Complete mitochondrial DNA genome variation in Peninsular Malaysia

The peopling of Southeast Asia has been vigorously debated over the past few decades by archaeologists, linguists and anthropologists, as well as evolutionary and population geneticists. Several ethnic minorities in the region, the Orang Asli groups (the Semang, Senoi and Aboriginal Malays) from Peninsular Malaysia, are widely thought of as “relicts” of human diversity in the ancient Sunda continent. However, mitochondrial DNA (mtDNA analysis of these groups has hitherto been restricted to a small number of populations and largely based on the mtDNA control region hypervariable segment I (HVS-I), supplemented by a very small number of whole-mtDNA genomes. In this study, I have both expanded the number of populations examined and analysed 226 lineages at the level of whole-mtDNA genomes from both Orang Asli and modern Malay populations, covering most of the extant mtDNA diversity in Peninsular Malaysia, in the context of Southeast Asian variation more generally, including a total of 2206 complete mtDNA sequences in the phylogeographic analysis. This has confirmed that the Orang Asli populations indeed experienced high genetic drift, likely due to their extremely small group sizes and population subdivision. All three Orang Asli groups have local roots that trace back to ~50 ka, and all have been affected to a greater or lesser extent by subsequent migrations to Peninsular Malaysia. The Semang and Senoi show much less haplogroup diversity than the Aboriginal Malays, although the latter have some indigenous ancestry that is as deep as that of the Semang and Senoi in Peninsular Malaysia. However, this drift, and the loss of lineages that it has entailed, is compensated for by the retention of many related ancient lineages in the extant modern Malay, who therefore provide a more comprehensive view of ancient Malay Peninsula, and more generally ancient Sunda, mtDNA diversity. Indeed, contrary to the model that posits a recent ancestry for Malay in Island Southeast Asia (ISEA), a majority of their maternal lineages appear to have had a local ancestry within Mainland Southeast Asia (MSEA) and the Malay Peninsula. Combining the Orang Asli and Malay data indicates a very deep ancestry for multiple indigenous maternal lineages that date back locally (or regionally) to the late Pleistocene. Many can be traced to the original inhabitants of Southeast Asia, who colonised the Sunda region from South Asia ~50–60 ka. It appears that the spread of the so-called “Coastal Neolithic” foraging groups (who may have engaged in horticulture, but were largely pre-rice agriculture) may have provided the main contribution to the north–south lineage expansions and the spread of Austro-Asiatic languages to the Orang Asli and to the Nicobars may be connected to some of these dispersals. Apart from preserving these ancient lineages, many of which have been lost by drift in the relict populations, the modern Malay also preserve complex maternal influences from further afield at various times stretching back to the Last Glacial Maximum, from ISEA (as far east as the New Guinea region), to a lesser extent from East Asia, and to an even lesser extent South Asia. Climatic change and sea-level rises were likely the most important driving force behind the demographic history of Southeast Asia, mainland as well as insular, as shown by a sharp signal of early Holocene population crash and subsequent re-expansion in both the modern Malay and the Orang Asli. Although there is substantial lineage sharing between modern Malay and their close Sunda neighbours in Sumatra, ISEA lineages amount to little more than a quarter of the maternal variation of Malay, and even if there was a major migration to the Peninsula in the Late Holocene, the majority of their maternal ancestry seems to lie within the bounds of the Sunda continent