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.2017 Aug 8;114(32):E6498-E6506.
doi: 10.1073/pnas.1704906114. Epub 2017 Jul 17.

Genomic landscape of human diversity across Madagascar

Denis Pierron  1, Margit Heiske  1, Harilanto Razafindrazaka  1, Ignace Rakoto  2, Nelly Rabetokotany  2, Bodo Ravololomanga  2, Lucien M-A Rakotozafy  2, Mireille Mialy Rakotomalala  2, Michel Razafiarivony  2, Bako Rasoarifetra  2, Miakabola Andriamampianina Raharijesy  2, Lolona Razafindralambo  2, Ramilisonina  2, Fulgence Fanony  2, Sendra Lejamble  3, Olivier Thomas  3, Ahmed Mohamed Abdallah  3, Christophe Rocher  3, Amal Arachiche  3, Laure Tonaso  1, Veronica Pereda-Loth  1, Stéphanie Schiavinato  1, Nicolas Brucato  1, Francois-Xavier Ricaut  1, Pradiptajati Kusuma  1  4  5, Herawati Sudoyo  4  5, Shengyu Ni  6, Anne Boland  7, Jean-Francois Deleuze  7, Philippe Beaujard  8, Philippe Grange  9, Sander Adelaar  10, Mark Stoneking  6, Jean-Aimé Rakotoarisoa  11, Chantal Radimilahy  11, Thierry Letellier  12
Affiliations

Genomic landscape of human diversity across Madagascar

Denis Pierron et al. Proc Natl Acad Sci U S A..

Abstract

Although situated ∼400 km from the east coast of Africa, Madagascar exhibits cultural, linguistic, and genetic traits from both Southeast Asia and Eastern Africa. The settlement history remains contentious; we therefore used a grid-based approach to sample at high resolution the genomic diversity (including maternal lineages, paternal lineages, and genome-wide data) across 257 villages and 2,704 Malagasy individuals. We find a common Bantu and Austronesian descent for all Malagasy individuals with a limited paternal contribution from Europe and the Middle East. Admixture and demographic growth happened recently, suggesting a rapid settlement of Madagascar during the last millennium. However, the distribution of African and Asian ancestry across the island reveals that the admixture was sex biased and happened heterogeneously across Madagascar, suggesting independent colonization of Madagascar from Africa and Asia rather than settlement by an already admixed population. In addition, there are geographic influences on the present genomic diversity, independent of the admixture, showing that a few centuries is sufficient to produce detectable genetic structure in human populations.

Keywords: Indian Ocean; Malagasy origins; genetics; genome-wide data; proto-globalization.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Geographic distribution of Asian and African genetic ancestry across Madagascar. (A) Sampling grid across Madagascar: Three to four villages were sampled in each of 82 spots that are each 50 km in diameter. Image courtesy of Google Earth ©2016 TerraMetrics. (B) Exponential kriging interpolation of the ancestry across the Madagascar landscape based on the frequency of mtDNA lineages and Y chromosome lineages in each village and the average of Admixture (k = 3) analysis for genome-wide data based on the high-density panel.
Fig. 2.
Fig. 2.
Uniparental lineages. (A) Distribution of mtDNA lineages according to continental origin. Asian lineages are in blue, African lineages are in red, and M23 (unknown origin) is in purple. (B) Distribution of Y chromosome lineages according to continental origin. Asian lineages are in blue, African lineages are in red, and Eurasian lineages are in green.
Fig. 3.
Fig. 3.
Genome-wide analysis: Admixture plots based on a worldwide population panel (Dataset S1: low density) for k = 9. (A) Boxplot of the distribution of shared IBD segments between any Malagasy and any individual from the reference population in high-density panel 2 from Eurasia in blue (B) or Africa in red (C).
Fig. 4.
Fig. 4.
Genetic groups. (A) Geographic distribution of genetic groups in Madagascar. Each dot represents a village, and the intensity of the color corresponds to the relative presence of individuals of each group. (B) Kriging model of the spatial distribution of genetic groups based on the frequency of each group in each sampled village. (C) Superposition of all genetic groups distributions (based on kriging model). Colors were assigned according to the dominant genetic cluster present in a given area. Plain colors were used for locations where the majority of people (>50%) belong to this cluster.
Fig. 5.
Fig. 5.
Demographic model of the settlement of Madagascar. The plots in the three panels share the samex axis. (A) Timeline of the point and smoothed estimation of the average number of common ancestors shared between Malagasy and Borneo (in blue) and Malagasy and Bantu (in red) populations, as estimated by shared IBD segments from genome-wide data. (B) Estimation of percentage and date of admixture for each genetic group of Madagascar. The straight line represents the uncertainty (±1 SD) of admixture dates estimated from GLOBEtrotter. Some populations overlap. (More detailed results are provided in Fig. S7B). (C) Estimation of changes in the effective population size across time for selected genetic groups and for the whole Malagasy population, estimated by shared IBD genome-wide.
Fig. 6.
Fig. 6.
Overview of the inferred history of Madagascar. Descriptions and dates are given inA–D.
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