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.

Introduction: Revisiting the “Negrito” Hypothesis: A Transdisciplinary Approach to Human Prehistory in Southeast Asia

“…However, although female-biased patterns of admixture are observed in Malayo-Polynesian-speaking societies of eastern Indonesia (Cox et al 2010;Xu et al 2012), the general Philippine population is sex neutral in this respect (Cox et al 2010). Among Philippine negrito groups in northern Luzon, both male-and female-biased effective population sizes are observed (Heyer et al this issue).…”

The Checkered Prehistory of Rice Movement Southwards as a Domesticated Cereal—from the Yangzi to the Equator

“…The movement of rice southeastwards through Indonesia eventually ceased owing to the presence of a resistant Papuan-speaking population, still dominant today in New Guinea, that had no interest in its adoption as a viable crop. The density and food-producing status of this indigenous population brought the Malayo-Polynesian migration to a linguistic and genetic standstill in the southeastern corner of Indonesia (Lansing et al 2011;Cox et al 2010;Karafet et al 2010). There is really no clear evidence at all for any migration of MalayoPolynesian-speaking populations from west to east in the vicinity of New Guinea, neither to its north nor to its south, and it is suggested here that they moved in the opposite direction, from the Bismarcks to Indonesia.…”

Genetic Diversity of Four Filipino Negrito Populations from Luzon: Comparison of Male and Female Effective Population Sizes and Differential Integration of Immigrants into Aeta and Agta Communities

“…A previous estimate for admixture based on SNPs found that the Asian contribution to another group of Aeta was approximately 17% smaller for the X chromosome than for the autosomes, while balanced among the general Philippine population (Cox et al 2010). Although our own nuclear DNA data indicate different sex-specific behaviors between negrito populations, we only compare these groups to the general population using haploid loci.…”

“…It was proposed that this sex-biased genetic admixture involving Austronesian women and Near Oceanic men was the result of the matrilineal structure and matrilocal residence pattern of Austronesian societies in the past (Jordan et al 2009;Lansing et al 2011). An exception to this global trend can be found in an Aeta group from the Luzon region of the Philippines, where X-chromosome admixture levels were significantly lower than those for the autosomes; in contrast, the non-negrito populations studied had balanced amounts of admixture (Cox et al 2010).…”

“…Although single-locus studies may not accurately reflect the actual demographic history, a comparison of X-chromosomal and autosomal single-nucleotide polymorphism (SNP) data from Indonesia (Cox et al 2010) reached the same conclusion of a strong sex bias to patterns of admixture, such that Asian women made a higher contribution to the resulting gene pool. It was proposed that this sex-biased genetic admixture involving Austronesian women and Near Oceanic men was the result of the matrilineal structure and matrilocal residence pattern of Austronesian societies in the past (Jordan et al 2009;Lansing et al 2011).…”