Independent histories of human Y chromosomes from Melanesia and Australia

Abstract

To investigate the origins and relationships of Australian and Melanesian populations, 611 males from 18 populations from Australia, Melanesia, and eastern/southeastern Asia were typed for eight single-nucleotide polymorphism (SNP) loci and seven short tandem-repeat loci on the Y chromosome. A unique haplotype, DYS390.1del/RPS4Y711T, was found at a frequency of 53%-69% in Australian populations, whereas the major haplotypes found in Melanesian populations (M4G/M5T/M9G and DYS390.3del/RPS4Y711T) are absent from the Australian populations. The Y-chromosome data thus indicate independent histories for Australians and Melanesians, a finding that is in agreement with evidence from mtDNA but that contradicts some analyses of autosomal loci, which show a close relationship between Australian and Melanesian (specifically, highland Papua New Guinean) populations. Since the Australian and New Guinean landmasses were connected when first colonized by humans > or =50,000 years ago but separated some 8,000 years ago, a possible way to reconcile all the genetic data is to infer that the Y-chromosome and mtDNA results reflect the past 8,000 years of independent history for Australia and New Guinea, whereas the autosomal loci reflect the long preceding period of common origin and shared history. Two Y-chromosome haplotypes (M119C/M9G and M122C/M9G) that originated in eastern/southeastern Asia are present in coastal and island Melanesia but are rare or absent in both Australia and highland Papua New Guinea. This distribution, along with demographic analyses indicating that population expansions for both haplotypes began approximately 4,000-6,000 years ago, suggests that these haplotypes were brought to Melanesia by the Austronesian expansion. Most of the populations in this study were previously typed for mtDNA SNPs; population differentiation is greater for the Y chromosome than for mtDNA and is significantly correlated with geographic distance, a finding in agreement with results of similar analyses of European populations.

Figure 1

Y-chromosome haplotypes, as defined by six Y-chromosome SNPs and two specific deletions at the Y-chromosome STR locus DYS390, and their frequency distribution in human populations from eastern/southeastern Asia, Melanesia, Polynesia, and Australia. Color codings are as follows: black, complete ancestral haplotype (with respect to the markers analyzed); gray, M9G; red, M4G/M5T/M9G; yellow, M119C/M9G; orange, M122C/M9G; green, RPS4Y711T; dark blue, DYS390.1del/RPS4Y711T; purple, DYS390.3del/M9G; and light blue, DYS390.3del/RPS4Y711T. Abbreviations are as follows: Aus1 = Australia, Arnhem Land; Aus2 = Australia, Sandy Desert; Bor = southern Borneo; Chi = China; Coo = Cook Islands; Jav = Java; Kor = Korea; Mal = Malaysia; Mol = Moluccas; Phi = Philippines; PNC = PNG coast; PNH = PNG highlands; TaC = Taiwan Chinese; Tai = Taiwan aborigines; Ten = Nusa Tenggara; TNB = Tolai New Britain; Tro = Trobriand Islands; Vie = Vietnam.

Figure 2

Y-chromosome haplotypes, based on six Y-chromosome SNPs and two specific deletions at the Y-chromosome STR locus DYS390, and their phylogenetic relationship. The superscript “a” denotes a recurrent mutation event.

Figure 3

Structure of the Y-chromosome STR locus DYS390, and proposed mutational events leading to the DYS390.1 deletion and the DYS390.3 deletion.

Figure 4

Median-joining network of 41 Y-chromosome STR haplotypes found in 51 individuals carrying the M4G/M5T/M9G haplotype. Circles denote the Y-chromosome STR haplotypes, with the area of the circle being proportional to the number of individuals. Lines denote mutation steps (one-step distance is indicated); parallel lines represent identical mutations. Color coding is as follows: red, highland PNG; blue, coastal PNG/New Britain; green, Trobriand Islands; yellow, eastern Indonesia.

Figure 5

Bayesian-based demographic inference of associated Y-chromosome STR variation concerning the DYS390.1del/RPS4Y711T haplotype (a and b), the M119C/M9G haplotype (c and d), and the M4G/M5T/M9G haplotype (e and f). Prior probabilities (dashed lines) and posterior-probability distributions (continuous lines) are shown for the time when population expansion began (a, c, and e) and for the TMRCA (b, d, and f).

Figure 6

PC plot of Y-chromosome haplotype frequencies for 18 populations from eastern/southeastern Asia, Melanesia, Polynesia, and Australia (for abbreviations, see the legend to figure 1). Geographic regions are highlighted.

Figure 7

Correlation analysis of genetic distance (F_ST based on SNP markers) and geographic distance (km), for 12 populations from eastern/southeastern Asia, Melanesia, and Australia (for particular populations, see the text), for mtDNA (triangles, dashed trendline) and Y-chromosome DNA (squares, continuous trendline).