Latent admixture causes spurious serial founder effect

There is a series of interesting papers on Amerindian populations in the early view section of the American Journal of Physical Anthropology. One of them struck my interest, because it deals with an issue that has been a familiar topos of this blog, and has, in my opinion, much greater potential applicability than the settlement of the Americas.

The basic idea of the paper is the following: the serial founder effect (SFE) is a model, whereby populations expand by successive splits, with daughter populations expanding and colonizing new territories. It is a tree model, with the nodes furthest from the root representing late founder populations, and the ones closest to the root representing early splits close (geographically and temporally) to the initial colonization impetus.

Gene identity is the probability that two random alleles from either two individuals in a population, or from two individuals from different populations will be identical. This has been used to argue for a SFE in the Americas, because it apparently matches expectations: the most basal populations are in north America, and gene identity increases toward south America.

However, the authors of the current paper show that the observed pattern is due to European admixture in native American populations; this makes the north American populations (that are more European-admixed and hence more different than the rest) appear both more basal and more diverse.

From the paper:

Many aspects of the pattern of neutral genetic variation in the Americas are consistent with the predictions of the serial founder effects process. The NJ tree is rooted in northern North America, it shows a northsouth pattern of internal branching, and gene identity within populations increases steadily with increasing geographic distance from Beringia. However, admixture with Europeans could account for all of these features. The tree is rooted in northern North America because the gene identities between the three northern North America populations and the other Native American populations are particularly low (Fig. 2). European admixture has contributed to this low identity, and, in principle, it could account for the position of the root. The Admixture tree (Fig. 5A) topology indicates that the north-south pattern of branching in the NJ tree might be the result of relatively high admixture in northern North America, intermediate levels in Central America and northern South America, and low levels in eastern South America. The partial correlation analyses show that the north-south increase in gene identity within populations can also be explained by geographically patterned admixture (Table 2). We conclude that geographically patterned admixture between Native Americans and Europeans has obscured our ability to reconstruct precontact evolutionary processes in the Americas.

Of course, this is an extremely important piece of work that future studies of Amerindian populations must take into account. It is no longer feasible to interpret the observed gene identity pattern in the Americas as a remnant of the migration and spread of Amerindian ancestors thousands of years ago. It is more likely a result of much more recent events, namely the different intensity of European admixture in post-1492 times.

Hunley and Healy is important not only for the Americas, however. The serial founder effect has been evoked to explain both the spread of modern humans from east Africa, as well as more recent Neolithic expansions in different parts of the world. We must now be vigilant that these patterns may, in part, be the result of latent admixture.

In the Americas, we know (from historical documents) that this admixture took place, and we have relatively unadmixed populations still in existence. But, there may very well have been admixture events before the birth of history, and many ancestral populations may no longer exist in unadmixed form. So, we may be interpreting patterns of modern human variation as the result of ancient colonization processes, oblivious to the presence of latent admixture.

For example, there is an increase in gene identity from eastern Africa through Arabia, and India, all the way to Siberia, and southward across the Americas. Hunley and Healy deal with the latter part of this cline, but the whole of it has been interpreted as evidence of an orderly Out of Africa colonization as a series of founder effects.

However, the Eurasian portion of the pattern may also be spurious: current east Africans, for example, are partially admixed, both with West Eurasians and with people from other parts of the continent. Likewise, Arabians often have African admixture, whereas South Asians have been convincingly shown to be largely 2-way mixes of West Eurasians and "Ancestral South Indians". To top it all off, we now have convincing evidence that archaic admixture may have played a role in the evolution of some living Africans: this would furthermore increase their gene diversity and contribute to a perceived Eurasian cline.

Tree models are orderly and well-behaved. It would be great if people behaved that way, because the math would be easier. But, people aren't laboratory mice that follow predefined paths in a maze: they mix with their neighbors, they split and move forward, but sometimes, they split and move backward. Hopefully, H&H's paper will lead to an increased appreciation of admixture in the human story, beyond the case of the Americas.

AJPA DOI: 10.1002/ajpa.21506

The Impact of Founder Effects, Gene Flow, and European Admixture on Native American Genetic Diversity

Keith Hunley and Meghan Healy

Abstract
Recent studies have concluded that the global pattern of neutral genetic diversity in humans reflects a series of founder effects and population movements associated with our recent expansion out of Africa. In contrast, regional studies tend to emphasize the significance of more complex patterns of colonization, gene flow, and secondary population movements in shaping patterns of diversity. Our objective in this study is to examine how founder effects, gene flow, and European admixture have molded patterns of neutral genetic diversity in the Americas. Our strategy is to test the fit of a serial founder effects process to the pattern of neutral autosomal genetic variation and to examine the contribution of gene flow and European admixture to departures from fit. The genetic data consist of 678 autosomal microsatellite loci assayed by Wang and colleagues in 530 individuals in 29 widely distributed Native American populations. We find that previous evidence for serial founder effects in the Americas may be driven in part by high levels of European admixture in northern North America, intermediate levels in Central America, and low levels in eastern South America. Geographically patterned admixture may also account for previously reported genetic differences between Andean and Amazonian groups. Though admixture has obscured the precise details of precontact evolutionary processes, we find that genetic diversity is still largely hierarchically structured and that gene flow between neighboring groups has had surprisingly little impact on macrogeographic patterns of genetic diversity in the Americas.

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