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Caribbean Genomics

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Father of Lies

Father of Lies

More often than not the discipline of history seems to swing between the true and trivial (or perhaps more precisely, picayune), and grand narratives which emphasize a nearly fictionalized story. In some ways this is not entirely a problem. When teaching young children the history of the United States a punctilious adherence to fact is essential, but, one can not deny that the selection of topicality can sway and shade the direction of the lessons learned. But far too often this ideological element of the historical narrative determines the central focus, rather than floating along the margins. With erudite command of detail historical scholars can, if they so choose, engage in a game of ideological sophistry, cultural flattery, and underhanded polemic. Both Howard Zinn and David Barton were and are players at this game. But there are still those who engage in the Sisyphean task of perceiving the world as it is, not as we would wish it to be, through the dark glass. Such a colossal enterprise, to ascertain the objective character of an exceedingly complex phenomenon, requires every tool at hand. Historians have traditionally been hunters of musty texts in neglected libraries, but they have on many an occasion received auxiliary data from scholars working in more material domains, such as archaeologists and engineers. Today you must add geneticists to the growing brigade of scholars attempting to excavate the past.

It is known

It is known

In truth the power of genetics is most evident and necessary in areas where history is silent, before written records can build a narrative skeleton in which we can play. Using both modern and ancient DNA samples the geneticists, working with archaeologists, can still make vague inferences where before there was only darkness. But illumination can be had even in time periods when historical records are quite good. Though the public understands evolution to transpire over eons, basic population genetic processes occur over a matter of generations, and so can give us fresh insight into dynamics which played out quite recently in time. A new paper in PLoS GENETICS, Reconstructing the Population Genetic History of the Caribbean, does just this. Obviously we already have a history of the Caribbean. As every schoolboy knows it began in 1492, and proceeded across the centuries as a palimpsest of European colonial powers, and later independent nations, rose and fell. But history is more than just wars, international congresses, and once-in-a-generation discoveries. It is the ebbing and flowing of peoples themselves in their aggregate masses. Conventional textual narratives and coarse archaeological inferences can get us rather far. See Charles C. Mann’s magisterial 1493 for an example. But historical population genetics goes a step further, as it attempts to infer demography through patterns of variation in genes, the most elemental instrumental variable for tracing demographic patterns one might imagine.

journal.pgen.1003925.g004 What the above paper does is reiterate, emphasize, and clarify, particular population genetic demographic events which have been suspected. First, the Amerindian populations were not static creatures in equilibrium with nature, but dynamic. There is clear evidence in these results that some groups migrated from South America to Central America, and especially the Caribbean. This is not unreasonable a priori, but far too often our stylized models presume the Amerindian population as a homogeneous, uniform, almost ahistorical substrate upon which European agency and African tragedy can unfold. But on the contrary, the peoples of the New World had their own history, oral as it may be. As you can see the Maya, one of the most iconic of Amerindian peoples, seem to exhibit some southern affinities, perhaps the result of an ancient “back migration.” If the Old World is any guide there may have been many forward and back migrations.

journal.pgen.1003925.g004 This ancient legacy is evident in the admixed populations, the Mestizos, Zambos, and Mulattos of the Greater Caribbean region. Looking in particular at the Puerto Rican and Dominican populations you see low, but significant, levels of admixture from specific native groups. One the one hand you may not be surprised, but it must be stated that before the genetic evidence there was much skepticism as to whether any Amerindian genetic heritage persisted in the populations of the Caribbean. A particular style of cultural/humanistic scholar intuited that perhaps an emphasis on indigenous ancestry was a mechanism for people of some African ancestry to deflect attention away from this aspect of their heritage because of the fraught history of slavery. Though the internal logic here seems reasonable, the empirical evidence makes it clear that the legacy of the Amerindians does persist in these islands, among these peoples. Their motive may have been unpalatable, but their argument was right.

Who were these Amerindian people? And how did they become integrated with the synthetic populations which came to dominate these islands? This is where textual history and genetics operate in a complimentary fashion. Both history and ethnography document mass population collapse in concert with an androcide of the Amerindians. By this, I mean that European males took Amerindian women as concubines, and engaged in de facto polygyny in the New World. Hernan Cortes, conqueror of the Aztecs, illustrates his phenomenon, as he had an illegitimate son, Martin Cortes, with his native translator, and later on a legitimate son, another Martin Cortes, with a Spanish noblewoman. This pattern of sexual liberty and license was common in the early years, and has been extensively documented by historians. It is a reason many anthropologists give for the relatively low rates of legitimacy in much of Latin America. And of course what applied to Amerindian females also applied to African females. What the genetics makes clear is that this asymmetric pattern of cultural power relations was demographically very significant. Populations with a near total lack of Amerindian and African Y chromosomal lineages, passed from father to son, may still have high levels of non-European mtDNA, passed from mother to daughter. In this study they also looked at the X chromosome, which spends 2/3 of its time in females, and did find an enrichment of Amerindian ancestry there as well.

Tract But they didn’t just focus on the nature of admixture today, they inferred its history. The technique is rooted in basic concepts in genetics. When you have chromosomes come together from parents in a child, those are distinct and identical in nature to segments of ancestry one might find in parents. But genetic recombination in the next generation shuffles the segments, so that parental elements become mixed together on the same segment. When parents are from different geographic populations you see alternative segments of “ancestry tracts.” For example a chromosomal segment with alternative regions of European, Amerindian, and African, ancestry. Because there are only 20-30 recombination events per generation per individual the distribution of the length of these tracts is a function of the length of time since admixture. The early years after admixture will be characterized by long blocks of ancestry from one population, alternated with another. As time passes the segments will get smaller, and alternate much more rapidly. What the authors found was that indeed Amerindian segments exhibited the latter pattern, while European and African segments were more diverse in their distribution. The distinction was strongest in the Caribbean populations, but was evident elsewhere. The explanation is the one above. The early years of Iberian settlement were characterized by de facto polygyny and decimation of male Amerindians through enslavement (though there was population collapse more generally due to disease). Amerindian ancestry came in one singular pulse, and slowly dissipated and distributed itself through the population.

Finally, the results here also yield the finding that Latin American European ancestry seems to have diverged from its parent source. A detailed exploration of the technical issues can be found at the Haldane’s Sieve weblog, but I will say I am convinced that the authors have made a good, if not definitive, case for the proposition that the Latin American ancestral component is one which has diverged significantly. Again, the reason was listed above: de facto polygyny. This drives down the effective population, increases the drift, and skews the allele frequency distribution rapidly away from the source population. If this is a true result it shows us the possibilities for how new populations can arise through fission and rapid expansion. In particular, they may be male mediated. For this period, from 1500-1900, we have extensive documentation to corroborate the broad inferences made. But not so for many regions deep into the past. What these sorts of papers illustrate is the fine-grained power of genetics in shedding light on topics and issues which might otherwise have remained off limits. In particular genetics taps into some of the most primal activities of humankind, those that lead to procreation.

Citation: Moreno-Estrada A, Gravel S, Zakharia F, McCauley JL, Byrnes JK, et al. (2013) Reconstructing the Population Genetic History of the Caribbean. PLoS Genet 9(11): e1003925. doi:10.1371/journal.pgen.1003925

 
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Christopher Columbus

A few year ago there was a minor controversy when some evolutionary genomicists reported that they had reconstructed the genome of the extinct Taino people of Puerto Rico by reassembling fragments preserved in contemporary populations long since admixed. The controversy had to do with the fact that some individuals today claim to be Taino, and therefore, they were not an extinct population. Though that controversy eventually blew over, the methods lived on, and continue to be used. Now some of the same people who brought you that have come out with work which reconstructs the recent demographic history of the Caribbean, both maritime and mainland, using genomics. Even better, it’s totally open access because it’s up on arXiv, Reconstructing the Population Genetic History of the Caribbean (please see the comments at Haldane’s Sieve as well, kicked off by little old me). Though the authors pooled a variety of data sets (e.g., HapMap, POPRES, HGDP) the focus is on the populations highlighted in the map above.

Much of the novel insight in the results begins with their observation of a distinct “Latino” population genetic cluster with strong affinities with Europe within the Caribbean populations. This is clearly visible in their ADMIXTURE analysis. What they did was pool various populations, and run a method which decomposes the ancestry of each individual as a combination of K ancestral populations. In cases where the pooled populations are clear and distinct the results will be clear and distinct. For example, if you had 50 Finns and 50 Nigerians and pooled them, and ran ADMIXTURE at K = 2, then with a non-trivial number of SNPs (10,000 is more than sufficient) all the Finns and Nigerians will partition into two distinct ancestral populations according to these sorts of model based clustering. But it always has to be remembered that though these methods map onto reality, and give us some sense of the variation within the data sets, the K’s themselves are artificial constructs. So, for example, the HGDP Maya population is known to have non-trivial European gene flow. If you use this sort of Maya population as your “Native American” reference, then you will underestimate Native ancestry in admixed groups because your reference Native population is already skewed toward Europeans (this is obviously a major problem when you don’t have the appropriate reference because it is extinct, such as with the Taino).

With those cautionary preliminaries out of the way what’s going on in these results? As you can see many of the Caribbean populations are straightforward combinations of various continental ‘parent’ populations. This is clearly evident in K = 3, where green = Africa, red = European, and blue = Native (note that the Maya have a range of European ancestry just as I said). By looking at individual variation within populations you can already gain some insights as to the nature of the admixture. In Mexico there is a wide range of the European vs. Native fraction, though in this data set there are no “pure” individuals. Additionally, there are low, but relatively even, amounts of African ancestry across the population. Though African consciousness this is not a major element of modern Mexican national identity, people of African ancestry were a major part of the Spanish colonial enterprise (see Empire: How Spain Became a World Power, 1492-1763). In some areas, such as Veracruz, people of visibly African ancestry remain, but in much of Mexico these individuals intermarried and their physical characteristics were diluted toward the point of not being visible.

The situation in the maritime Caribbean is somewhat more complex. In these contexts it was the Native, not African, ancestry which was subsumed and submerged. It is genomics which has ‘rediscovered’ this ancestry, to the extent that many scholars had previously been skeptical of the possibility that modern Puerto Ricans and Dominicans inherited a substantial share of Taino ancestry. In both Puerto Rico and the Dominican Republic the relevant issue is that there is a wide range of proportion of African and European ancestry, with Cuba being the notable extreme case of this phenomenon. What’s going on with Cuba in particular is that there were late waves of migration from Spain, so some modern white Cubans are much less affected by admixture than other Caribbeans (remember that Cuba was part of Spain until 1898). In Haiti the situation is reversed, where the revolutions of the late 18th and early 19th centuries had a racial tinge, and whites were expelled (leaving a small mulatto class).

But it is K = 8 where things really get interesting. The black component is a European Iberian-like element which is distinct to Latino populations (including Maya). As you can see on this PCA the Latino element is related to the Iberian populations, as they took the European segments from the Caribbean populations and used them to flesh out the distribution in ancestry. There are several ways to interpret this. Dienekes suggested this might simply be a function of the source Iberian populations hundreds of years ago being somewhat different from the contemporary ones. For example, obviously contemporary Spaniards would be more subject to gene flow with other Europeans >1600 than their New World cousins. Another possibility is that there was extreme sampling from a particular region of Spain, and that has how broken out as its own cluster. For example, I know that a disproportionate number of migrants were from Andalucia and Extramadura. But the pattern here doesn’t suggest to me that possibility (the black dots should be more south-shifted I would think if they were from those two provinces).

Rather, the interpretation they seem to favor is that this element has been drifted away from the ancestral populations due to a bottleneck. This is not ethnographically implausible; the early years of the Spanish colonial experiment was characterized by de facto polygyny. Many adventurers lived lives not unlike those of the white grandees of the East India company in the late 18th century. Some have argued that this period of ubiquitous common law polygyny has influenced the fact that illegitimate births have traditionally been very common in Latin America. One reason the authors favor the bottleneck model is that the genetic distance between the Latino element and the Iberian one is rather high. This is often common in situations where drift/bottleneck has deviated allele frequencies particularly rapidly. Not only that, but the tendency is most strong in maritime Latin America, many of whose islands received relatively fewer subsequent migrants than the large and expansive mainland viceroyalties.

23andMe ancestry decomposition for friend who is 1/4 Asian

Another way the authors explored the demographic history was to look at the length distribution of the tracts of ancestries. How this works is simple. A first generation hybrid will have unbroken lengths of ancestry each parent, but subsequent generations will start to have fragmentation occur as recombination breaks apart long blocks identical by descent. You can see this in the figure to the left, where my friend who has one Asian grandparent has blocks of alternating European and Asian ancestry because of meiotic recombination events. The longer from the time of admixture the smaller and smaller the blocks will become, as recombination slices apart long blocks and recombines ancestral components. By looking at the distribution and mix of lengths the authors can construct demographic histories of the populations. In short it looks like much of the European ancestry came in one short quick pulse, rather early on in settlement. This is in keeping with the high reproductive output attested for European males thanks to polygyny during this period.

The same method was performed for the African ancestry, and the authors discovered an intriguing result. It seems that in the early years most of the Caribbean black slaves were derived from the western tip of Sub-Saharan Africa, from the Senegal river down to modern Ghana. Later on the longer tracts show affinities with populations further east, from the Bight of Benin toward the Equator. I don’t know the history of slavery well enough to confirm or deny the reality of this finding, but it illustrates the power of genomics combined with wide sampling strategies. More relevantly I suspect genomics’ role will be to assign magnitudes to known dynamics.

Finally, the authors also inferred diverse relationships for the Native admixture in the Caribbean populations. They confirmed some evidence of south-to-north migration into Central and Caribbean America, and also specific ethno-linguistic associations between now de facto extinct Caribbean populations and those of mainland South America. Some of these results have long been suggested, but lack of historical documentation makes inferences shadowy. Genomics can not resolve these debates, but they shed light upon them.

Overall this is an interesting study because I think it is a test run at the sort of historical-demographic questions that genomics will be used for. There has long been a ‘genetics as a tool’ school of thought among many ecologists and phylogeneticists, and now you shall have a ‘genomics as a tool’ to sit right along side that in many more diverse fields. Caribbean and Latin American populations are the low hanging fruit, because the Spanish and Portuguese colonial experiment are reasonably well attested, and the source populations are very distinct (so easy to pick signal out of the noise). But there are other historical questions of the same period which are also of interest. In Albion’s Seed David Hackett Fisher describes four Anglo-American folkways which contributed to the culture of this nation. Of these, ~20,000 Puritans arrived between 1620-1640 and became the ancestors of ~700,000 by 1970. Though 20,000 is not quite a bottleneck (in fact, they arrived from different sectors of England), I am curious if these individuals, a segment of “Old Americans,” can still be discerned in the genomic data. This is just one of many possible questions which will be with reach of answer in the near future….

Citation: arXiv:1306.0558
(Republished from Discover/GNXP by permission of author or representative)
 
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Razib Khan
About Razib Khan

"I have degrees in biology and biochemistry, a passion for genetics, history, and philosophy, and shrimp is my favorite food. If you want to know more, see the links at http://www.razib.com"