The Genetic History of Indigenous Populations of the Peruvian and Bolivian Altiplano: The Legacy of the Uros

The Altiplano region of the South American Andes is marked by an inhospitable climate to which the autochthonous human populations adapted and then developed great ancient civilizations, such as the Tiwanaku culture and the Inca Empire. Since pre-Columbian times, different rulers established themselves around the Titicaca and Poopo Lakes. By the time of the arrival of Spaniards, Aymara and Quechua languages were predominant on the Altiplano under the rule of the Incas, although the occurrence of other spoken languages, such as Puquina and Uruquilla, suggests the existence of different ethnic groups in this region. In this study, we focused on the pre-Columbian history of the autochthonous Altiplano populations, particularly the Uros ethnic group, which claims to directly descend from the first settlers of the Andes, and some linguists suggest they might otherwise be related to Arawak speaking groups from the Amazon. Using phylogeographic, population structure and spatial genetic analyses of Y-chromosome and mtDNA data, we inferred the genetic relationships among Uros populations (Los Uros from Peru, Uru-Chipaya and Uru-Poopo from Bolivia), and compared their haplotype profiles with eight Aymara, nine Quechua and two Arawak (Machiguenga and Yanesha) speaking populations from Peru and Bolivia. Our results indicated that Uros populations stand out among the Altiplano populations, while appearing more closely related to the Aymara and Quechua from Lake Titicaca and surrounding regions than to the Amazon Arawaks. Moreover, the Uros populations from Peru and Bolivia are genetically differentiated from each other, indicating a high heterogeneity in this ethnic group. Finally, our results support the distinctive ancestry for the Uros populations of Peru and Bolivia, which are likely derived from ancient Andean lineages that were partially replaced during more recent farming expansion events and the establishment of complex civilizations in the Andes

Genetic ancestry of families of putative inka descent

This study focuses on the descendants of the royal Inka family. The Inkas ruled Tawantinsuyu, the largest pre-Columbian empire in South America, which extended from southern Colombia to central Chile. The origin of the royal Inkas is currently unknown. While the mummies of the Inka rulers could have been informative, most were destroyed by Spaniards and the few remaining disappeared without a trace. Moreover, no genetic studies have been conducted on present-day descendants of the Inka rulers. In the present study, we analysed uniparental DNA markers in 18 individuals predominantly from the districts of San Sebastian and San Jerónimo in Cusco (Peru), who belong to 12 families of putative patrilineal descent of Inka rulers, according to documented registries. We used single-nucleotide polymorphisms and short tandem repeat (STR) markers of the Y chromosome (Y-STRs), as well as mitochondrial DNA D-loop sequences, to investigate the paternal and maternal descent of the 18 alleged Inka descendants. Two Q-M3* Y-STR clusters descending from different male founders were identified. The first cluster, named AWKI-1, was associated with five families (eight individuals). By contrast, the second cluster, named AWKI-2, was represented by a single individual; AWKI-2 was part of the Q-Z19483 sub-lineage that was likely associated with a recent male expansion in the Andes, which probably occurred during the Late Intermediate Period (1000–1450 AD), overlapping the Inka period. Concerning the maternal descent, different mtDNA lineages associated with each family were identified, suggesting a high maternal gene flow among Andean populations, probably due to changes in the last 1000 years

The Genetic History of Indigenous Populations of the Peruvian and Bolivian Altiplano: The Legacy of the Uros

The Altiplano region of the South American Andes is marked by an inhospitable climate to which the autochthonous human populations adapted and then developed great ancient civilizations, such as the Tiwanaku culture and the Inca Empire. Since pre-Columbian times, different rulers established themselves around the Titicaca and Poopo Lakes. By the time of the arrival of Spaniards, Aymara and Quechua languages were predominant on the Altiplano under the rule of the Incas, although the occurrence of other spoken languages, such as Puquina and Uruquilla, suggests the existence of different ethnic groups in this region. In this study, we focused on the pre-Columbian history of the autochthonous Altiplano populations, particularly the Uros ethnic group, which claims to directly descend from the first settlers of the Andes, and some linguists suggest they might otherwise be related to Arawak speaking groups from the Amazon. Using phylogeographic, population structure and spatial genetic analyses of Y-chromosome and mtDNA data, we inferred the genetic relationships among Uros populations (Los Uros from Peru, Uru-Chipaya and Uru-Poopo from Bolivia), and compared their haplotype profiles with eight Aymara, nine Quechua and two Arawak (Machiguenga and Yanesha) speaking populations from Peru and Bolivia. Our results indicated that Uros populations stand out among the Altiplano populations, while appearing more closely related to the Aymara and Quechua from Lake Titicaca and surrounding regions than to the Amazon Arawaks. Moreover, the Uros populations from Peru and Bolivia are genetically differentiated from each other, indicating a high heterogeneity in this ethnic group. Finally, our results support the distinctive ancestry for the Uros populations of Peru and Bolivia, which are likely derived from ancient Andean lineages that were partially replaced during more recent farming expansion events and the establishment of complex civilizations in the Andes

Non-metric MDS plot generated with PAST for mtDNA control region sequences for all haplogroups among 22 Bolivian and Peruvian populations.

<p>It was used Reynolds’ Φ<i>st</i> genetic distances among populations. Uros: red triangles, Aymaras: blue circles, Quechuas: yellow squares, and Arawaks: green squares.</p

AMOVA results for 17 Y-STRs of the Q-M3 and Q-M346^* lineages involving 22 Peruvian and Bolivian populations (n = 387).

*<p>Between populations within groups.</p>**<p><i>Rct</i> (between groups), p-values>0.05.</p>***<p>p-values<0.01 (significant).</p

Map of the western South America showing the Andes and locations of the 22 Peruvian and Bolivian populations under study.

<p>Population codes are found in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073006#s2" target="_blank">Materials and Methods</a> (Sampling section). Yellow circles represent Quechua populations, blue circles represent Aymara, green circles represent Arawak, and red circles represent Uroś populations. A detailed map of the Andean Altiplano region can be seen in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073006#pone.0073006.s002" target="_blank">Figure S2</a>.</p

Median Joining network of mtDNA control region haplotypes found in 22 Peruvian and Bolivian populations.

<p>Different population groups are defined by distinct colors, where Aymaran and Quechuan communities from the border of the lakes (Titicaca and Poopo) are discriminated. The mtDNA haplotypes (Hp#) are represented by circles with sizes proportional to numbers of individuals (Hp10 = 1 individual), and branch lengths are proportional to nucleotide changes (1 mutation step between Hp1 and Hp3). Clusters of haplotypes into four mtDNA haplogroups (A2, B2, C1, D1) are indicated.</p

AMOVA results for mtDNA control region sequences on the A2, B2, C1 and D1 haplogroups found among 22 Peruvian and Bolivian populations (n = 388).

*<p>Between populations within groups.</p>**<p><i>Fct</i> (between groups), p-value>0.05.</p>***<p>p-values<0.01 (significant).</p

Median Joining network for Q-M3 STR haplotypes among 22 Peruvian and Bolivian populations.

<p>Different population groups are defined by distinct colors, where Aymara and Quechua communities from the border of the lakes (Titicaca and Poopo) are discriminated. The haplotypes (H#) composed of 15 Y-STRs are represented by circles with sizes proportional to numbers of individuals (H3 = 1, H1 = 13 males), and branch lengths are proportional to STR mutation steps (one repeat unit between H3 and H4). Haplotype names are according to the 15 Y-STRs (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0073006#pone.0073006.s005" target="_blank">Table S2c</a>).</p