A South American Prehistoric Mitogenome: Context, Continuity, and the Origin of Haplogroup C1d

<div><p>Based on mitochondrial DNA (mtDNA), it has been estimated that at least 15 founder haplogroups peopled the Americas. Subhaplogroup C1d3 was defined based on the mitogenome of a living individual from Uruguay that carried a lineage previously identified in hypervariable region I sequences from ancient and modern Uruguayan individuals. When complete mitogenomes were studied, additional substitutions were found in the coding region of the mitochondrial genome. Using a complete ancient mitogenome and three modern mitogenomes, we aim to clarify the ancestral state of subhaplogroup C1d3 and to better understand the peopling of the region of the Río de la Plata basin, as well as of the builders of the mounds from which the ancient individuals were recovered. The ancient mitogenome, belonging to a female dated to 1,610±46 years before present, was identical to the mitogenome of one of the modern individuals. All individuals share the mutations defining subhaplogroup C1d3. We estimated an age of 8,974 (5,748–12,261) years for the most recent common ancestor of C1d3, in agreement with the initial peopling of the geographic region. No individuals belonging to the defined lineage were found outside of Uruguay, which raises questions regarding the mobility of the prehistoric inhabitants of the country. Moreover, the present study shows the continuity of Native lineages over at least 6,000 years.</p></div

TMRCA estimates for the putative common ancestors of haplogroup C1d and subhaplogroup C1d3.

<p>BSP: Bayesian skyline plot. See Tables A and B in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0141808#pone.0141808.s004" target="_blank">S2 Text</a> for further details.</p><p>TMRCA estimates for the putative common ancestors of haplogroup C1d and subhaplogroup C1d3.</p

Map showing the location of the Uruguayan samples belonging to subhaplogroup C1d3 with the five complete mitogenomes used in this study.

<p>The locations of the living individuals (circles) correspond to their mothers’ birthplace. The archaeological site where the prehistoric sample was recovered is marked with a square.</p

Ancient DNA Analysis of Mid-Holocene Individuals from the Northwest Coast of North America Reveals Different Evolutionary Paths for Mitogenomes

<div><p>To gain a better understanding of North American population history, complete mitochondrial genomes (mitogenomes) were generated from four ancient and three living individuals of the northern Northwest Coast of North America, specifically the north coast of British Columbia, Canada, current home to the indigenous Tsimshian, Haida, and Nisga’a. The mitogenomes of all individuals were previously unknown and assigned to new sub-haplogroup designations D4h3a7, A2ag and A2ah. The analysis of mitogenomes allows for more detailed analyses of presumed ancestor–descendant relationships than sequencing only the HVSI region of the mitochondrial genome, a more traditional approach in local population studies. The results of this study provide contrasting examples of the evolution of Native American mitogenomes. Those belonging to sub-haplogroups A2ag and A2ah exhibit temporal continuity in this region for 5000 years up until the present day. Of possible associative significance is that archaeologically identified house structures in this region maintain similar characteristics for this same period of time, demonstrating cultural continuity in residence patterns. The individual dated to 6000 years before present (BP) exhibited a mitogenome belonging to sub-haplogroup D4h3a. This sub-haplogroup was earlier identified in the same general area at 10300 years BP on Prince of Wales Island, Alaska, and may have gone extinct, as it has not been observed in any living individuals of the Northwest Coast. The presented case studies demonstrate the different evolutionary paths of mitogenomes over time on the Northwest Coast.</p></div

Phylogeny of complete mitochondrial genomes sequenced in this study.

<p>Mutations are transitions unless specified. Transversions are indicated by an A, G, C, or T after the nucleotide position. Insertions are indicated by an “i”, deletions are indicated by a “d”, recurrent mutations are underlined, and mutations back to the rCRS nucleotide are designated by a “@”. The C stretch length polymorphism in region 303–315 was disregarded in the tree. The sample “Haida 9″ was analyzed in Schurr et al. (2012). All other samples were analyzed in this study.</p

Lemur aDNA sequence data and bait capture information

Lemur aDNA sequence data and bait capture informatio

Procrustes-transformed multidimensional scaling plots of Eurasian and American individuals.

<p>(A) 641 individuals from 53 populations after resampling of 82 individuals from each of 14 nonoverlapping groups of European, Central and South Asian, East Asian, and American populations (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s007" target="_blank">Figure S7</a>). (B) 641 individuals from 41 populations after resampling of 82 individuals from each of 15 nonoverlapping groups of European, East Asian, and American populations (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s008" target="_blank">Figure S8</a>). (C) 393 individuals from 22 populations after resampling of 82 individuals from each of 10 nonoverlapping groups of European and American populations (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s009" target="_blank">Figure S9</a>). (D) 450 individuals from 34 populations after resampling of 82 individuals from each of 11 nonoverlapping groups of East Asian and American populations (<a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s010" target="_blank">Figure S10</a>). Procrustes similarity statistics are <i>t</i>₀ = 0.958 between <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g004" target="_blank">Figures 4B</a> and <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g005" target="_blank">5A</a>, <i>t</i>₀ = 0.999 between <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g005" target="_blank">Figures 5A and 5B</a>, <i>t</i>₀ = 0.956 between <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g005" target="_blank">Figures 5B and 5C</a>, and <i>t</i>₀ = 0.997 between <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g005" target="_blank">Figures 5B and 5D</a>. Population colors and symbols follow <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g001" target="_blank">Figure 1</a>.</p

Time of European and East-Asian admixture in North and Central America estimated using the admixture linkage disequilibrium approach in <i>ALDER</i>[44].

α<p>Populations considered as admixed populations using <i>ALDER</i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[44]</a>.</p>β<p>Sets of European populations considered separately in <i>ALDER</i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[44]</a> as reference populations for admixture.</p><p><i>EurA</i> : Toscani (TSI); Caucasian (CEU); Russian; Basque; French; Sardinian.</p><p><i>EurB</i> : Toscani (TSI); Basque ; French; Sardinian.</p><p><i>EurC</i> : Toscani (TSI); Caucasian (CEU); Basque; French; Sardinian.</p>γ<p><i>Sets of</i> East Asian populations considered separately in <i>ALDER</i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[44]</a> as reference populations for admixture.</p><p><i>na</i>: No significant admixture was found with any of the reference populations considered.</p><p><i>AsA</i> : Japanese (JPT); Japanese.</p><p><i>AsB</i> : Han; Han (CHB); Han (CHD); Japanese (JPT); Japanese.</p><p><i>AsC</i> : Han; Han (CHB); Han (CHD); Japanese (JPT); Japanese; Yakut.</p>δ<p>Mean admixture time in years (25 years for generation time) estimated by <i>ALDER</i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[44]</a> across the reference populations considered ± mean of the admixture time standard deviations obtained across the reference populations considered.</p>∈<p>Mean admixture rate estimated by <i>ALDER </i><a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530-Loh1" target="_blank">[<i>44</i>]</a> across the reference populations considered ± standard deviation.</p

Worldwide Admixture structure.

<p>Plotted are modes with clustering solutions obtained with 30 replicates at each value of <i>K</i>. Values of <i>K</i> and the number of runs in the mode shown appear on the left. In each plot, each cluster is represented by a different color, and each individual is represented by a vertical line divided into <i>K</i> colored segments with heights proportional to genotype memberships in the clusters. Thin black lines separate individuals from different populations. The same 528 individuals included in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g004" target="_blank">Figure 4B</a> are considered in the Admixture analyses. Alternate clustering solutions for values of <i>K</i> from 2 to 12 appear in <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s003" target="_blank">Figure S3</a>.</p

Individual-level population structure.

<p>(A) Multidimensional scaling plot of pairwise allele-sharing distance (ASD) among 2,140 individuals in the combined dataset. (B) Multidimensional scaling plot of pairwise ASD among 528 individuals from 63 worldwide populations, following the resampling of a maximum of 82 individuals each from 11 different population groups. Group choices for resampling were taken from <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen.1004530.s006" target="_blank">Figure S6</a>. Population colors and symbols follow <a href="http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1004530#pgen-1004530-g001" target="_blank">Figure 1</a>.</p