Autosomal and X-linked single nucleotide polymorphisms reveal a steep Asian-Melanesian ancestry cline in eastern Indonesia and a sex bias in admixture rates

Abstract

The geographical region between mainland Asia and New Guinea is characterized by numerous small islands with isolated human populations. Phenotypically, groups in the west are similar to their neighbours in mainland Southeast Asia, eastern groups near New Guinea are similar to Melanesians, and intervening populations are intermediate in appearance. A long-standing question is whether this pattern primarily reflects mixing between groups with distinct origins or whether natural selection has shaped this range of variation by acting differentially on populations across the region. To address this question, we genotyped a set of 37 single nucleotide polymorphisms that are evolutionarily independent, putatively neutral and highly informative for Asian-Melanesian ancestry in 1430 individuals from 60 populations spanning mainland Asia to Melanesia. Admixture analysis reveals a sharp transition from Asian to Melanesian genetic variants over a narrow geographical region in eastern Indonesia. Interestingly, this admixture cline roughly corresponds to the human phenotypic boundary noted by Alfred Russell Wallace in 1869. We conclude that this phenotypic gradient probably reflects mixing of two long-separated ancestral source populations-one descended from the initial Melanesian-like inhabitants of the region, and the other related to Asian groups that immigrated during the Paleolithic and/or with the spread of agriculture. A higher frequency of Asian X-linked markers relative to autosomal markers throughout the transition zone suggests that the admixture process was sex-biased, either favouring a westward expansion of patrilocal Melanesian groups or an eastward expansion of matrilocal Asian immigrants. The matrilocal marriage practices that dominated early Austronesian societies may be one factor contributing to this observed sex bias in admixture rates.

Figure 1.

Local admixture rates across the Indo-Pacific region. (a) Pie charts showing mean regional admixture rates (Asian component in white; Melanesian component in black). Wallace's biogeographic line is shown as a dotted line. Regional admixture rates are shown for data reduction purposes; admixture rates for all 60 populations (with confidence intervals) are listed in the electronic supplementary material. (b) Change in Asian admixture rates calculated from all SNPs combined (black line). Regions with no data indicated by a dashed line (exact gradient unknown). Asian admixture estimated from autosomal and X chromosomal SNPs are indicated by black and grey points, respectively. Note the decline in Asian admixture beginning in eastern Indonesia, as well as preferential retention of X chromosomal (grey) versus autosomal (black) diversity.