pmc.ncbi.nlm.nih.gov

Maternal History of Oceania from Complete mtDNA Genomes: Contrasting Ancient Diversity with Recent Homogenization Due to the Austronesian Expansion

Abstract

Archaeology, linguistics, and existing genetic studies indicate that Oceania was settled by two major waves of migration. The first migration took place approximately 40 thousand years ago and these migrants, Papuans, colonized much of Near Oceania. Approximately 3.5 thousand years ago, a second expansion of Austronesian-speakers arrived in Near Oceania and the descendants of these people spread to the far corners of the Pacific, colonizing Remote Oceania. To assess the female contribution of these two human expansions to modern populations and to investigate the potential impact of other migrations, we obtained 1,331 whole mitochondrial genome sequences from 34 populations spanning both Near and Remote Oceania. Our results quantify the magnitude of the Austronesian expansion and demonstrate the homogenizing effect of this expansion on almost all studied populations. With regards to Papuan influence, autochthonous haplogroups support the hypothesis of a long history in Near Oceania, with some lineages suggesting a time depth of 60 thousand years, and offer insight into historical interpopulation dynamics. Santa Cruz, a population located in Remote Oceania, is an anomaly with extreme frequencies of autochthonous haplogroups of Near Oceanian origin; simulations to investigate whether this might reflect a pre-Austronesian versus Austronesian settlement of the island failed to provide unequivocal support for either scenario.

Main Text

Within the boundaries of Oceania, one of the first and one of the last major colonization events by anatomically modern humans occurred. Settlement of New Guinea and Australia, which were then joined as a single landmass known as Sahul, occurred at least 44 kiloannum (ka) ago1,2 and humans spread essentially instantaneously across the Vitiaz Straight and to the islands of the Bismarck Archipelago.3,4 Descendants of this initial expansion voyaged and settled at least as far as Buka at the northernmost tip of the Solomons archipelago by 28 ka ago,5 and Manus in the Admiralty Islands by 12 ka ago,6 indicating that they possessed sufficient watercraft and sailing skills to voyage at least 200 km. However, there are no indications that they made regular long-distance voyages beyond Near Oceania,7 which comprises New Guinea, the Bismarck Archipelago, and the Solomon Islands as far southeast as Makira. Instead, it seems that the settlement of Remote Oceania (comprising the Reef Islands, Santa Cruz, Vanuatu, New Caledonia, Fiji, and Polynesia) and possibly much of the Solomon Islands8 was achieved by the descendants of an expansion that began in Taiwan (or possibly elsewhere in Southeast Asia) about 5–6 ka ago,9–11 reached Near Oceania between 3.5 and 3.3 ka ago,12–14 and were the first to colonize areas in Remote Oceania beginning around 3.1 ka ago,15 culminating in the settlement of the Hawai’ian Islands,16 Easter Island,17 and New Zealand18 within the last 800–1,200 years.

Each of these two major expansion events is associated by anthropologists, archaeologists, and linguists with peoples, phenotypes, cultures, and languages. People believed to be descended from the first expansion within Near Oceania are often referred to as Papuan, generally practice patrilocality, tend to have darker skin pigmentation reflecting the root of the region’s historical name—Melanesia—as the “dark islands,”7 and speak languages that appear to be so old and deep rooting that linguists are still unsure about their true relationships.19,20 By contrast, the second migration into Near Oceania is indicated by the presence of a particular material culture, including, but not limited to, a distinctive style of pottery (Lapita) and is associated with speakers of Austronesian languages that are clearly related and descended from a single language called Proto Oceanic (see Lynch et al.21 and references therein). Reconstructions suggest they lived in small, highly mobile matrilocal groups22 and were phenotypically more similar to Asian populations (e.g., with generally lighter skin pigmentation) than are Papuans.

We can also make genetic ties to both of these founding populations. The Austronesian expansion is associated with the spread of mtDNA haplogroup B, particularly haplogroup B4a1 and its descendent lineages, throughout Island South East Asia, Oceania, and even to Madagascar in the west.10,23–28 In particular, haplogroup B4a1a1a, defined by the “Polynesian motif,”29 an A-G transition at position 16247, and its descendants are associated with the spread of Austronesians throughout Oceania. This haplogroup reaches near fixation in Remote Oceania,24,29,30 though position 16247 has been found to back-mutate repeatedly on independent lineages and as such must be examined carefully.31 Meanwhile, Papuan ancestry is associated with haplogroups Q, P, M27, M28, and M29, which appear to be autochthonous to Near Oceania.24,32,33 Studies of Y chromosome SNPs and short tandem repeats (STRs) also support a dual-parental population model for Oceanians, particularly Remote Oceanians.24,34–36 Interestingly, no single Y chromosome haplogroup is dominant in the same way that mtDNA haplogroup B is predominant in Remote Oceanians and the frequency of Y chromosomes of Near Oceanian origin (∼66%) is much greater than that of Y chromosomes of Asian origin (∼28%).24 Moreover, genome-wide data37–39 support the dual ancestry model with more Asian ancestry than Near Oceanian ancestry in remote Oceania (approximately 80% Asian, 20% Near Oceanian), meaning that the genome-wide average is intermediate between the mtDNA and Y chromosome results.

Apart from these two well-attested population expansions, there is additional evidence to suggest interactions with Southeast Asia around 5 ka ago. Archaeologically this is evidenced in part by the introduction of domesticated pigs to New Guinea,7,40 which is the approximate time frame that previous studies have suggested for the entry of haplogroup E to Near Oceania.25 However, whether these two events are connected remains to be resolved.

In this study, we examined the maternal population structure and the history of admixture across Oceania. Previous studies exploring the maternal histories of the area have been limited because they largely make use of only a small portion of the genome known as the hypervariable region (HVR) (e.g., see Kayser et al.,24 Friedlaender et al.,25 Delfin et al.41); other studies making use of whole mtDNA sequences from Oceania have been limited in terms of sample sizes and number of populations analyzed (e.g., see Soares et al.,42 Benton et al.43). Our data set is, to our knowledge, the most comprehensive to date, and consists of 1,331 whole mitochondrial genome sequences from 34 populations spread from the Bismarck Archipelago to Polynesia (Figure 1). To facilitate comprehension and visualization of the patterns of variation, these 34 populations have been amalgamated into six groups on the basis of geographic proximity and/or shared cultural features (Figure 1). The first group consists of populations from New Britain in the Bismarck Archipelago (Anem, Ata, Nakanai) and the second group consists of populations from Bougainville and Buka (Buin, Buka, Nagovisi, Nasioi, Siwai, Torau), two islands at the northern tip of the Solomons Archipelago that politically are part of Papua New Guinea, and the easternmost site of known settlement in Pleistocene Oceania.5 The only other confirmed pre-Austronesian settlements in the Solomons Archipelago are sites from Guadalcanal with indications of human occupation approximately 6 ka ago.44,45 The third group consists of populations found in the islands of the rest of the Solomons Archipelago (Choiseul, Gela, Guadalcanal, Isabel, Kolombangara, Makira, Malaita, Ranongga, Russell, Savo, Shortlands, Simbo, Vella Lavella). Santa Cruz is the only population to be grouped alone; it is treated separately because it has been shown to be a genetic outlier in previous studies of mtDNA and Y chromosome variation41,46 as well as being linguistically distinct. Originally classified as a Papuan language, currently the Santa Cruz language and closely related languages of the Temotu group are thought to represent a very deep branch of the Oceanic family of Austronesian languages.47 The final two groupings concern populations believed to be predominantly of Austronesian heritage: these include populations from across Remote Oceania ranging geographically from Fiji to the Cook Islands (Cook Islands, Fiji, Futuna, Niue, Samoa, Tonga, Tuvalu), as well as four populations classified as Polynesian Outliers (Bellona, Ontong Java, Rennell, Tikopia). The latter are populations in Near Oceania that, based on linguistic and cultural evidence, are thought to be descended primarily from back migrations from Polynesia.48,49

Figure 1.

Figure 1

Map of Study Area

Populations are colored as to their group assignment: New Britain (black), Bougainville (blue), Solomon Islands main chain (green), Santa Cruz (red), Remote Oceania (gray), Polynesian Outliers (orange). Italicized labels indicate Papuan speaking populations. Additional geographic points mentioned in text are identified in the map inset.

Samples from New Britain were collected, in the form of whole blood, as described previously.25 Plasma from these samples was then shipped to Leipzig where they were extracted in 2011 with the QIAGEN DNeasy Blood and Tissue kit, as per the manufacturer’s protocol. After extraction samples were quantified for human mtDNA content by qPCR as previously described50 and samples that were found to have mtDNA concentrations of less than 5 ng/μl were subjected to whole-genome amplification with the QIAGEN REPLI-G minikit as per the manufacturer’s protocol and then re-extracted with the DNeasy Blood and Tissue kit but replacing the proteinase K incubation with an incubation in QIAGEN Buffer AL. Bougainvillean samples were collected with written informed consent in 2011 as 2 ml of saliva and stored in 2 ml of lysis buffer (50 mM Tris, 50 mM EDTA, 50 mM sucrose, 100 mM NaCl, 1% SDS) as described previously.51 Extraction was completed with the QIAGEN DNA midi-kit. DNA samples from all other populations have been described previously.24,34,41,52,53 This study was approved by the ethics commission of the University of Leipzig Medical Faculty, the National Research Institute of Papua New Guinea, and the Papua New Guinea Medical Research Advisory Committee.

Multiplex sequencing libraries were constructed and enriched for mtDNA sequences according to previous protocols54,55 with additional modifications described previously56 and also below. Various Illumina platforms and lengths of sequencing reads were used during this study; the conditions for each sample are provided in Table S1 available online, along with details concerning the coverage and amount of missing data. The 1,331 samples were aligned with MUSCLE v.3.857 and visualized in BioEdit.58 Heteroplasmies and indels were confirmed with SAMtools.59 There are no significant differences in the number of variant sites called per sequence with respect to coverage or sequencing platform. 536 sequences from the Solomon Islands, Santa Cruz, and Polynesian Outlier populations that belong to haplogroup B4a1a1 and descendent lineages were previously published as part of a study on the instability of the 16247G allele.31

Haplogroups were assigned to consensus sequences for each sample with the Haplogrep webtool and Phylotree Build 15.60,61 The haplogroup assigned to each individual is provided in Table S1, and haplogroup frequencies for each population are in Table S2. The relative frequencies of haplogroups of putative Near Oceanian, Austronesian (haplogroup B and sublineages), or other origin are depicted in Figure 2. In general, the frequencies of haplogroups of putative Near Oceanic origin are greater in New Britain and Bougainville and then decrease in frequency the further out a population is in the Pacific (Figure 2). Two populations that contradict this trend are the Nagovisi of Bougainville, with 97% frequency of haplogroup B, and Santa Cruz, with 85% frequency of Near Oceanian haplogroups (Figure 2).

Figure 2.

Figure 2

Relative Frequency of Near Oceanian, Austronesian, and Other Haplogroups by Population

For designation of haplogroup origin, see Table S2.

Haplogroup B is by far the predominant lineage in this study, accounting for 76% of the sequences. Haplogroup B4a1a1a and sublineages thereof account for 69% alone, confirming previous HVR studies24,25,41 that found that these haplogroups form a gradient of increasing frequency across the Pacific. Building on our previous results,31 we find additional evidence for back-mutations at position 16247 (Figure S1), on the background of both haplogroups B4a1a1a and B4a1a1a1. The general frequency of the back-mutation in haplogroup B4a1a1a1 remains constant at approximately 20% and was found in all groups except Santa Cruz and the three populations from New Britain (Table S2); the latter result probably reflects the low frequency of haplogroup B4a1a1a1 in these populations. In addition, haplogroup B4a1a1a3, identified previously as a Maori-specific haplogroup,43 is present in additional samples from Remote Oceania, reaching a frequency of 14% in the Cook Islands (Table S2).

An analysis of haplotype sharing provides a sense of how ubiquitous haplogroup B is in the Pacific and further supports the recent entry and rapid spread of haplogroup B across Oceania. Haplotype sharing was calculated by an in-house Perl script that compares all sequence pairs. The resultant identity matrix was visualized with the R package ggplot2.62 For all analyses except haplogroup assignment, the poly-C regions (positions 303–315 and 16182–16193) were removed from all sequences. Most pairs of populations share sequences belonging to haplogroup B (Figure 3A), whereas in a similar analysis of all other haplogroups, interpopulation sharing virtually disappears and almost all cases of haplotype sharing are restricted to members of the same population (Figure 3B). Because recent female movement between populations should affect all haplotypes to the same degree, this pattern indicates a comparative lack of recent interpopulation contact. Instead, the high proportion of sharing in haplogroup B is a clear signature of a spread via a not-too-ancient population expansion that involved mostly, if not exclusively, haplogroup B lineages. Although previous HVR studies have also shown high degrees of similarity within haplogroup B samples across Oceania,24,41,63 their conclusions about haplotype sharing are constricted by the small portion of the mtDNA genome analyzed. Here we assess the complete diversity of whole mitochondrial genome and still find high levels of haplotype sharing. That these haplotypes are sometimes shared from New Britain to Remote Oceania (a distance of more than 5,500 km) indicates that this expansion happened over such a short period of time that new mutations did not occur within these haplotypes, nor have they mutated extensively since the initial expansion.

Figure 3.

Figure 3

Haplotype Sharing between Populations

(A) Exclusively haplogroup B.

(B) Excluding haplogroup B.

The scope of the Austronesian expansion and the spread of haplogroup B4a1a1 and descendent lineages is also evidenced in a Bayesian Skyline Plot (BSP)64,65 of population size change through time. The BSP for haplogroup B4a1a1∗ coalesces just after 5 ka ago, or at the approximate time the Austronesian expansion is thought to have begun, and shows a steady increase in effective population size of approximately three orders of magnitude continuing to the present day (Figure 4A). In the middle of this population increase, there is a slight levelling out, or decrease in the rate of size increase, around 3 ka ago which could be a reflection of the “long pause” in exploration that is believed to have occurred after the colonizations of western Polynesia (Fiji, Tonga, Samoa) and before other waves of voyaging and settlement began in eastern Polynesia around 1.7 ka ago.7,66,67

Figure 4.

Figure 4

Bayesian Skyline Plots

(A) Haplogroup B4a1a1∗.

(B) Haplogroup E.

BSP calculations were conducted with the data partitioned between coding and noncoding regions with respective mutation rates of 1.708 × 10−8 ± 0.15 × 10−8 and 9.883 × 10−8 ± 0.15 × 10−8 after Soares et al.88 and the TN93 substitution model allowing for both invariant sites and gamma distribution.

Previous studies have suggested that, based on the reconstructed age of the B4a1a1 haplogroup in Near Oceania, it must have been present in the region before the Austronesian expansion reached the area.42 Although our reconstructions would also suggest a time depth for the lineage that is greater than 3.5 ka (Figure 4A), the reconstructed age of a haplogroup does not necessarily indicate when the haplogroup was introduced into a particular region; it could have been introduced much more recently. Thus, a pre-Lapita age of haplogroup B4a1a1 is not evidence for a pre-Lapita origin in Near Oceania. Moreover, even if haplogroup B4a1a1 was introduced to New Guinea by a pre-Austronesian migration, the subsequent spread of this haplogroup throughout the rest of Near Oceania and across Remote Oceania is clearly associated with the Austronesian dispersal.

Older haplogroups that are thought to be autochthonous to Near Oceania include M27, M28, M29, Q, and P.24,32,33 Within these older lineages, we find not only greater geographic specificity and much less sequence sharing than for haplogroup B lineages (Figures 3B and 5, Table S2) but also several new lineages; these haplogroups are underrepresented in the literature. We find three distinct lineages of haplogroup M27 that diverged from each other about 60,000 years ago (Figure 6) and are notably found only in populations from Bougainville and the main Solomon Islands, with the exception of a single individual from Santa Cruz with M27b (Table S2). All samples identified as M27b in this study are missing 8 of the 25 diagnostic mutations for M27b (Phylotree Build 15), and all except one of the samples lack a ninth diagnostic position, and hence are most likely a sister lineage to those M27b lineages already identified in the area33 (Figure S2). Also widespread are haplogroups M28a, identified in populations from all groups save the Polynesian Outliers, and Q1, which was found in 40% of the samples from Santa Cruz (Table S2). Some of the sublineages of Q1 appear to have regional specificity (such as Q1 + 16223!, found in New Britain only) (Table S2), but on closer examination many of these sequences did not meet the full requirements for the sublineage to which they were assigned by Haplogrep. These probably represent new lineages that help refine the phylogeny of haplogroup Q, as some of the existing diagnostic mutations may not be suitable markers because they appear on multiple independent branches (Figure S3). With our larger sample size and wide geographic coverage, we have been able to identify greater levels of diversity for the autochthonous lineages of Oceania than have been previously available based on HVR data or a small sample of whole genomes selected for sequencing on the basis of their HVR sequence.32,33

Figure 5.

Figure 5

Network of All Haplogroups of Putative Near Oceanian Origin

Networks were generated with the program Network and calculated first with a reduced median algorithm89 and then a median joining algorithm90 and with transversions weighted three times greater than transitions. Networks were postprocessed with the program Network Publisher.

Figure 6.

Figure 6

Schematic of Haplogroups and Coalescence Times for Haplogroups Found in Oceania, Based on Bayesian Phylogenetic Analyses and Mutation Rates

B4a1a1/B4a1a1a/B4a1a1a3/B4a1a1a4 are represented as a single clade. B4a1a1a3 and B4a1a1a4 branch from diversity within B4a1a1a and because of the recurrent back-mutations of the 16247G allele, the Bayesian tree does not accurately resolve the relationship between B4a1a1, B4a1a1a, and B4a1a1a1. The age estimates for haplogroups in the B4a1a1 lineage are therefore only approximate. Individual schematics for haplogroups B, E, M27/M28/M29/M∗, M7c3c, Q, and P were constructed from Bayesian maximum clade credibility trees generated by BEAST65 and TreeAnnotator91 with parameters as described in the legend of Figure 4. These six individual schematics were then arranged as per the current accepted mtDNA phylogeny (Phylotree Build 15); connections assigned by the authors are indicated by dashed lines.

Finally, a previously undocumented lineage that is here termed M∗ (Table S2) is likely to be another autochthonous haplogroup of Near Oceania. Found in Bougainville, the main Solomon Islands, and Santa Cruz, the divergence of this lineage is estimated at about 60 ka ago from an ancestral M28-M29 lineage (Figure 6). No close relatives to this lineage have been reported based on either complete mtDNA genome sequences or HVR sequences, save one HVR sequence from the Torau population of Bougainville25 and one HVR sequence from Vanuatu68 that share the diagnostic 16290A transversion. The M∗ lineages coalesce about 5.9 ka ago, which is much more recent than other autochthonous Near Oceanian lineages (Figure 6) and could therefore suggest an origin for M∗ outside of Near Oceania that then spread to Near Oceania before 5.9 ka ago. However, given that M∗ has not been found outside Near Oceania, despite the wealth of mtDNA sequence information available for Southeast Asia, its recent coalescent time probably reflects a bottleneck event sometime within the last 6 ka.

Beyond the lineages that are associated with either the original settlement of Sahul or the Austronesian expansion, the presence of other lineages in Near Oceania may suggest other population influences. The frequency distribution of haplogroup E is notably different from that of haplogroup B (Table S2), and its extreme frequency in the Ata, a Papuan speaking population from New Britain, has led to the suggestion that haplogroup E entered Near Oceania separately from the Austronesian expansion.25 Haplogroup E1b1 is found in more than 45% of samples from the Ata in New Britain, a population notable as the only one in this study with no observed haplogroup B, making it quite different from its neighbors in New Britain (Figure 2). Overall, haplogroup E1 lineages are restricted to New Britain, Bougainville, and the Solomons, while the only haplogroup E2 lineage, E2a, was found in just three samples from Isabel in the Solomon Islands. Haplogroup E is found in reasonably high frequency across much of Island Southeast Asia (ISEA) and also in Taiwan but is almost completely absent from mainland Asia.10,69–75 The absence of two major clades of haplogroup E in Taiwan (E1b and E2a), as well as the greater overall sequence diversity found in ISEA, has led some to posit that the lineage must have originated in ISEA during the last glacial maximum while the region was still part of the larger continent of Sunda.70 E1b is the most frequent lineage of haplogroup E found in this study (Table S2) and it is conspicuously absent in Taiwan and the Philippines,71,72,74 which would suggest a different source for entry into Near Oceania. In the reconstructed history of haplogroup E through the BSP, we note that despite having only 28 samples from haplogroup E, the coalescence time is approximately 14 ka ago, far earlier than that of haplogroup B4a1a1∗ (Figure 4B). Although this cannot be taken as evidence that this haplogroup has been present in Near Oceania for 14 ka, we do believe that this further supports the hypothesis that this haplogroup arrived in the area via a population expansion separate from haplogroup B and the Austronesian expansion. Still, this putative migration had a minimal impact on the maternal genetic structure of Oceania, as indicated by the fact that haplogroup E accounts for only about 2% of the mtDNA sequences in this study.

Haplogroup M7c3c was found in elevated frequency (∼25%) only in Ontong Java (Table S2); it also occurred in one individual each from Vella Lavella and Tuvalu. Although M7c3c (“M7c1c” in some earlier publications10,24,69,76) is found in Taiwanese aborigines,10,69 the purported source populations of the Austronesian expansion, it is also widespread across ISEA69,71–77 but is virtually absent in Near Oceania (Table S2). Because this haplogroup distribution does not seem to reflect the same history as that of haplogroup B (or haplogroup E), M7c3c could potentially represent a different migration other than the Austronesian expansion, possibly from ISEA and Indonesia because these are believed to have sustained contact with Near Oceania in the period before the Austronesian expansion.7 However, Micronesia is another potential source, because M7c3c has been documented there,78 and there are historical accounts of drift migration from Micronesia to Ontong Java.79

The elevated proportion of Near Oceanian haplogroups in Santa Cruz has been reported before41,46 and remains perplexing. Santa Cruz is the first landmass encountered once crossing the border into Remote Oceania. It is known to have been settled approximately 3.2 ka ago,80 possibly directly from the Bismarck Archipelago, with evidence of contact between Santa Cruz and New Britain continuing for hundreds of years.81 Whether the peculiar haplogroup composition for this population is evidence of this trade and contact remains to be satisfactorily answered. It is the population sample with the greatest number of polymorphic sites (despite a smaller sample size than many populations) and has the highest mean pairwise difference and the greatest nucleotide diversity values (Table 1). Moreover, there are several Near Oceanian haplogroups in Santa Cruz, and each is represented by several distinct sequence types (Table S2, Figure 5). Thus, it is unlikely that the high frequency of Near Oceanian haplogroups reflects a recent bottleneck or founder event in Santa Cruz. The people of Santa Cruz speak an Austronesian language, recognized now as probably a deep branch within the Oceanic family of Austronesian,47 yet they are starkly different genetically from all other Remote Oceanian populations and from Austronesian-speaking populations in Near Oceania.

Table 1.

Diversity Statistics Based on Complete mtDNA Genome Sequences

Population N Hts Ht Diversity Polymorphic Sites π MPD
Anem 32 18 0.93 ± 0.03 99 0.0011 ± 0.0006 18.30 ± 8.33
Ata 28 8 0.75 ± 0.07 65 0.0014 ± 0.0007 22.29 ± 10.12
Nakanai 42 19 0.94 ± 0.02 100 0.0015 ± 0.0007 24.41 ± 10.94
Buin 29 23 0.98 ± 0.02 104 0.0018 ± 0.0009 29.61 ± 13.33
Buka 11 10 0.98 ± 0.05 82 0.0017 ± 0.0009 28.15 ± 13.36
Siwai 26 17 0.95 ± 0.02 93 0.0014 ± 0.0007 22.51 ± 10.24
Nagovisi 38 14 0.88 ± 0.03 53 0.0003 ± 0.0001 4.23 ± 2.15
Nasioi 41 28 0.97 ± 0.01 142 0.0017 ± 0.0008 28.04 ± 12.53
Torau 34 20 0.96 ± 0.02 124 0.0017 ± 0.0009 28.37 ± 12.72
Choiseul 33 23 0.95 ± 0.03 149 0.0012 ± 0.0006 19.86 ± 9.01
Gela 40 23 0.94 ± 0.02 68 0.0010 ± 0.0005 17.12 ± 7.78
Guadalcanal 50 42 0.99 ± 0.01 155 0.0011 ± 0.0006 18.15 ± 8.19
Isabel 52 33 0.97 ± 0.01 114 0.0010 ± 0.0005 16.97 ± 7.67
Kolombangara 18 10 0.91 ± 0.04 69 0.0007 ± 0.0004 11.18 ± 5.33
Makira 17 14 0.97 ± 0.03 58 0.0005 ± 0.0003 8.46 ± 4.12
Malaita 89 50 0.96 ± 0.01 165 0.0013 ± 0.0006 21.05 ± 9.38
Ranongga 47 23 0.94 ± 0.02 117 0.0013 ± 0.0007 22.22 ± 9.97
Russell 39 12 0.86 ± 0.04 59 0.0003 ± 0.0002 5.44 ± 2.68
Savo 40 30 0.98 ± 0.01 92 0.0010 ± 0.0005 16.36 ± 7.44
Shortlands 14 12 0.98 ± 0.03 81 0.0014 ± 0.0007 23.43 ± 10.97
Simbo 22 15 0.96 ± 0.03 48 0.0004 ± 0.0002 5.97 ± 2.96
Vella Lavella 51 25 0.96 ± 0.01 143 0.0010 ± 0.0005 16.85 ± 7.62
Santa Cruz 47 27 0.95 ± 0.02 175 0.0019 ± 0.0009 30.93 ± 13.75
Cook Islands 65 26 0.88 ± 0.03 77 0.0003 ± 0.0002 5.59 ± 2.72
Fiji 49 32 0.96 ± 0.02 134 0.0007 ± 0.0004 12.04 ± 5.54
Futuna 48 22 0.94 ± 0.02 84 0.0004 ± 0.0002 6.35 ± 3.06
Niue 21 10 0.87 ± 0.06 12 0.0002 ± 0.0001 3.50 ± 1.85
Samoa 47 34 0.95 ± 0.02 109 0.0005 ± 0.0003 8.50 ± 4.00
Tonga 52 42 0.98 ± 0.01 116 0.0005 ± 0.0002 7.82 ± 3.70
Tuvalu 50 29 0.96 ± 0.02 94 0.0005 ± 0.0002 7.64 ± 3.62
Bellona 38 10 0.85 ± 0.03 15 0.0002 ± 0.0001 3.89 ± 2.00
Ontong Java 32 12 0.89 ± 0.03 46 0.0009 ± 0.0004 14.12 ± 6.50
Rennell 43 8 0.76 ± 0.05 13 0.0002 ± 0.0001 3.62 ± 1.87
Tikopia 46 15 0.85 ± 0.04 53 0.0003 ± 0.0002 4.56 ± 2.28

To further explore these patterns on a population level, we calculated p-distance matrices between populations for some autochthonous Near Oceanian haplogroups. The heatmap contains pairwise distances for all sequences that belong to haplogroups of Near Oceanian origin and shows that, in general, sequences are most closely related to others originating from the same group (Figure 7). However, there is also a relatively high similarity of sequences from the Ata and Nakanai of New Britain to those of Santa Cruz and Remote Oceania (Figure 7). Thus, despite the lack of haplotype sharing, the lower p-distances between Santa Cruz and New Britain suggest some sort of older contact or migration (Figure 7). In addition, there is a tendency for some populations from the western Solomons (in particular Ranongga and the Shortlands) to have lower p-distances with populations from Bougainville than with populations from elsewhere in the Solomons, suggesting an east-west distinction in the Solomons in keeping with some views of the culture history of the region,45 as well as a linguistic division between Oceanic languages in the southeast versus northwest Solomon Islands.82,83 The genetic affinities between these populations are apparent here because our data set covers a wide range of Oceanian populations and also because these analyses have been restricted to the autochthonous haplogroups. When studies of population relationships were carried out averaged across all sequences from all populations (i.e., for multidimensional scaling analyses, data not shown), these signals appeared diminished in large part due to the overwhelming signal of similarity produced by the elevated frequency of haplogroup B in most populations.

Figure 7.

Figure 7

P-Distances between Samples Belonging to Haplogroups

(A) M27, M28, and M29.

(B) Haplogroup Q.

(C) Haplogroup P.

Distances were calculated with MEGA v.592 with the Tamura Nei substitution model with a gamma distribution and omitting any sites with greater than 5% missing data.

Because of the high proportion of Near Oceanian haplogroups in Santa Cruz (Figure 2) and the dearth of haplotype sharing (Figures 3 and 5) but the apparent sequence affinities (Figure 7), we considered the possibility of a pre-Austronesian settlement of Santa Cruz from New Britain. Archaeological evidence has shown that people were sailing regularly between the Bismarck Archipelago and Santa Cruz by 3.2 ka ago, “leapfrogging” over the main Solomon Islands where there is no similar indication of large-scale obsidian movement.81 To test the possibility of a pre-Austronesian settlement of Santa Cruz, we used the coalescent simulator SIMCOAL84 to simulate various scenarios in which a source population splits to form two daughter populations of equal effective population sizes followed by no additional migration events. We simulated demographic scenarios with combinations of six time points for the population split (representing the founding of the Santa Cruz population), a generation time of 28 years,85 and six effective population sizes and then, with the Arlequin package,86,87 calculated the number of segregating sites, mean pairwise distances, and ΦST and compared them to our empirically observed values. A summary of results is in Figure 8. The number of segregating sites and nucleotide diversity values for each population are informative as to the effective population size for New Britain and Santa Cruz, and the ΦST value (together with the effective population size estimate) is informative as to the time of population divergence (Figure 8). Although some of the findings hint at the possibility of an older settlement time for Santa Cruz, based on the best-fitting effective population sizes of between 1,500 and 2,500 for both New Britain and Santa Cruz, the 95% confidence intervals do not allow us to discount a settlement time of approximately 3 ka ago. Although a pre-Austronesian settlement for Santa Cruz is not ruled out by these results, neither is a pre-Austronesian settlement convincingly supported. The reason for the unusual genetic composition of Santa Cruz remains an enigma. Some studies of Y chromosome STRs24,34,41 and autosomal STRs and SNPs have already been undertaken in Oceania;37–39 however, additional studies of Y chromosome variation and whole-genome SNPs will be an important direction for future work and may help to clarify the history of Santa Cruz.

Figure 8.

Figure 8

Simulation Results for the Founding of Santa Cruz

(A and B) Segregating sites within the New Britain (A) and Santa Cruz (B) populations.

(C and D) Mean pairwise distance within the New Britain (C) and Santa Cruz (D) populations.

(E) ΦST between the New Britain and Santa Cruz populations.

In all cases the empirically observed value is indicated by the horizontal red line. Simulated demographic scenarios are grouped by the time since population split and then by simulated effective population size. Mean values for each simulation are indicated by black circles and the corresponding 95% confidence intervals by grey bars.

To conclude, we have investigated the maternal population history of 34 Oceanic populations, ranging from the Bismarck Archipelago to eastern Polynesia, with whole mitochondrial genome sequencing. Our results demonstrate the huge impact of the Austronesian expansion and its genetic legacy: haplogroup B lineages are found all across Oceania, account for 76% of all lineages, and in a very short time period have spread across the entire region. To consider this within the terms of population admixture, it seems that the Austronesians were very successfully integrated into existing Papuan societies; indeed, some populations that speak Papuan languages are among those with the highest frequencies of haplogroup B. However, by studying the non-Austronesian genetic signature, we can find evidence of population substructure and affinities between particular populations, perhaps indicative of relationships that existed before the entry of Austronesians to Near Oceania. The haplogroups of putative Near Oceanian origin found in this study appear to be quite ancient with coalescence times exceeding 60 ka ago, and we have identified new lineages that refine the current mtDNA phylogeny. Furthermore, some of these Near Oceanian haplogroups have highly regionally specific distributions, suggestive of population structure and minimal contact over a period of tens of thousands of years. We also find signals that suggest that beyond the two accepted population expansions, Near Oceania has potentially had other lesser migration events, each carrying with it specific haplogroups that appear to be localized to specific populations within Near Oceania. In addition, we do not find evidence to support a pre-Austronesian settlement of Santa Cruz, which remains a strong outlier in Remote Oceania because of its extraordinarily high frequency of autochthonous Near Oceanian haplogroups.

Acknowledgments

We thank all sample donors for contributing to this study and the numerous individuals in Bougainville who assisted with the sample collection. We thank the Sequencing Group within the Evolutionary Genetics Department for expert production of the sequences, and Gabriel Renaud and Udo Stenzel for their assistance with the HiSeq data. We thank Chiara Barbieri, Sebastian Lippold, and Sebastian Zöllner for helpful discussions and suggestions. We thank Laura Bañuelos, Torsten Blass, Alexander Hübner, and Roland Schröder for technical assistance. We thank Peter Sheppard and David Roe for sharing their knowledge of Near Oceanian archaeology. We thank Brigitte Pakendorf for helpful comments on the manuscript. This research was supported by the Max Planck Society, the Wenner-Gren Foundation for Anthropological Research, the National Science Foundation, and the National Geographic Society.

Supplemental Data

Document S1. Figures S1–S3

Table S1. Summary of Sequencing Conditions per Sample and Assigned Haplogroup per Sample

Table S2. Haplogroup Frequency and Putative Origin per Population

Document S2. Article plus Supplemental Data

Web Resources

The URLs for data presented herein are as follows:

Accession Numbers

The GenBank accession numbers for the 795 novel sequences reported in this paper are KJ154155–KJ154949.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Document S1. Figures S1–S3

Table S1. Summary of Sequencing Conditions per Sample and Assigned Haplogroup per Sample

Table S2. Haplogroup Frequency and Putative Origin per Population

Document S2. Article plus Supplemental Data