Evolutionary history of modern Samoans

Abstract

Archaeological studies estimate the initial settlement of Samoa at 2,750 to 2,880 y ago and identify only limited settlement and human modification to the landscape until about 1,000 to 1,500 y ago. At this point, a complex history of migration is thought to have begun with the arrival of people sharing ancestry with Near Oceanic groups (i.e., Austronesian-speaking and Papuan-speaking groups), and was then followed by the arrival of non-Oceanic groups during European colonialism. However, the specifics of this peopling are not entirely clear from the archaeological and anthropological records, and is therefore a focus of continued debate. To shed additional light on the Samoan population history that this peopling reflects, we employ a population genetic approach to analyze 1,197 Samoan high-coverage whole genomes. We identify population splits between the major Samoan islands and detect asymmetrical gene flow to the capital city. We also find an extreme bottleneck until about 1,000 y ago, which is followed by distinct expansions across the islands and subsequent bottlenecks consistent with European colonization. These results provide for an increased understanding of Samoan population history and the dynamics that inform it, and also demonstrate how rapid demographic processes can shape modern genomes.

Keywords: Austronesian; Oceania; fine-scale population structure; genetically understudied populations; rare variants.

Fig. 1.

Increased admixture in urban regions. (A) Global ancestry proportions estimated by ADMIXTURE (34, 35) analysis for each Samoan individual. (B) Source of African, East Asian, and European admixture. Proportion of the AUA, NWU, and ROU admixed individuals’ genomes attributed to the different source populations as determined by ChromoPainter (36) and Globetrotter (37). Our interpretation of each ancestry cluster is included in Lower Right.

Fig. 2.

Denisovan ancestry is correlated to Papuan ancestry. The x axis represents f4 ratio-estimated Papuan ancestry proportions, and the y axis represents the D-statistic test for Denisovan admixture in Samoan and other modern Austronesian individuals. Samoans are represented by black points, and other Austronesian individuals are represented by blue points. Polynesian and Polynesian outlier individuals are represented by red squares.

Fig. 3.

Samoan population structure is strongly influenced by urbanization. Map of Samoan census regions, with arrows indicating the between-region rare variant sharing and the white numbers representing within-region rare variant sharing. Red arrows represent the following comparisons with P < 0.05: SAV shares more with AUA than with ROU (P = 0.044), ROU shares more with NWU than with SAV (P = 0.043), ROU shares more with AUA than with SAV (P = 0.001), and ROU shares more with AUA than with NWU (P = 0.048) (SI Appendix, Fig. S8). Shaded geographical regions represent their corresponding census regions (SI Appendix, Fig. S2). Each value represents the average number of rare variants shared between all pairs of individuals, and all values were multiplied by 10,000 for visualization.

Fig. 4.

Samoan population history. The colored lines represent the N_e history from IBDNe (43) of SAV and Upolu. The lighter-shaded polygons around the lines represent the 95% CI. All N_e values are plotted on a log₁₀ scale. The icons below the N_e results represent a summary of known events in Samoan history from archaeological and historical records, assuming a 30-y human generation time (8). European sustained contact, rise of Samoan chiefdoms, Samoan interarchipelago voyages increase, pottery disappears, potential migration into Samoa, sparse peopling of all Samoan islands, and initial settlement of Upolu are shown from left to right. The icons are derived from Samoan and Polynesian archaeology, material culture, and ethnohistoric accounts. The Lapita pottery sherd is copied from a similar sherd found at the Mulifanua archaeological site (14). The triangular shape of the human icons is modeled after rock art pictographs in Polynesia (e.g., Tonga and Hawaii), although no anthropomorphic rock art is known for Samoa. The Samoan chief icon holds a to’oto’o, the staff associated with tulafale or orator-chiefs. The Tongan maritime chiefdom icon depicts some items exchanged between Samoa, Tonga, and Fiji: basalt for adzes and other tools, bird feathers (particularly red colored), and timber and mats for canoe building (SI Appendix, Table S5).