mtDNA variation in South America and evolutionary history of native South Americans

In Central Andes, exploitation of marine resources and introduction of intensive agriculture caused population size to increase early in its prehistory.  Also, since its prehistory, there were constant movements of people in the Andes due to vertical use of the ecosystem, series of state expansions, forced migration by Inca, and migration to larger cities after European contact.  These events probably had great effects on the genetic variation, but what extent these event influenced genetic variation is still uncertain.  In this post, I reviewed recent mtDNA data from Central Andes to address these questions.

Following Tarazona-Santos et al. (2001), Fuselli et al. (2003) argues that mtDNA data supports Y chromosome data and Western part of South America, mainly Andes, and Eastern part of South America, mainly Amazon, had separate evolutionary histories.  The Andean populations have high within-population genetic diversity and they are genetically similar to each other.   They argue that both large effective population size and gene flow contributed for large within-population genetic diversity.  The Amazonian populations, on the other hand, have low within-population genetic diversity and they are genetically differentiated, because without gene flow, genetic drift had a great effect on geographically isolated small populations.

Lewis et al. (2005, 2007) analyzed mtDNA sequence variation of five highland Peruvian populations and compared to two of three highland Peruvian populations that Fuselli et al. (2003) analyzed and lowland populations.  Supporting the argument that Fusellli et al. put forth, Lewis et al. found high within-population genetic diversity among highland Peruvian populations and Andeans populations were genetically homogeneous compared to Amazonian populations.  However, their AMOVA results suggest that there is no significant genetic difference between Andean group and Amazonian group.  Lewis and Long (2008) found more mtDNA variation in Eastern South American and less genetic variation in the Andean region than previously reported, when regional variation was accounted for. 

Analyses of mtDNA variation among the populations that occupy in the transitional zone between Andes and Amazon provide more complicated perspectives on the South American evolutionary history.  Bert et al. (2004) and Corella et al. (2007) analyzed mtDNA variation of lowland Bolivians from the Department of Beni and Cabana et al. (2006) analyzed that of Gran Chaco.  In general, these populations have genetic diversity values intermediate of Andean and Amazonian populations and they are genetically differentiated from each other.  These patterns are expected from smaller relatively isolated populations. 

However, they found evidence suggesting that these populations were not reproductively isolated and there were gene flows among these populations as well as between Andeans and populations in the transitional zone responding to state expansion from Andean highland or reorganization of indigenous societies during the colonial era.  First, some of these small populations from lowland Bolivia have unexpectedly high within-population genetic diversity.  Second, when the Ayoreo is excluded from analyses, Gran Chaco populations were very homogeneous.  Finally, some these populations are genetically very similar to Andeans.

The population size in Central Andes may have been large enough for them to be genetically more diverse than other populations in South America, but the constant movements, or interactions, of people made populations in Central Andes genetically homogeneous and potentially genetically more diverse.  This interaction sphere may have extended into the transitional zones making populations from the transitional zone genetically diverse and similar to Central Andeans.  My review of articles on Central Andeans mtDNA variation, however, shows that no one has examined whether female effective population size or gene flow contribute more on mtDNA variation of these populations.

Bert, F., A. Corella, et al. (2004). “Mitochondrial DNA diversity in the Llanos de Moxos: Moxo, Movima and Yuracare Amerindian populations from Bolivia lowland.” Ann Hum Biol 31: 9-28.

Cabana, G. S., D. A. Merriwether, et al. (2006). “Is the genetic structure of Gran Chaco populations unique? Interregional perspectives on native South American mitochondrial DNA variation.” American Journal of Physical Anthropology 131(1): 108-119.

Corella, A., F. Bert, et al. (2007). “Mitochondrial DNA diversity of the Amerindian populations living in the Andean Piedmont of Bolivia: Chimane, Moseten, Aymara and Quechua.” Annals of Human Biology 34(1): 34-55.

Fuselli, S., E. Tarazona-Santos, et al. (2003). “Mitochondrial DNA diversity in South America and the genetic history of Andean highlanders.” Molecular Biology and Evolution 20(10): 1682-1691.

Lewis, C. M. J., B. Lizárraga, et al. (2007). “Mitochondrial DNA and the peopling of South America.” Human Biology 79: 159-178.

Lewis, C. M., Jr. and J. C. Long (2008). “Native South American genetic structure and prehistory inferred from hierarchical modeling of mtDNA.” Molecular Biology and Evolution 25(3): 478-486.

Lewis, C. M. J., R. Y. Tito, et al. (2005). “Land, language, and loci: mtDNA in Native Americans and the genetic history of Peru.” American Journal of Physical Anthropology 127: 351-360.

Tarazona-Santos, E., D. R. Carvalho-Silva, et al. (2001). “Genetic Differentiation in south amerindians is related to environmental and cultural diversity: Evidence from the Y chromosome.” American Journal of Human Genetics 68(6): 1485-1496.

DNA genome of an unknown hominin from southern Siberia

Krause, J., Q. Fu, et al. (2010). “The complete mitochondrial DNA genome of an unknown hominin from southern Siberia.” Nature advance online publication.

This article is very interesting and also covered by and Prancing Papio.  I believe the research findings presented in this article provide an interesting perspective on the human evolution and genetic diversity existed in the past.

The complete mitochondrial DNA genome of the fossil remain from Denisova Cave in the Altai region of Russia dated to 48 to 30 kyr ago was analyzed.  Their results of analyses show that the Denisova individual was genetically very different from Neanderthals or modern humans.  An average of nucleotide position differences was 385 between the Denisova individual and modern human, which is about twice as many difference between Neanderthals and modern human (202 positions) (Figure 2).

The phylogenetic treesof complete mtDNA show that the ancestors of the Denisova individual sprit from the ancestors of Neanderthals and modern human, before archaic human lineages began diverge (Figure 3).  TMRCA of all three lineages is about one million years ago (mean=1,04,900 with 95% C.I. ranging 779,300-1,313,500).

So, who is this Denisova individual?  Home erectus left Africa and around 1.9 myr ago and was in Asia by 1.7 myr ago, so the Denisova individual was probably not H. erectus (TMRC of three lineages is about one myr ago.  That is after H. erectus spread into East Asia).  If the Denisova is H. erectus much older TMRCA is expected (> 1.9 myr?).  Homo heidelbergensis, probable ancestors of Neantherthals, emerged after divergence of three lineages.  However, since the 95% C.I. of TMRCA slightly overlaps with the time that H. heidelbergensis existed, so we cannot reject the hypothesis of the Denisova individual = a descendant of H. heidelbergenesis, but if H. heidelbergenesis were ancestors of Neanderthals, the ancestors of Neanderthals and the Denisova individual were genetically quit different.

The findings from this project generally support Huff et al. (2010) and these two projects have shown that great genetic diversity existed in the past (> 30,000 years ago).  It is very interesting that there were many species or subspecies of Home may have co-existed in some parts of the world.  Around time the Denisova individual lived, there is also possible existence of Neanderthal and anatomically modern human in the area (Don’t forget H. erectus existed in East Asia about same time).  However, only anatomically modern human survived and others disappeared without leaving clear genetic evidence of ancient admixture.

Update (April 1, 2010)

I forgot about H. ergaster and that is another possibility in addition to H. heidelbergensis.  If we believe that Asian H. erectus was a different species from African H. ergaster who were direct ancestors of H. heidelbergenesis, H. neanderthalensis, and H. sapiens, the Denisova individual could be a descendant of H. ergaster who took very different evolutionary path from Neanderthals and Anatomically modern human.  The 95% C.I. of TMRCA (1.-0.7) also slightly overlap with the time H. ergaster existed in East Africa (1.8-1.3 mya).  If we believe this scenario, first there was an out of Africa event of H. erectus into Asia and then another out of Africa event of H. ergaster into Western Eurasia.  However, TMRCA is too young for Asian H. erectus and all others to share the common ancestor that recent, so mtDNA of the Denisova individual is not that of H. erectus.  Of course, we are talking about only maternal side of evolutionary history.

Updata (April 3, 2010)

I considered the possibility of an unsampled Neanderthal, but I thought that the TMRCA is too old, considering that Neanderthals analyzed so far is genetically not diverse and effects of drift affecting mtDNA is strong because of small effective population size of mtDNA.  If, in fact, the Denisova individual was a Neanderthal, Neanderthal was genetically much more diverse than many genetic researchers thought and phylogenetic tree suggests that Neanderthals were ancestors of modern human.   Judging from the genetic evidence we have, this is unlikely scenario.  Of course, we should not conclude that the Denisova individual was not Neanderthals, because we do not know enough about this individual or human evolution.

Did the Chibchans experience population expansion?

Melton, P. E., I. Briceño, et al. (2007). “Biological relationship between Central and South American Chibchan speaking populations: evidence from mtDNA.” American Journal of Physical Anthropology 133: 753-770.

Melton et al. propose that Chibchan speakers in Central and South America experienced population around 10,000-14,000 years ago as they shifted their subsistence when the Holocene climate change occurred.  They estimated the time of expansion using mismatch distribution, while noting the problem of dating using mtDNA data.  But, they could explain how the populations with genetic signature of founder effect or bottleneck show evidence of population expansion.  Compared to other Latin American populations, the Chibchans have very small genetic diversity.  Probably, the effects of genetic drift were strong because of lack of female gene flow due to their matrilocal post-marital residence, but I thought that genetic drift should erase the evidence of population expansion, and in fact, tests of neutrality do not support the Chibchan population expansion hypothesis well.