European Roma groups show complex West Eurasian admixture footprints and a common South Asian genetic origin

Author summary Human demographic processes and admixture events leave traceable footprints in the genomes of the populations and they can modulate the genetic architecture of complex diseases. Here, we aim to study the Roma people, an admixed population with a particular demographic history recognized as the largest ethnic minority in Europe. Previous studies suggest that they originated in South Asia 1,500 years ago and followed a diaspora towards Europe with extensive admixture with non-Roma West Eurasian groups. However, the genetic components of the Roma have not been deeply characterized. Our study reveals a common South Asian origin of all European Roma, closely related to a Punjabi group from Northwestern India. Through fine-scale haplotype-based methods, we describe a complex West Eurasian genetic component in the Roma groups, identifying a common Balkan ancestry and country-specific admixture footprints consistent with the dispersion through Europe. Our findings provide new insights into the demographic history and recent admixture events that have shaped the genetic composition of European Roma groups and could enable a better genetic characterization of complex disease in this population. The Roma population is the largest transnational ethnic minority in Europe, characterized by a linguistic, cultural and historical heterogeneity. Comparative linguistics and genetic studies have placed the origin of European Roma in the Northwest of India. After their migration across Persia, they entered into the Balkan Peninsula, from where they spread into Europe, arriving in the Iberian Peninsula in the 15th century. Their particular demographic history has genetic implications linked to rare and common diseases. However, the South Asian source of the proto-Roma remains still untargeted and the West Eurasian Roma component has not been yet deeply characterized. Here, in order to describe both the South Asian and West Eurasian ancestries, we analyze previously published genome-wide data of 152 European Roma and 34 new Iberian Roma samples at a fine-scale and haplotype-based level, with special focus on the Iberian Roma genetic substructure. Our results suggest that the putative origin of the proto-Roma involves a Punjabi group with low levels of West Eurasian ancestry. In addition, we have identified a complex West Eurasian component (around 65%) in the Roma, as a result of the admixture events occurred with non-proto-Roma populations between 1270-1580. Particularly, we have detected the Balkan genetic footprint in all European Roma, and the Baltic and Iberian components in the Northern and Western Roma groups, respectively. Finally, our results show genetic substructure within the Iberian Roma, with different levels of West Eurasian admixture, as a result of the complex historical events occurred in the Peninsula.This work was supported by the Spanish Ministry of Economy and Competitiveness (grant number CGL2016-75389-P and "Unidad Maria de Maeztu" (MDM-2014-0370) to DC and FC; and Agencia de Gestio d'Ajuts Universitaris i de la Recerca (Generalitat de Catalunya, grant 2017SGR00702). NF-P was supported by a FPU17/03501 fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript