History Shaped the Geographic Distribution of Genomic Admixture on the Island of Puerto Rico

Marc Via,Shweta Choudhry,Juan Carlos Martínez-Cruzado,Neil Risch,Lindsey A Roth,Taras K Oleksyk,Christopher R Gignoux,Elad Ziv,Esteban González Burchard,Joshua Galanter,Laura Fejerman,Gladys Toro-Labrador,Jorge Viera-Vera,Kenneth Beckman

doi:10.1371/journal.pone.0016513

Abstract

Contemporary genetic variation among Latin Americans human groups reflects population migrations shaped by complex historical, social and economic factors. Consequently, admixture patterns may vary by geographic regions ranging from countries to neighborhoods. We examined the geographic variation of admixture across the island of Puerto Rico and the degree to which it could be explained by historic and social events. We analyzed a census-based sample of 642 Puerto Rican individuals that were genotyped for 93 ancestry informative markers (AIMs) to estimate African, European and Native American ancestry. Socioeconomic status (SES) data and geographic location were obtained for each individual. There was significant geographic variation of ancestry across the island. In particular, African ancestry demonstrated a decreasing East to West gradient that was partially explained by historical factors linked to the colonial sugar plantation system. SES also demonstrated a parallel decreasing cline from East to West. However, at a local level, SES and African ancestry were negatively correlated. European ancestry was strongly negatively correlated with African ancestry and therefore showed patterns complementary to African ancestry. By contrast, Native American ancestry showed little variation across the island and across individuals and appears to have played little social role historically. The observed geographic distributions of SES and genetic variation relate to historical social events and mating patterns, and have substantial implications for the design of studies in the recently admixed Puerto Rican population. More generally, our results demonstrate the importance of incorporating social and geographic data with genetics when studying contemporary admixed populations.

Highlights

Worldwide patterns of modern human genetic variation have been shaped by a long history of demographic events, such as migrations or changes in population size
The differences in genetic admixture among individuals within a population result from assortative mating based on socioeconomic status and skin color [12], the consequences of a social hierarchy established by the colonial powers
Mean admixture proportions showed significant differences both at regional and municipal levels (p,1024 for European and African, p,0.01 for Native American, Table 1 and Figure 1C). These geographic differences were driven by the variation in African ancestry: 23.9% of variance in African ancestry was between regions versus within regions, compared to 14.6 and 3.1% for European and Native American contributions, respectively (ANOVA p,0.001 for all comparisons)

Summary

Introduction

Worldwide patterns of modern human genetic variation have been shaped by a long history of demographic events, such as migrations or changes in population size. Geographic components have been included in the study of the original settlement of human populations or in the detection of ancient demographic events, such as Neolithic expansions [5], and population structure, even at fine scales [6,7,8]. The differences in genetic admixture among individuals within a population result from assortative mating based on socioeconomic status and skin color [12], the consequences of a social hierarchy established by the colonial powers. Despite this heterogeneity, most research efforts on admixture have analyzed populations as a whole while largely ignoring the spatial and social factors that have shaped contemporary admixture patterns [13]

Methods

Results

Conclusion