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A genetic history of the pre-contact Caribbean

Abstract

Humans settled the Caribbean about 6,000 years ago, and ceramic use and intensified agriculture mark a shift from the Archaic to the Ceramic Age at around 2,500 years ago1,2,3. Here we report genome-wide data from 174 ancient individuals from The Bahamas, Haiti and the Dominican Republic (collectively, Hispaniola), Puerto Rico, Curaçao and Venezuela, which we co-analysed with 89 previously published ancient individuals. Stone-tool-using Caribbean people, who first entered the Caribbean during the Archaic Age, derive from a deeply divergent population that is closest to Central and northern South American individuals; contrary to previous work4, we find no support for ancestry contributed by a population related to North American individuals. Archaic-related lineages were >98% replaced by a genetically homogeneous ceramic-using population related to speakers of languages in the Arawak family from northeast South America; these people moved through the Lesser Antilles and into the Greater Antilles at least 1,700 years ago, introducing ancestry that is still present. Ancient Caribbean people avoided close kin unions despite limited mate pools that reflect small effective population sizes, which we estimate to be a minimum of 500–1,500 and a maximum of 1,530–8,150 individuals on the combined islands of Puerto Rico and Hispaniola in the dozens of generations before the individuals who we analysed lived. Census sizes are unlikely to be more than tenfold larger than effective population sizes, so previous pan-Caribbean estimates of hundreds of thousands of people are too large5,6. Confirming a small and interconnected Ceramic Age population7, we detect 19 pairs of cross-island cousins, close relatives buried around 75 km apart in Hispaniola and low genetic differentiation across islands. Genetic continuity across transitions in pottery styles reveals that cultural changes during the Ceramic Age were not driven by migration of genetically differentiated groups from the mainland, but instead reflected interactions within an interconnected Caribbean world1,8.

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Fig. 1: Geography and genetic structure.
Fig. 2: Genetic affinities of ancient Caribbean people.
Fig. 3: Estimates of Ne from shared haplotypes.

Data availability

The aligned sequences are available through the European Nucleotide Archive under accession number PRJEB38555. Genotype data used in analysis are available at https://reich.hms.harvard.edu/datasets. Any other relevant data are available from the corresponding authors upon reasonable request.

Code availability

The custom code used in this study is available from https://github.com/DReichLab/ADNA-Tools.

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Acknowledgements

We acknowledge the ancient people who were the source of the skeletal material analysed in this study, as well as modern people from the Caribbean who have a genetic or cultural legacy from some of the ancient populations we analysed. This work was supported by a grant from the National Geographic Society to M. Pateman to facilitate analysis of skeletal material from The Bahamas and by a grant from the Italian ‘Ministry of Foreign Affairs and International Cooperation’ (Italian archaeological, anthropological and ethnological missions abroad, DGPSP Ufficio VI). D.R. was funded by NSF HOMINID grant BCS-1032255, NIH (NIGMS) grant GM100233, the Paul Allen Foundation, the John Templeton Foundation grant 61220 and the Howard Hughes Medical Institute. We thank J. Avilés, J. Acayaguana Delvalle, J. Estevez, D. T. Golding Frankson, J. Gregory, L. A. Guitar, L. Kelly, G. A. Lopez Castellano, K. R. Nibonri and O. Patterson for comments on early versions of this manuscript and discussions that improved the presentation of this work; V. A. Forbes-Pateman and N. Albury for their assistance compiling descriptions for archaeological sites in The Bahamas; E. Harney, R. Maier and N. Nakatsuka for help with data processing; and M. Chintalapati, P. Moorjani and N. Patterson for advice on analysis. We dedicate this article to the memory of F. Luna Calderon, who would have been a co-author had he not passed away in the course of the work for this study.

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Authors and Affiliations

Authors

Contributions

W.F.K., A. Coppa, M. Lipson, R.P. and D.R. supervised the study. J.S., O.C., C.A.A., E.V.C., R.C., A. Cucina, F.G., C.K., F.L.P., M. Lucci, M.V.M., C.T.M., C.M., I.P., M.P., T.M.S., C.G.S. and M.V. provided skeletal materials and/or assembled and interpreted archaeological and anthropological information. C.A.A., E.V.C., C.K., M.V.M., C.T.M., C.M., I.P., M.P., T.M.S. and C.G.S. contributed local perspectives to the interpretation and contextualization of new genetic data. B.M.-T. provided data from present-day populations. N.R., M.M., S.M., N.A., R.B., G.B., N.B., O.C., K.C., F.C., L.D., K.S.D.C., S.F., A.M.L., K.M., J.O., K.T.Ö., C.S., R.S., K.S. and F.Z. performed ancient DNA laboratory and/or data-processing work. B.J.C., R.J.G., L.E., F.M., W.C.M., F.T. and D.J.K. performed radiocarbon analysis and stable isotope work; D.J.K. supervised this work. D.M.F., K.A.S., H.R., M.M., S.M., I.O. and M. Lipson analysed genetic data. D.M.F., K.A.S., W.F.K. and D.R. wrote the manuscript with input from all co-authors.

Corresponding authors

Correspondence to Alfredo Coppa, Ron Pinhasi or David Reich.

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Extended data figures and tables

Extended Data Fig. 1 Temporal distribution of newly reported individuals and overview of population structure.

a, Numbers represent individuals from each site; thick lines denote direct 14C dates (95.4% calibrated confidence intervals); thin lines denote archaeological-context dating; grey area identifies the first arrivals of ceramic users in the Caribbean. Colours and labels are consistent with Fig. 1. b, PCA plot with ancient individuals shown as solid squares or circles for Archaic- or Ceramic-associated individuals, respectively. Newly reported individuals are outlined in black; genetic outliers are outlined in red; and individuals with <30,000 SNPs are outlined in blue. Individuals are separated by subclades, and three individuals from the site of Cueva Roja (Dominican Republic) who were excluded from clading analysis analysis are labelled *Dominican_Archaic (Cueva Roja) and coloured magenta. Individual PDI009, previously assessed elsewhere as an outlier11, is denoted with a cross. Three previously published ancient Caribbean individuals9,10 are shown as inverted triangles outlined in grey and coloured for the subclade that encompasses the geographical region with which they are associated. This plot focuses on ancient individuals and does not show some present-day populations; a full plot is provided as Supplementary Fig. 17. c, ADMIXTURE analysis best supports K = 6 ancestral elements. Newly reported and co-analysed individuals are clustered by subclade; all newly reported individuals are identified by a black bar to the side of the plot. The same three previously published individuals9,10 shown in b are included, and three present-day populations (Suruí, Cabécar and Piapoco) are shown for reference.

Extended Data Fig. 2 FST distances.

a, b, Average pairwise FST distances and standard errors (×100) between clades (a) and sites with more than two unrelated individuals (b), demonstrating both overall high levels of genetic similarity between the *Caribbean_Ceramic subclades and the sites composing them, as well as the magnitude of genetic differentiation between those and the groups with Archaic- and Venezuela-related ancestries.

Extended Data Fig. 3 Maximum-likelihood population tree from allele frequencies using Treemix.

The *Caribbean_Ceramic subclades are inferred to be on the same branch as modern Arawak-speaking groups (Palikur and Jamamadi). Orange arrows represent admixture events, although observations from other analyses (for example, qpAdm admixture modelling) suggest that the indicated direction of admixture may be inaccurate (for example, we believe it is more likely that there is *GreaterAntilles_Archaic admixture into *Haiti_Ceramic than the reverse scenario (Supplementary Information section 9)).

Extended Data Fig. 4 Estimated effective population sizes.

a, Estimates per site are based on ROH blocks 4–20 cM long using a likelihood model (Supplementary Information section 7). Colours as per subclades; numbers denote the count of analysed individuals. Highly consanguineous individuals with a sum of ROH > 20 above 50 cM were excluded. b, As in a, but for IBD segments 8–20 cM long shared on the X chromosome between all pairs of males. Closely related pairs of individuals with a sum of IBD X > 20 above 25 cM were excluded. Numbers denote counts of all remaining pairs. In a, b, points represent maximum-likelihood estimate and vertical bars represent 95% confidence interval.

Extended Data Fig. 5 Conditional heterozygosity by clade.

Conditional heterozygosity in the ancient Caribbean was similar to that of contemporaneous groups from Peru71, except for the Archaic-associated groups and *Venezuela_Ceramic. First- and second-degree relatives were excluded from the analysis, including the pair of related individuals who represent *Haiti_Ceramic. Coloured circles represent point estimates (colour scheme matching Fig. 1); bars represent three s.e.

Extended Data Fig. 6 Pairwise kinship estimates for all individuals from sites where close relatives were identified using autosomal data.

Dotted lines identify family clusters and intersite relationships; bottom rows correspond to relationships per individual.

Extended Data Table 1 Ne values for each site
Extended Data Table 2 Subset of cross-site relatives from different islands, identified through IBD analysis
Extended Data Table 3 Ancestry proportion estimates using qpAdm for present-day Caribbean individuals from Cuba (and its provinces), Dominican Republic and Puerto Rico
Extended Data Table 4 Statistics testing for an Australasian link

Supplementary information

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Fernandes, D.M., Sirak, K.A., Ringbauer, H. et al. A genetic history of the pre-contact Caribbean. Nature 590, 103–110 (2021). https://doi.org/10.1038/s41586-020-03053-2

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