diminished inbreeding by increasing population sizes and lowering endogamy, i.e. inbreeding due to population isolation. On the other hand, increased sedentism, as well as the advent of private property may have promoted inbreeding through the emergence of consanguineous marriage customs or via ethnic and caste endogamy. The net impact is unknown, and to date, no systematic study on the temporal frequency of inbreeding in human societies has been conducted. Here we present a new approach for reliable estimation of runs of homozygosity (ROH) in genomes with ≥3x mean coverage across >1 million SNPs, and apply this to 440 ancient Eurasian genomes from the last 15,000 years. We show that the frequency of inbreeding, as measured by ROH, has decreased over time. The strongest effect is associated with the Neolithic transition, but the trend has since continued, indicating a population size effect on inbreeding prevalence. We further show that most inbreeding in our historical sample can be attributed to endogamy, although singular cases of high consanguinity can also be found in the archaeogenomic record.

I think it is hard to think this is unrelated to decreased pairwise Fst between populations over the Holocene. Fst is a statistic that measures the proportion of genetic variation across two populations in relation to the total variance. In a Pleistocene world of small clans occupying a thinly populated landscape, one can envisage a scenario where gene flow is far more viscous than the more sedentary, but interconnected, world of agriculturalists.

Hunter-gatherers were probably not more xenophobic. Rather, increasing populations by an order of magnitude increases the number of potential geographically close mates a lot.

Another consequence of more gene flow and more partners is that inbreeding also declines, as people have more recent ancestors in their pedigree.

The main caveat I would put into this though is that this applies to dense Eurasian time transects. There is some reason to think that hominins on the northern Eurasian fringe were always on the knife’s edge of sustainability.

Neanderthal Y chromosomes are paleo-modern?

I don’t have time to blog in detail today so I’ll point you to Ann Gibbon’s story, How Neanderthals lost their Y chromosome. You can find the link to the paper in there. The big issue here is that both mtDNA and Y chromosomes were replaced due to introgression from a population closer to modern humans than the Neandersovans, though basal to any modern humans alive today. This new group may actually be basal to the “basal human” group hypothesized by some scholars (there are suggestions of its existence in autosomal admixture into Neanderthals).

The probability of fixation of a newly introduced allele is the frequency of that allele, so how is it that these paleo-modern variants swept into Neanderthals? Perhaps on one locus, but two? One solution offered is naturals selection. This seems plausible, but the possibility of natural selection on Y and mtDNA lineages has always been a “wild card” that would make us rethink a lot of our phylogeography in general.

Finally, though it looks like the vast majority of modern ancestry outside of Africa is derived from a relatively recent (60,000 years ago) rapid expansion, it is clear that the picture at any given time is more complex than the signal we see today. It seems more and more likely that there was more a continuum between the African and Neandersovan lineages, and I strongly suspect that some of the paleo-modern lineages will at some point be detected in some modern groups once we have ancient DNA (the closer genetic distance and low fraction makes it hard for these segments to be identified in extant modern lineages using standard inference).

ABO introgression from Eurasian hominins

One of the oldest group of loci investigated for variation in humans are the ABO antigen markers. There are several reasons for this. First, you can assay them with pre-DNA methods. Second, they vary a lot. Third, they’re very important for things like blood donation.

The fact that they vary a lot means that researchers in the early 20th century used these markers to try and figure out population history. This was not workable for two reasons. First, looking at a locus here and there is not really informative. Y and mtDNA have special characteristics, but even these markers are really informative in a broader context. Second, the ABO locus is subject to natural selection. More precisely, it looks like a lot of immunological markers the ABO locus is subject to balancing selection which keeps it quite diverse.

What does this mean? Basically, variation at any locus is going to turnover. All the polymorphism will “coalesce” back to a common ancestor. The date of coalescence is going to be conditional on parameters such as genetic drift, and selection. Strong sweeps mean all the variance is removed and the coalescence is shallow. Similarly, bottlenecks mean short lifetimes for lineages, since drift cranks away variation. Balancing selection results in the opposite effect. At immunological loci the coalescence is often deeper than the time between the separation of species. The reason is that frequency-dependent selection prevents rare alleles from going extinct (the fitness goes up the rarer the allele).

This is the context of a new preprint, ABO genetic variation in Neanderthals and Denisovans:

Variation at the ABO locus was one of the earliest sources of data in the study of human population identity and history, and to this day remains widely genotyped due to its importance in blood and tissue transfusions. As one of the first genetic markers, variation at the ABO gene has been studied for over 60 years, and yet there are some aspects of its evolution that remain mysterious. Here, we look at ABO blood type variants in our archaic relatives: Neanderthals and Denisovans. Our goal is to understand the genetic landscape of the ABO gene in archaic humans, and how it relates to modern human ABO variation. We analyze coding variation at the ABO locus from next-generation sequences in ~2,500 individuals from 28 populations, including three Neanderthal and one Denisovan individuals. We use the modern human haplotypes to impute ABO genotypes for the four archaic human genomes. We found that the Siberian Neanderthals, Altai and Chagyrskaya, are both homozygous for a derived Neanderthal variant of the O allele, while the European Neanderthal, Vindija, is a heterozygote for two derived Neanderthal variants, an O variant different from Altai and Chagyrskaya, and a rare cis-AB variant. The Denisovan individual is homozygous for an ancestral variant of the O allele, similar to variants found widely in modern humans. Perhaps more surprisingly, the derived O allele variant found in the Altai Neanderthal can be found at low frequencies in modern European and Southeast Asian individuals, and the derived O allele variant found in the Vindija Neanderthal is also found at very low frequency in East Asian individuals. Our genetic distance analyses suggests both alleles were introgressed through Neanderthal-human gene flow. In summary, our study identifies the genetic variation of the ABO gene in archaic humans, we find that ABO allele diversity in Neanderthals was likely high, and that some of these alleles still survive in modern humans due to inbreeding with Neanderthals.

The results are in alignment with theoretical expectations (which were probabilistic though). Alleles from these Eurasian hominins are probably beneficial in some way. Admixture with diverged lineages is a way to “rescue” diversity that may have been lost. The interesting point in the discussion though is that the Neanderthal population that the rare alleles were obtained had more variation than the small samples of European and Altai Neanderthals that we have now. This is not surprising, as it was probably a Near Eastern extension of European Neanderthals, and may even had have a larger long-term effective population than the groups further north.