The Genetic Legacy of the Indian Ocean Slave Trade: Recent Admixture and Post-admixture Selection in the Makranis of Pakistan

Abstract

From the eighth century onward, the Indian Ocean was the scene of extensive trade of sub-Saharan African slaves via sea routes controlled by Muslim Arab and Swahili traders. Several populations in present-day Pakistan and India are thought to be the descendants of such slaves, yet their history of admixture and natural selection remains largely undefined. Here, we studied the genome-wide diversity of the African-descent Makranis, who reside on the Arabian Sea coast of Pakistan, as well that of four neighboring Pakistani populations, to investigate the genetic legacy, population dynamics, and tempo of the Indian Ocean slave trade. We show that the Makranis are the result of an admixture event between local Baluch tribes and Bantu-speaking populations from eastern or southeastern Africa; we dated this event to ∼300 years ago during the Omani Empire domination. Levels of parental relatedness, measured through runs of homozygosity, were found to be similar across Pakistani populations, suggesting that the Makranis rapidly adopted the traditional practice of endogamous marriages. Finally, we searched for signatures of post-admixture selection at traits evolving under positive selection, including skin color, lactase persistence, and resistance to malaria. We demonstrate that the African-specific Duffy-null blood group-believed to confer resistance against Plasmodium vivax infection-was recently introduced to Pakistan through the slave trade and evolved adaptively in this P. vivax malaria-endemic region. Our study reconstructs the genetic and adaptive history of a neglected episode of the African Diaspora and illustrates the impact of recent admixture on the diffusion of adaptive traits across human populations.

Multiple selective sweeps of ancient polymorphisms in and around LTα located in the MHC class III region on chromosome 6

“…However, further analysis of a larger set of populations will be needed to distinguish: 1) whether the above extended LD in African Americans was due to strong selection on pre-existing common variation at rs 73396237 that became beneficial in novel environments, or 2) a selective event had occurred first in the ancestors of Europeans who then admixed with the West African ancestors of present-day African Americans. Interestingly, recent studies have reported instances of populations acquiring selected alleles through past admixture [66–68]. Thus, it is highly conceivable that a selected allele could have been introduced into African Americans through admixture between African and non-African parental populations.…”

Distribution of local ancestry and evidence of adaptation in admixed populations

“…Finally, we suggest that the European NI haplotypes on chromosome 8p23.1 were disadvantaged in favour of the Native-American NI haplotypes in the context of new heterogeneous genomic diversity landscapes and changing environmental conditions which arose after post-Columbian admixture events in the Americas, in Brazil and Mexico. Selection after admixture has been described in archaic admixture between modern humans and Neanderthals 51,52 , but it is not entirely understood in more recent admixture events 53 .…”

Human Immunology through the Lens of Evolutionary Genetics

“…Since the admixture event, the Fulani have retained high levels of African ancestry for the ACKR1 (also known as DARC) gene, the null allele of which confers resistance to Plasmodium vivax malaria, and high levels of Eurasian ancestry at the LCT locus, which contains a lactase persistence allele facilitating the digestion of milk in adults (Busby et al, 2017). The highly adaptive nature of the Duffy null allele and its rapid spread across populations via admixture is supported by other studies reporting high African ancestry in admixed populations from Pakistan and Madagascar, where vivax malaria is endemic (Hodgson et al, 2014;Laso-Jadart et al, 2017;Pierron et al, 2018). These studies provide proof of concept that host adaptation to pathogens can be accelerated by gene flow, but they are generally restricted to a few cases in populations of African descent.…”