Mitochondrial genome evidence reveals successful Late Paleolithic settlement on the Tibetan Plateau

Abstract

Due to its numerous environmental extremes, the Tibetan Plateau--the world's highest plateau--is one of the most challenging areas of modern human settlement. Archaeological evidence dates the earliest settlement on the plateau to the Late Paleolithic, while previous genetic studies have traced the colonization event(s) to no earlier than the Neolithic. To explore whether the genetic continuity on the plateau has an exclusively Neolithic time depth, we studied mitochondrial DNA (mtDNA) genome variation within 6 regional Tibetan populations sampled from Tibet and neighboring areas. Our results confirm that the vast majority of Tibetan matrilineal components can trace their ancestry to Epipaleolithic and Neolithic immigrants from northern China during the mid-Holocene. Significantly, we also identified an infrequent novel haplogroup, M16, that branched off directly from the Eurasian M founder type. Its nearly exclusive distribution in Tibetan populations and ancient age (>21 kya) suggest that M16 may represent the genetic relics of the Late Paleolithic inhabitants on the plateau. This partial genetic continuity between the Paleolithic inhabitants and the contemporary Tibetan populations bridges the results and inferences from archaeology, history, and genetics.

Fig. 1.

Sampling locations of the Chinese populations under study and of the excavated archaeological sites summarized from the literature. Codes 1–72 label the populations (with solid pentacles labeling locations of Tibetan populations collected in this study; see Table S2 for details). Solid triangles refer to excavation sites dating to pre-LGM, open triangles represent sites with Paleolithic age based on lithic comparison, and inverted triangles indicate post-LGM sites (see Table S1 for more details).

Fig. 2.

PCA of the populations under study. The map was constructed based on the basal haplogroup frequency matrix in Table S4. N_Tib, Nakchu Tibetan; R_Tib, Shigatse Tibetan; T_Tib, Tibet Tibetan; Q_Tib, Qinghai Tibetan; Y_Tib, Yunnan Tibetan; S_Tib, Sichuan Tibetan; G_Tib, Gansu Tibetan. See Table S3 for details of the group classifications.

Fig. 3.

Reconstructed mtDNA tree of the completely sequenced representatives of the major Tibetan mtDNA lineages. Suffixes “A,” “C,” “G,” and “T” refer to transversions, “d” denotes deletion, and “+” indicates an insertion event (without specifying the number of inserted nucleotides). Suffixes “Y” and “R” denote heteroplasmic mutations (C/T and A/G, respectively); recurrent mutations are underlined; “@” denotes a reverse mutation; “s” means synonymous and “ns” means nonsynonymous mutation; “−nc” refers to mutations at the intergenic noncoding regions in segments 577–16023; and “∼r” and “∼t” denote mutations in rRNA genes and tRNA genes, respectively. The C stretch length polymorphism in region 303–315 was disregarded for the tree reconstruction. Suffixes “MT#,” “MI#,” “QPK#,” and “PS#” next to the sample names refer to the sources Tanaka et al. (38), Ingman et al. (39), Kong et al. (19, 24), and Soares et al. (40), respectively. Codes “N,” “R,” “Q,” “Y,” and “G” refer to sampling locations (Nakchu, Shigatse, Qinghai, Yunnan, and Gansu, respectively) of different regional Tibetan populations.

Fig. 4.

Estimated ages of the Tibetan-prevalent mtDNA lineages. Open cycles indicate the estimated ages of a haplogroup, with red, brown, green, blue, and black cycles referring to the calibration rates for segment 16051-16400 substitutions (35), coding region synonymous substitutions (35), modified coding region synonymous transitions (34), modified coding region substitutions (34), and complete genome substitutions (35), respectively.

Fig. 5.

Constructed median network displaying the control region information of M16 lineages. This network was constructed manually according to Bandelt et al. (31). The data used here were collected from the literature (Table S2) and the present study (Table S3). The sequence information used for network construction was confined to segment 16047-16497. Time estimation was carried out based on segment 16051-16400 as described previously (35). The asterisk denotes the ancestral node of the haplogroup defined by motif 16223-16260-16295-73-150-204-263. See the legend of Fig. 3 for more information.