Melanesian origin of Polynesian Y chromosomes

BACKGROUND: Two competing hypotheses for the origins of Polynesians are the 'express-train' model, which supposes a recent and rapid expansion of Polynesian ancestors from Asia/Taiwan via coastal and island Melanesia, and the 'entangled-bank' model, which supposes a long history of cultural and genetic interactions among Southeast Asians, Melanesians and Polynesians. Most genetic data, especially analyses of mitochondrial DNA (mtDNA) variation, support the express-train model, as does linguistic and archaeological evidence. Here, we used Y-chromosome polymorphisms to investigate the origins of Polynesians. RESULTS: We analysed eight single nucleotide polymorphisms (SNPs) and seven short tandem repeat (STR) loci on the Y chromosome in 28 Cook Islanders from Polynesia and 583 males from 17 Melanesian, Asian and Australian populations. We found that all Polynesians belong to just three Y-chromosome haplotypes, as defined by unique event polymorphisms. The major Y haplotype in Polynesians (82% frequency) was restricted to Melanesia and eastern Indonesia and most probably arose in Melanesia. Coalescence analysis of associated Y-STR haplotypes showed evidence of a population expansion in Polynesians, beginning about 2,200 years ago. The other two Polynesian Y haplotypes were widespread in Asia but were also found in Melanesia. CONCLUSIONS: All Polynesian Y chromosomes can be traced back to Melanesia, although some of these Y-chromosome types originated in Asia. Together with other genetic and cultural evidence, we propose a new model of Polynesian origins that we call the 'slow-boat' model: Polynesian ancestors did originate from Asia/Taiwan but did not move rapidly through Melanesia; rather, they interacted with and mixed extensively with Melanesians, leaving behind their genes and incorporating many Melanesian genes before colonising the Pacific.     

The impact of the Austronesian expansion: evidence from mtDNA and Y chromosome diversity in the Admiralty Islands of Melanesia

The genetic ancestry of Polynesians can be traced to both Asia and Melanesia, which presumably reflects admixture occurring between incoming Austronesians and resident non-Austronesians in Melanesia before the subsequent occupation of the greater Pacific; however, the genetic impact of the Austronesian expansion to Melanesia remains largely unknown. We therefore studied the diversity of nonrecombining Y chromosomal (NRY) and mitochondrial (mt) DNA in the Admiralty Islands, located north of mainland Papua New Guinea, and updated our previous data from Asia, Melanesia, and Polynesia with new NRY markers. The Admiralties are occupied today solely by Austronesian-speaking groups, but their human settlement history goes back 20,000 years prior to the arrival of Austronesians about 3,400 years ago. On the Admiralties, we found substantial mtDNA and NRY variation of both Austronesian and non-Austronesian origins, with higher frequencies of Asian mtDNA and Melanesian NRY haplogroups, similar to previous findings in Polynesia and perhaps as a consequence of Austronesian matrilocality. Thus, the Austronesian language replacement on the Admiralties (and elsewhere in Island Melanesia and coastal New Guinea) was accompanied by an incomplete genetic replacement that is more associated with mtDNA than with NRY diversity. These results provide further support for the "Slow Boat" model of Polynesian origins, according to which Polynesian ancestors originated from East Asia but genetically mixed with Melanesians before colonizing the Pacific. We also observed that non-Austronesian groups of coastal New Guinea and Island Melanesia had significantly higher frequencies of Asian mtDNA haplogroups than of Asian NRY haplogroups, suggesting sex-biased admixture perhaps as a consequence of non-Austronesian patrilocality. We additionally found that the predominant NRY haplogroup of Asian origin in the Admiralties (O-M110) likely originated in Taiwan, thus providing the first direct Y chromosome evidence for a Taiwanese origin of the Austronesian expansion. Furthermore, we identified a NRY haplogroup (K-P79, also found on the Admiralties) in Polynesians that most likely arose in the Bismarck Archipelago, providing the first direct link between northern Island Melanesia and Polynesia. These results significantly advance our understanding of the impact of the Austronesian expansion and human history in the Pacific region.     

Melanesian mtDNA complexity

Melanesian populations are known for their diversity, but it has been hard to grasp the pattern of the variation or its underlying dynamic. Using 1,223 mitochondrial DNA (mtDNA) sequences from hypervariable regions 1 and 2 (HVR1 and HVR2) from 32 populations, we found the among-group variation is structured by island, island size, and also by language affiliation. The more isolated inland Papuan-speaking groups on the largest islands have the greatest distinctions, while shore dwelling populations are considerably less diverse (at the same time, within-group haplotype diversity is less in the most isolated groups). Persistent differences between shore and inland groups in effective population sizes and marital migration rates probably cause these differences. We also add 16 whole sequences to the Melanesian mtDNA phylogenies. We identify the likely origins of a number of the haplogroups and ancient branches in specific islands, point to some ancient mtDNA connections between Near Oceania and Australia, and show additional Holocene connections between Island Southeast Asia/Taiwan and Island Melanesia with branches of haplogroup E. Coalescence estimates based on synonymous transitions in the coding region suggest an initial settlement and expansion in the region at approximately 30-50,000 years before present (YBP), and a second important expansion from Island Southeast Asia/Taiwan during the interval approximately 3,500-8,000 YBP. However, there are some important variance components in molecular dating that have been overlooked, and the specific nature of ancestral (maternal) Austronesian influence in this region remains unresolved.     

Globin genes in Micronesia: origins and affinities of Pacific Island peoples.

DNA polymorphisms and copy-number variants of alpha-, zeta-, and gamma-globin genes have been studied in seven Micronesian island populations and have been compared with those in populations from Southeast Asia, Melanesia, and Polynesia. Micronesians are not significantly different from Polynesians at these loci and appear to be intermediate between Southeast Asians and Melanesians. There is evidence of significant Melanesian input into the Micronesian gene pool and of substantial proto-Polynesian contact with Melanesia.     

A 9.1-kb insertion/deletion polymorphism suggests a common pattern of genetic diversity in Island Melanesia

Earlier reports suggest a distinct pattern of genetic variation linked to both language and geographic distance in Island Melanesia. Inland Papuan-speaking populations from different islands tend to share one allelic profile, while shore-based or more cosmopolitan populations share another, related to Southeast Asian influence over the past 3000 years. In the present paper, we report the genotypes and allele frequencies of an informative 9.1-thousand-base-pairs (kb) insertion/deletion polymorphism in 19 populations living in Island Melanesia. The populations studied inhabit the islands of New Britain, New Ireland, New Hanover, and Mussau in the Bismarck Archipelago, and speak either Austronesian or Papuan languages. We also include for reference a collection from New Guinea and Bougainville. The data show a marked fluctuation in the allele frequency among the different isolates, with the 9.1-kb(-) allele frequency ranging from 0.67 to 0.98. The deletion allele reaches fixation in some Papuan-speaking interior populations of New Britain, as well as in the interiors of New Guinea and Bougainville. However, certain inland Austronesian-speaking populations also share a similar high frequency of the deletion. Our data suggest that language distinctions are generally, but not invariably, indicative of diverse allelic patterns in this complex region, where inland groups on large islands tend to be often distinctive from shore-based populations.     

Mitochondrial DNA variation is an indicator of austronesian influence in Island Melanesia.

Past studies have shown a consistent association of a specific set of mitochondrial DNA 9 base pair (bp) deletion haplotypes with Polynesians and their Austronesian-speaking relatives, and the total lack of the deletion in a short series of New Guinea Highlanders. Utilizing plasma and DNA samples from various old laboratory collections, we have extended population screening for the 9-bp deletion into "Island Melanesia," an area notorious for its extreme population variation. While the 9-bp deletion is present in all Austronesian, and many non-Austronesian-speaking groups, it is absent in the more remote non-Austronesian populations in Bougainville and New Britain. These results are consistent with the hypothesis that this deletion was first introduced to this region about 3,500 years ago with the arrival of Austronesian-speaking peoples from the west, but has not yet diffused through all populations there. The pattern cannot be reconciled with the competing hypothesis of a primarily indigenous Melanesian origin for the ancestors of the Polynesians. Although selection clearly has operated on some other genetic systems in this region, both migration and random genetic drift primarily account for the remarkable degree of biological diversity in these small Southwest Pacific populations.     

Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific

The human settlement of the Pacific Islands represents one of the most recent major migration events of mankind. Polynesians originated in Asia according to linguistic evidence or in Melanesia according to archaeological evidence. To shed light on the genetic origins of Polynesians, we investigated over 400 Polynesians from 8 island groups, in comparison with over 900 individuals from potential parental populations of Melanesia, Southeast and East Asia, and Australia, by means of Y chromosome (NRY) and mitochondrial DNA (mtDNA) markers. Overall, we classified 94.1% of Polynesian Y chromosomes and 99.8% of Polynesian mtDNAs as of either Melanesian (NRY-DNA: 65.8%, mtDNA: 6%) or Asian (NRY-DNA: 28.3%, mtDNA: 93.8%) origin, suggesting a dual genetic origin of Polynesians in agreement with the "Slow Boat" hypothesis. Our data suggest a pronounced admixture bias in Polynesians toward more Melanesian men than women, perhaps as a result of matrilocal residence in the ancestral Polynesian society. Although dating methods are consistent with somewhat similar entries of NRY/mtDNA haplogroups into Polynesia, haplotype sharing suggests an earlier appearance of Melanesian haplogroups than those from Asia. Surprisingly, we identified gradients in the frequency distribution of some NRY/mtDNA haplogroups across Polynesia and a gradual west-to-east decrease of overall NRY/mtDNA diversity, not only providing evidence for a west-to-east direction of Polynesian settlements but also suggesting that Pacific voyaging was regular rather than haphazard. We also demonstrate that Fiji played a pivotal role in the history of Polynesia: humans probably first migrated to Fiji, and subsequent settlement of Polynesia probably came from Fiji.     

The dentition of New Britain West Nakanai Melanesians. VIII. Peopling of the pacific

The dental crown morphology and size of 48 male West Nakanai, New Britain, Melanesians is described and compared with other Pacific and Asian dental samples. The West Nakanai dentition is like those of other Melanesians, much less like those of Polynesians and Micronesians, and very dissimilar to teeth of modern and Neolithic Southeast Asians. It is suggested that the origin of the modern Melanesian dental pattern (large but simplified teeth) was probably in Melanesia, not Southeast Asia as the orthodox view of a Hoabinhian-Australmelanesian relation claims.     

Genetic affinities of oceanic populations based on RFLP and haplotype analysis of genetic loci on three chromosomes.

Restriction fragment length polymorphisms at the renin and factor 13B loci located at chromosome 1q32-1q42 were studied in 14 ethnic groups in the west Pacific region. The allele frequencies were combined with previously described beta-globin and albumin-vitamin D binding protein haplotype frequencies and used to assess genetic affinities among eight major ethnic-geographic groups in this region. These population groups divide into two clusters with Australian Aborigines, Island Melanesians, and Highland Melanesians forming one cluster and east Asians, Southeast Asians, Micronesians, and Polynesians forming the other. The results indicate that Micronesians and Polynesians are derived from populations in Southeast Asia and that they originated independently of the Melanesian populations.     

Independent histories of human Y chromosomes from Melanesia and Australia

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.     

The peopling of New Guinea: evidence from class I human leukocyte antigen.

This study utilizes newly developed direct DNA typing methods for human leukocyte antigens (HLA) to provide new information about the peopling of New Guinea. The complete polymorphism of eight Melanesian populations was examined. The groups included were highlanders, northern and southern highlands fringe populations, a Sepik population, northern and southern coastal New Guinea populations, and populations from the Bismarck Archipelago and New Caledonia. The study concluded that, based on HLA and other evidence. Melanesians are likely to have evolved largely from the same ancestral stock as Aboriginal Australians but to have since differentiated. Highlanders are likely to be descendants of earlier migrations who have been isolated for a long period of time. Northern highlands fringe and Sepik populations are likely to share a closer common ancestry but to have differentiated due to long term isolation and the relative proximity to the coast of the Sepik. Southern fringe populations are likely to have a different origin, possibly from the Gulf region, although there may be some admixture with neighboring groups. Coastal populations have a wider range of polymorphisms because of the genetic trail left by later population movement along the coast from Asia that did not reach Australia or remote Oceania. Other polymorphisms found in these populations may have been introduced by the movement of Austronesian-speaking and other more recent groups of people into the Pacific, because they share many polymorphisms with contemporary southeast Asians, Polynesians, and Micronesians that are not found in highlanders or Aboriginal Australians. There is evidence suggestive of later migration to Melanesia from Polynesia and Micronesia.     

Population Genetic Structure and Origins of Native Hawaiians in the Multiethnic Cohort Study

The population genetic structure of Native Hawaiians has yet to be comprehensively studied, and the ancestral origins of Polynesians remain in question. In this study, we utilized high-resolution genome-wide SNP data and mitochondrial genomes of 148 and 160 Native Hawaiians, respectively, to characterize their population structure of the nuclear and mitochondrial genomes, ancestral origins, and population expansion. Native Hawaiians, who self-reported full Native Hawaiian heritage, demonstrated 78% Native Hawaiian, 11.5% European, and 7.8% Asian ancestry with 99% belonging to the B4 mitochondrial haplogroup. The estimated proportions of Native Hawaiian ancestry for those who reported mixed ancestry (i.e. 75% and 50% Native Hawaiian heritage) were found to be consistent with their self-reported heritage. A significant proportion of Melanesian ancestry (mean = 32%) was estimated in 100% self-reported Native Hawaiians in an ADMIXTURE analysis of Asian, Melanesian, and Native Hawaiian populations of K = 2, where K denotes the number of ancestral populations. This notable proportion of Melanesian admixture supports the “Slow-Boat” model of migration of ancestral Polynesian populations from East Asia to the Pacific Islands. In addition, approximately 1,300 years ago a single, strong expansion of the Native Hawaiian population was estimated. By providing important insight into the underlying population structure of Native Hawaiians, this study lays the foundation for future genetic association studies of this U.S. minority population.     

Affinities among Melanesians,Micronesians, and Polynesians: a neutral biparental genetic perspective

The human colonization of Remote Oceania, the vast Pacific region including Micronesia, Polynesia, and Melanesia beyond the northern Solomon Islands, ranks as one of the greatest achievements of prehistory. Many aspects of human diversity have been examined in an effort to reconstruct this late Holocene expansion. Archaeolinguistic analyses describe a rapid expansion of Austronesian-speaking "Lapita people" from Taiwan out into the Pacific. Analyses of biological markers, however, indicate genetic contributions from Pleistocene-settled Near Oceania into Micronesia and Polynesia, and genetic continuity across Melanesia. Thus, conflicts between archaeolinguistic and biological patterns suggest either linguistic diffusion or gene flow across linguistic barriers throughout Melanesia. To evaluate these hypotheses and the general utility of linguistic patterns for conceptualizing Pacific prehistory, we analyzed 14 neutral, biparental genetic (short tandem repeat) loci from 965 individuals representing 27 island Southeast Asian, Melanesian, Micronesian, and Polynesian populations. Population bottlenecks during the colonization of Remote Oceania are indicated by a statistically significant regression of loss of heterozygosity on migration distance from island Southeast Asia (r = 0.78, p < 0.001). Genetic and geographic distances were consistently correlated (r > 0.35, p < 0.006), indicating extensive gene flow primarily focused among neighboring populations. Significant correlations between linguistic and geographic patterns and between genetic and linguistic patterns depended upon the inclusion of Papuan speakers in the analyses. These results are consistent with an expansion of Austronesian-speaking populations out of island Southeast Asia and into Remote Oceania, followed by substantial gene flow from Near Oceanic populations. Although linguistic and genetic distinctions correspond at times, particularly between Western and Central-Eastern Micronesia, gene flow has reduced the utility of linguistic data within Melanesia. Overall, geographic proximity is a better predictor of biparental genetic relationships than linguistic affinities.     

Increased Y-chromosome resolution of haplogroup O suggests genetic ties between the Ami aborigines of Taiwan and the Polynesian Islands of Samoa and Tonga

The Austronesian expansion has left its fingerprint throughout two thirds of the circumference of the globe reaching the island of Madagascar in East Africa to the west and Easter Island, off the coast of Chile, to the east. To date, several theories exist to explain the current genetic distribution of Austronesian populations, with the “slow boat” model being the most widely accepted, though other conjectures (i.e., the “express train” and “entangled bank” hypotheses) have also been widely discussed. In the current study, 158 Y chromosomes from the Polynesian archipelagos of Samoa and Tonga were typed using high resolution binary markers and compared to populations across Mainland East Asia, Taiwan, Island Southeast Asia, Melanesia and Polynesia in order to establish their patrilineal genetic relationships. Y-STR haplotypes on the C2 (M38), C2a (M208), O1a (M119), O3 (M122) and O3a2 (P201) backgrounds were utilized in an attempt to identify the differing sources of the current Y-chromosomal haplogroups present throughout Polynesia (of Melanesian and/or Asian descent). We find that, while haplogroups C2a, S and K3-P79 suggest a Melanesian component in 23%-42% of the Samoan and Tongan Y chromosomes, the majority of the paternal Polynesian gene pool exhibits ties to East Asia. In particular, the prominence of sub-haplogroup O3a2c* (P164), which has previously been observed at only minimal levels in Mainland East Asians (2.0-4.5%), in both Polynesians (ranging from 19% in Manua to 54% in Tonga) and Ami aborigines from Taiwan (37%) provides, for the first time, evidence for a genetic connection between the Polynesian populations and the Ami.     

Genome-wide analysis indicates more Asian than Melanesian ancestry of Polynesians

Analyses of mitochondrial DNA (mtDNA) and nonrecombining Y chromosome (NRY) variation in the same populations are sometimes concordant but sometimes discordant. Perhaps the most dramatic example known of the latter concerns Polynesians, in which about 94% of Polynesian mtDNAs are of East Asian origin, while about 66% of Polynesian Y chromosomes are of Melanesian origin. Here we analyze on a genome-wide scale, to our knowledge for the first time, the origins of the autosomal gene pool of Polynesians by screening 377 autosomal short tandem repeat (STR) loci in 47 Pacific Islanders and compare the results with those obtained from 44 Chinese and 24 individuals from Papua New Guinea. Our data indicate that on average about 79% of the Polynesian autosomal gene pool is of East Asian origin and 21% is of Melanesian origin. The genetic data thus suggest a dual origin of Polynesians with a high East Asian but also considerable Melanesian component, reflecting sex-biased admixture in Polynesian history in agreement with the Slow Boat model. More generally, these results also demonstrate that conclusions based solely on uniparental markers, which are frequently used in population history studies, may not accurately reflect the history of the autosomal gene pool of a population.     

Earliest Pottery on New Guinea Mainland Reveals Austronesian Influences in Highland Environments 3000 Years Ago

Austronesian speaking peoples left Southeast Asia and entered the Western Pacific c.4000-3000 years ago, continuing on to colonise Remote Oceania for the first time, where they became the ancestral populations of Polynesians. Understanding the impact of these peoples on the mainland of New Guinea before they entered Remote Oceania has eluded archaeologists. New research from the archaeological site of Wañelek in the New Guinea Highlands has broken this silence. Petrographic and geochemical data from pottery and new radiocarbon dating demonstrates that Austronesian influences penetrated into the highland interior by 3000 years ago. One potsherd was manufactured along the northeast coast of New Guinea, whereas others were manufactured from inland materials. These findings represent the oldest securely dated pottery from an archaeological context on the island of New Guinea. Additionally, the pottery comes from the interior, suggesting the movements of people and technological practices, as well as objects at this time. The antiquity of the Wañelek pottery is coincident with the expansion of Lapita pottery in the Western Pacific. Such occupation also occurs at the same time that changes have been identified in subsistence strategies in the archaeological record at Kuk Swamp suggesting a possible link between the two.     

Melanesians and Polynesians share a unique alpha-thalassemia mutation.

Several genetic markers that provide information on population migrations and affinities have been detected by studies of proteins and cellular antigens in blood. Analysis of DNA polymorphisms promises to yield many further population markers, and we report here the distribution of a new alpha-globin gene deletion (-alpha 3.7 III) detected by a restriction enzyme mapping. This is found frequently in Melanesians and Polynesians but not in five other populations in which alpha-thalassemia is prevalent. We used restriction enzyme haplotype analysis to support a single origin for this mutation and propose that it is a useful population marker. Its geographical distribution supports a route through Island Melanesia for the colonizers of Polynesia.     

The colonization of the Pacific: the story according to human leukocyte antigens.

The human leukocyte antigen (HLA) distributions in 16 Pacific populations have been collated from published and unpublished reports. Gene frequency and linkage disequilibrium relationships among groups show that Australians and Papuans share a common ancestry, that coastal Melanesia has about 16% Austronesian admixture, and that Fiji is truly intermediate between Melanesia and Polynesia. In Polynesia, Cook Islanders show closer affinity with populations of Western Polynesia than with Maoris and Easter Islanders, in contrast to their linguistic affiliations, but otherwise HLA distributions show a clear division between the populations of Eastern and Western Polynesia. This study emphasizes the contribution the HLA system can make to anthropological studies and has provided a version of colonization of the Pacific compatible with theories based on prodigious efforts in many disciplines.     

The mode of inheritance of ovalocytosis/elliptocytosis in Malaysian Orang Asli families

Summary Hereditary ovalocytosis/elliptocytosis occurs in polymorphic frequencies among several Malaysian populations and also in Melanesia. Although the condition has been described as an autosomal dominant, Melanesian family studies suggest that it is inherited recessively. Based on 75 Orang Asli families, it is shown that the Malaysian form of elliptocytosis is most likely inherited as an autosomal dominant. It appears, therefore, that either the inference of recessive inheritance in Melanesians is incorrect or that the ovalocytosis/elliptocytosis phenotypes are due to distinct genetic entities in the two regions.     

The incidence and expression of the subcondylar tubercle of the mandible in early Polynesians, modern Indians and modern Europeans

A sample of pre-European Polynesian and Melanesian mandibles, modern Asian Indians and cadaveric European mandibles were investigated to establish the prevalence of a subcondylar tubercle and to attempt to relate its presence to mandibular function. Among the three population samples, the subcondylar tubercle appeared 1.5 times more frequently among the Polynesians/Melanesians, than either the Indian or European groups. It was fairly equally present on both sides in all three groups. Where it was present unilaterally, it was far more likely to be present on the left side. This left-side presence coincided with a significantly greater right-side condylar height and ramal width.