Harilanto Razafindrazaka

A recent bottleneck of Y chromosome diversity coincides with a global change in culture

It is commonly thought that human genetic diversity in non-African populations was shaped primarily by an out-of-Africa dispersal 50-100 thousand yr ago (kya). Here, we present a study of 456 geographically diverse high-coverage Y chromosome sequences, including 299 newly reported samples. Applying ancient DNA calibration, we date the Y-chromosomal most recent common ancestor (MRCA) in Africa at 254 (95% CI 192-307) kya and detect a cluster of major non-African founder haplogroups in a narrow time interval at 47-52 kya, consistent with a rapid initial colonization model of Eurasia and Oceania after the out-of-Africa bottleneck. In contrast to demographic reconstructions based on mtDNA, we infer a second strong bottleneck in Y-chromosome lineages dating to the last 10 ky. We hypothesize that this bottleneck is caused by cultural changes affecting variance of reproductive success among males.

Genome-wide evidence of Austronesian–Bantu admixture and cultural reversion in a hunter-gatherer group of Madagascar

Significance The Mikea are the last known Malagasy population reported to be still practicing a hunter-gatherer lifestyle. Earlier writers thought the Mikea were descended from ancient forager groups who have maintained their way of life up to the present. However, our analyses show that the Mikea are not a remnant population and, to the contrary, derived from a recent admixture of two agriculturalist populations: the Bantu (from Africa) and the Austronesian (from east-Asia). Thus, it is probable that the Mikea have adopted their hunter-gatherer way of life through a recent cultural reversion. Linguistic and cultural evidence suggest that Madagascar was the final point of two major dispersals of Austronesian- and Bantu-speaking populations. Today, the Mikea are described as the last-known Malagasy population reported to be still practicing a hunter-gatherer lifestyle. It is unclear, however, whether the Mikea descend from a remnant population that existed before the arrival of Austronesian and Bantu agriculturalists or whether it is only their lifestyle that separates them from the other contemporary populations of South Madagascar. To address these questions we have performed a genome-wide analysis of >700,000 SNP markers on 21 Mikea, 24 Vezo, and 24 Temoro individuals, together with 50 individuals from Bajo and Lebbo populations from Indonesia. Our analyses of these data in the context of data available from other Southeast Asian and African populations reveal that all three Malagasy populations are derived from the same admixture event involving Austronesian and Bantu sources. In contrast to the fact that most of the vocabulary of the Malagasy speakers is derived from the Barito group of the Austronesian language family, we observe that only one-third of their genetic ancestry is related to the populations of the Java-Kalimantan-Sulawesi area. Because no additional ancestry components distinctive for the Mikea were found, it is likely that they have adopted their hunter-gatherer way of life through cultural reversion, and selection signals suggest a genetic adaptation to their new lifestyle.

Complete mitochondrial DNA sequences provide new insights into the Polynesian motif and the peopling of Madagascar

More than a decade of mitochondrial DNA (mtDNA) studies have given the ‘Polynesian motif’ renowned status as a marker for tracing the late-Holocene expansion of Austronesian speaking populations. Despite considerable research on the Polynesian motif in Oceania, there has been little equivalent work on the western edge of its expansion – leaving major issues unresolved regarding the motifs evolutionary history. This has also led to considerable uncertainty regarding the settlement of Madagascar. In this study, we assess mtDNA variation in 266 individuals from three Malagasy ethnic groups: the Mikea, Vezo, and Merina. Complete mtDNA genome sequencing reveals a new variant of the Polynesian motif in Madagascar; two coding region mutations define a Malagasy-specific sub-branch. This newly defined ‘Malagasy motif’ occurs at high frequency in all three ethnic groups (13–50%), and its phylogenetic position, geographic distribution, and estimated age all support a recent origin, but without conclusively identifying a specific source region. Nevertheless, the haplotypes limited diversity, similar to those of other mtDNA haplogroups found in our Malagasy groups, best supports a small number of initial settlers arriving to Madagascar through the same migratory process. Finally, the discovery of this lineage provides a set of new polymorphic positions to help localize the Austronesian ancestors of the Malagasy, as well as uncover the origin and evolution of the Polynesian motif itself.

A new deep branch of eurasian mtDNA macrohaplogroup M reveals additional complexity regarding the settlement of Madagascar

BackgroundCurrent models propose that mitochondrial DNA macrohaplogroups M and N evolved from haplogroup L3 soon after modern humans left Africa. Increasingly, however, analysis of isolated populations is filling in the details of, and in some cases challenging, aspects of this general model.ResultsHere, we present the first comprehensive study of three such isolated populations from Madagascar: the Mikea hunter-gatherers, the neighbouring Vezo fishermen, and the Merina central highlanders (n = 266). Complete mitochondrial DNA genome sequences reveal several unresolved lineages, and a new, deep branch of the out-of-Africa founder clade M has been identified. This new haplogroup, M23, has a limited global distribution, and is restricted to Madagascar and a limited range of African and Southwest Asian groups.ConclusionsThe geographic distribution, phylogenetic placement and molecular age of M23 suggest that the colonization of Madagascar was more complex than previously thought.

Mitochondrial DNA and the Y chromosome suggest the settlement of Madagascar by Indonesian sea nomad populations

BackgroundLinguistic, cultural and genetic characteristics of the Malagasy suggest that both Africans and Island Southeast Asians were involved in the colonization of Madagascar. Populations from the Indonesian archipelago played an especially important role because linguistic evidence suggests that the Malagasy language branches from the Southeast Barito language family of southern Borneo, Indonesia, with the closest language spoken today by the Ma’anyan. To test for a genetic link between Malagasy and these linguistically related Indonesian populations, we studied the Ma’anyan and other Indonesian ethnic groups (including the sea nomad Bajo) that, from their historical and linguistic contexts, may be modern descendants of the populations that helped enact the settlement of Madagascar.ResultA combination of phylogeographic analysis of genetic distances, haplotype comparisons and inference of parental populations by linear optimization, using both maternal and paternal DNA lineages, suggests that Malagasy derive from multiple regional sources in Indonesia, with a focus on eastern Borneo, southern Sulawesi and the Lesser Sunda islands.ConclusionSettlement may have been mediated by ancient sea nomad movements because the linguistically closest population, Ma’anyan, has only subtle genetic connections to Malagasy, whereas genetic links with other sea nomads are more strongly supported. Our data hint at a more complex scenario for the Indonesian settlement of Madagascar than has previously been recognized.

Contrasting Linguistic and Genetic Origins of the Asian Source Populations of Malagasy

The Austronesian expansion, one of the last major human migrations, influenced regions as distant as tropical Asia, Remote Oceania and Madagascar, off the east coast of Africa. The identity of the Asian groups that settled Madagascar is particularly mysterious. While language connects Madagascar to the Ma’anyan of southern Borneo, haploid genetic data are more ambiguous. Here, we screened genome-wide diversity in 211 individuals from the Ma’anyan and surrounding groups in southern Borneo. Surprisingly, the Ma’anyan are characterized by a distinct, high frequency genomic component that is not found in Malagasy. This novel genetic layer occurs at low levels across Island Southeast Asia and hints at a more complex model for the Austronesian expansion in this region. In contrast, Malagasy show genomic links to a range of Island Southeast Asian groups, particularly from southern Borneo, but do not have a clear genetic connection with the Ma’anyan despite the obvious linguistic association.

Genomic landscape of human diversity across Madagascar

Significance The origins of the Malagasy raise questions about ancient connections between continents; moreover, because ancestors are fundamental to Malagasy society, Malagasy origins is also a heated topic around the country, with numerous proposed hypotheses. This study provides a comprehensive view of genomic diversity (including maternal lineages, paternal lineages, and genome-wide data) based on a sampling of 257 villages across Madagascar. The observed spatial patterns lead to a scenario of a recent and sex-biased admixture between Bantu and Austronesian ancestors across the island. Moreover, we find geographical influences creating subtle signals of genetic structure that are independent of the Bantu/Austronesian admixture, suggesting that recent history has a role in the genomic diversity of the Malagasy. 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.

Genetic Admixture and Flavor Preferences: Androstenone Sensitivity in Malagasy Populations

ABSTRACT The genetic basis of androstenone anosmia has been well studied due to androstenones putative role as a human sex pheromone and its presence in pork meat. Polymorphisms have been identified on the olfactory receptor gene OR7D4, which significantly affect perception of androstenone pleasantness and intensity in several Western populations. This study aims to investigate androstenone sensitivity and the influence of OR7D4 polymorphisms in non-Western populations. Androstenone perception was tested in 132 individuals from Madagascar using a double three-alternative choice test with two concentrations of androstenone (0.17 and 1.7 µg/ml). We found that Malagasy populations described this molecule in a similar way to European populations, and 21% of the sample was not able to smell androstenone. In contrast to previous studies, there was no significant evidence of the influence of rs61729907: C>T (R88W) and rs5020278: C>T polymorphisms (T133M) on androstenone sensitivity in Malagasy populations. We found, however, a significant effect of the polymorphism rs61732668 (P79L) and a significant difference in androstenone perception between populations in different locations across Madagascar. This study indicates the existence of population-specific factors in androstenone sensitivity, suggesting that population history has a role in shaping an individuals smell and flavor preferences and food preferences in general.

Strong selection during the last millennium for African ancestry in the admixed population of Madagascar

While admixed populations offer a unique opportunity to detect selection, the admixture in most of the studied populations occurred too recently to produce conclusive signals. By contrast, Malagasy populations originate from admixture between Asian and African populations that occurred ~27 generations ago, providing power to detect selection. We analyze local ancestry across the genomes of 700 Malagasy and identify a strong signal of recent positive selection, with an estimated selection coefficient >0.2. The selection is for African ancestry and affects 25% of chromosome 1, including the Duffy blood group gene. The null allele at this gene provides resistance to Plasmodium vivax malaria, and previous studies have suggested positive selection for this allele in the Malagasy population. This selection event also influences numerous other genes implicated in immunity, cardiovascular diseases, and asthma and decreases the Asian ancestry genome-wide by 10%, illustrating the role played by selection in recent human history.The population of Madagascar arose from admixture of Austronesian and Bantu genetic backgrounds. Analyzing local ancestry in genomes of 700 Malagasy, Pierron et al. identify signals of recent positive selection for African ancestry in a region on chromosome 1 with implications for physiology and disease risk.

Human testis-specific genes are under relaxed negative selection

Recent studies have suggested that selective forces and constraints acting on genes varied during human evolution depending on the organ in which they are expressed. To gain insight into the evolution of organ determined negative selection forces, we compared the non-synonymous SNP diversity of genes expressed in different organs. Based on a HAPMAP dataset, we determined for each SNP its frequency in 11 human populations and, in each case, predicted whether or not the change it produces is deleterious. We have shown that, for all organs under study, SNPs predicted to be deleterious are present at a significantly lower frequency than SNPs predicted to be tolerated. However, testis-specific genes contain a higher proportion of deleterious SNPs than other organs. This study shows that negative selection is acting on the whole human genome, but that the action of negative selection is relaxed on testis-specific genes. This result adds to and expands the hypothesis of a recent evolutionary change in the human male reproductive system and its behavior.