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Reconstructing the Population Genetic History of the Caribbean

Author

Listed:
  • Andrés Moreno-Estrada
  • Simon Gravel
  • Fouad Zakharia
  • Jacob L McCauley
  • Jake K Byrnes
  • Christopher R Gignoux
  • Patricia A Ortiz-Tello
  • Ricardo J Martínez
  • Dale J Hedges
  • Richard W Morris
  • Celeste Eng
  • Karla Sandoval
  • Suehelay Acevedo-Acevedo
  • Paul J Norman
  • Zulay Layrisse
  • Peter Parham
  • Juan Carlos Martínez-Cruzado
  • Esteban González Burchard
  • Michael L Cuccaro
  • Eden R Martin
  • Carlos D Bustamante

Abstract

The Caribbean basin is home to some of the most complex interactions in recent history among previously diverged human populations. Here, we investigate the population genetic history of this region by characterizing patterns of genome-wide variation among 330 individuals from three of the Greater Antilles (Cuba, Puerto Rico, Hispaniola), two mainland (Honduras, Colombia), and three Native South American (Yukpa, Bari, and Warao) populations. We combine these data with a unique database of genomic variation in over 3,000 individuals from diverse European, African, and Native American populations. We use local ancestry inference and tract length distributions to test different demographic scenarios for the pre- and post-colonial history of the region. We develop a novel ancestry-specific PCA (ASPCA) method to reconstruct the sub-continental origin of Native American, European, and African haplotypes from admixed genomes. We find that the most likely source of the indigenous ancestry in Caribbean islanders is a Native South American component shared among inland Amazonian tribes, Central America, and the Yucatan peninsula, suggesting extensive gene flow across the Caribbean in pre-Columbian times. We find evidence of two pulses of African migration. The first pulse—which today is reflected by shorter, older ancestry tracts—consists of a genetic component more similar to coastal West African regions involved in early stages of the trans-Atlantic slave trade. The second pulse—reflected by longer, younger tracts—is more similar to present-day West-Central African populations, supporting historical records of later transatlantic deportation. Surprisingly, we also identify a Latino-specific European component that has significantly diverged from its parental Iberian source populations, presumably as a result of small European founder population size. We demonstrate that the ancestral components in admixed genomes can be traced back to distinct sub-continental source populations with far greater resolution than previously thought, even when limited pre-Columbian Caribbean haplotypes have survived.Author Summary: Latinos are often regarded as a single heterogeneous group, whose complex variation is not fully appreciated in several social, demographic, and biomedical contexts. By making use of genomic data, we characterize ancestral components of Caribbean populations on a sub-continental level and unveil fine-scale patterns of population structure distinguishing insular from mainland Caribbean populations as well as from other Hispanic/Latino groups. We provide genetic evidence for an inland South American origin of the Native American component in island populations and for extensive pre-Columbian gene flow across the Caribbean basin. The Caribbean-derived European component shows significant differentiation from parental Iberian populations, presumably as a result of founder effects during the colonization of the New World. Based on demographic models, we reconstruct the complex population history of the Caribbean since the onset of continental admixture. We find that insular populations are best modeled as mixtures absorbing two pulses of African migrants, coinciding with the early and maximum activity stages of the transatlantic slave trade. These two pulses appear to have originated in different regions within West Africa, imprinting two distinguishable signatures on present-day Afro-Caribbean genomes and shedding light on the genetic impact of the slave trade in the Caribbean.

Suggested Citation

  • Andrés Moreno-Estrada & Simon Gravel & Fouad Zakharia & Jacob L McCauley & Jake K Byrnes & Christopher R Gignoux & Patricia A Ortiz-Tello & Ricardo J Martínez & Dale J Hedges & Richard W Morris & Cele, 2013. "Reconstructing the Population Genetic History of the Caribbean," PLOS Genetics, Public Library of Science, vol. 9(11), pages 1-19, November.
  • Handle: RePEc:plo:pgen00:1003925
    DOI: 10.1371/journal.pgen.1003925
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    References listed on IDEAS

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    1. Carlos D. Bustamante & Francisco M. De La Vega & Esteban G. Burchard, 2011. "Genomics for the world," Nature, Nature, vol. 475(7355), pages 163-165, July.
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    1. Mateus H. Gouveia & Amy R. Bentley & Thiago P. Leal & Eduardo Tarazona-Santos & Carlos D. Bustamante & Adebowale A. Adeyemo & Charles N. Rotimi & Daniel Shriner, 2023. "Unappreciated subcontinental admixture in Europeans and European Americans and implications for genetic epidemiology studies," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    2. Julian R Homburger & Andrés Moreno-Estrada & Christopher R Gignoux & Dominic Nelson & Elena Sanchez & Patricia Ortiz-Tello & Bernardo A Pons-Estel & Eduardo Acevedo-Vasquez & Pedro Miranda & Carl D La, 2015. "Genomic Insights into the Ancestry and Demographic History of South America," PLOS Genetics, Public Library of Science, vol. 11(12), pages 1-26, December.
    3. Buzbas, Erkan Ozge & Verdu, Paul, 2018. "Inference on admixture fractions in a mechanistic model of recurrent admixture," Theoretical Population Biology, Elsevier, vol. 122(C), pages 149-157.
    4. Douglas J. Kennett & Mark Lipson & Keith M. Prufer & David Mora-Marín & Richard J. George & Nadin Rohland & Mark Robinson & Willa R. Trask & Heather H. J. Edgar & Ethan C. Hill & Erin E. Ray & Paige L, 2022. "South-to-north migration preceded the advent of intensive farming in the Maya region," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    5. Rozaimi Mohamad Razali & Juan Rodriguez-Flores & Mohammadmersad Ghorbani & Haroon Naeem & Waleed Aamer & Elbay Aliyev & Ali Jubran & Andrew G. Clark & Khalid A. Fakhro & Younes Mokrab, 2021. "Thousands of Qatari genomes inform human migration history and improve imputation of Arab haplotypes," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    6. Angela Andaleon & Lauren S Mogil & Heather E Wheeler, 2019. "Genetically regulated gene expression underlies lipid traits in Hispanic cohorts," PLOS ONE, Public Library of Science, vol. 14(8), pages 1-21, August.

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