Paternal population history of East Asia: sources, patterns, and microevolutionary processes

Abstract

Asia has served as a focal point for human migration during much of the Late Pleistocene and Holocene. Clarification of East Asia's role as a source and/or transit point for human dispersals requires that this region's own settlement history be understood. To this end, we examined variation at 52 polymorphic sites on the nonrecombining portion of the Y chromosome (NRY) in 1,383 unrelated males, representing 25 populations from southern East Asia (SEAS), northern East Asia (NEAS), and central Asia (CAS). The polymorphisms defined 45 global haplogroups, 28 of which were present in these three regions. Although heterozygosity levels were similar in all three regions, the average pairwise difference among haplogroups was noticeably smaller in SEAS. Multidimensional scaling analysis indicated a general separation of SEAS versus NEAS and CAS populations, and analysis of molecular variance produced very different values of Phi(ST) in NEAS and SEAS populations. In spatial autocorrelation analyses, the overall correlogram exhibited a clinal pattern; however, the NEAS populations showed evidence of both isolation by distance and ancient clines, whereas there was no evidence of structure in SEAS populations. Nested cladistic analysis demonstrated that population history events and ongoing demographic processes both contributed to the contrasting patterns of NRY variation in NEAS and SEAS. We conclude that the peopling of East Asia was more complex than earlier models had proposed-that is, a multilayered, multidirectional, and multidisciplinary framework is necessary. For instance, in addition to the previously recognized genetic and dental dispersal signals from SEAS to NEAS populations, CAS has made a significant contribution to the contemporary gene pool of NEAS, and the Sino-Tibetan expansion has left traces of a genetic trail from northern to southern China.

Figure 1

Map of 25 sampling localities, divided into three regional groupings (NEAS, SEAS, and CAS). Numbers indicate population numerical codes, given in table 1.

Figure 2

Evolutionary tree for 45 NRY haplogroups (h1–h45). The root of the haplogroup tree is indicated by an arrow. The 52 mutational events, of which the first 42 appear in table 1 in the report by Hammer et al. (2001), are shown by cross-hatches. The 10 additional mutational sites are from reports by Underhill et al. (2000) and Shen et al. (2000), where UTY1= UTY1-3678+537 and UTY2= UTY1-1330+18. Haplogroups are color-coded according to geographic region (see figure for key); circles without colors denote absence in NEAS, SEAS, and CAS. The pie charts represent the frequency of occurrence of the haplogroups within each of the three Asian geographic regions shown in figure 1. The overall size of each pie chart corresponds to one of six frequency classes (see figure for frequency-class key) and represents the frequency of that haplogroup in the total sample of 1,383 chromosomes.

Figure 3

MDS plot of 25 Asian populations, based on Φ_ST genetic distances. For three-letter population codes, see table 1.

Figure 4

Spatial autocorrelation plots. a, 25 Asian populations. b, NEAS (diamonds) versus SEAS (circles) populations.

Figure 5

Regression of genetic-distance estimates for pairs of populations against the log of geographic distances. a, 25 Asian populations. b, NEAS populations. c, SEAS populations.

Figure 6

Nested cladistic design for 45 NRY haplogroups. The 52 mutational events (cross-hatches), 45 haplogroups (h1–h45), and cladogram root (arrow) are as described in figure 2. Black circles represent haplogroups that were missing in this sample of Y chromosomes. Ovals contain one-step clades (designated as “1-1” through “1-14”); rectangles contain two-step clades (designated as “2-1” through “2-6”); and rounded rectangles contain three-step clades (designated as “3-1” through “3-3”). Double-dotted lines contain one four-step clade (designated as “4-1”). A single five-step clade (5-1) encompasses the entire cladogram.