A genetic history of the pre-contact Caribbean

doi:10.1038/s41586-020-03053-2

. 2021 Feb;590(7844):103-110.

doi: 10.1038/s41586-020-03053-2. Epub 2020 Dec 23.

A genetic history of the pre-contact Caribbean

Daniel M Fernandes^#^{1

2}, Kendra A Sirak^#^{3

4}, Harald Ringbauer^{3

4}, Jakob Sedig^{3

4}, Nadin Rohland^{3

5}, Olivia Cheronet¹, Matthew Mah^{3

4

5

6}, Swapan Mallick^{3

4

5

6}, Iñigo Olalde^{3

7}, Brendan J Culleton⁸, Nicole Adamski^{3

6}, Rebecca Bernardos^{3

6}, Guillermo Bravo^{1

9}, Nasreen Broomandkhoshbacht^{3

6

10}, Kimberly Callan^{3

6}, Francesca Candilio¹¹, Lea Demetz¹, Kellie Sara Duffett Carlson¹, Laurie Eccles¹², Suzanne Freilich¹, Richard J George¹³, Ann Marie Lawson^{3

6}, Kirsten Mandl¹, Fabio Marzaioli¹⁴, Weston C McCool¹³, Jonas Oppenheimer^{3

6

15}, Kadir T Özdogan¹, Constanze Schattke¹, Ryan Schmidt¹⁶, Kristin Stewardson^{3

6}, Filippo Terrasi¹⁴, Fatma Zalzala^{3

6}, Carlos Arredondo Antúnez¹⁷, Ercilio Vento Canosa¹⁸, Roger Colten¹⁹, Andrea Cucina²⁰, Francesco Genchi²¹, Claudia Kraan²², Francesco La Pastina²¹, Michaela Lucci²³, Marcio Veloz Maggiolo²⁴, Beatriz Marcheco-Teruel²⁵, Clenis Tavarez Maria²⁶, Christian Martínez²⁶, Ingeborg París²⁷, Michael Pateman^{28

29}, Tanya M Simms³⁰, Carlos Garcia Sivoli²⁷, Miguel Vilar³¹, Douglas J Kennett¹³, William F Keegan³², Alfredo Coppa^{33

34

35}, Mark Lipson^{3

4}, Ron Pinhasi³⁶, David Reich^{37

38

39

40}

Affiliations

¹ Department of Evolutionary Anthropology, University of Vienna, Vienna, Austria.
² CIAS, Department of Life Sciences, University of Coimbra, Coimbra, Portugal.
³ Department of Genetics, Harvard Medical School, Boston, MA, USA.
⁴ Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA.
⁵ Broad Institute of Harvard and MIT, Cambridge, MA, USA.
⁶ Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.
⁷ Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain.
⁸ Institutes of Energy and the Environment, The Pennsylvania State University, University Park, PA, USA.
⁹ Department of Legal Medicine, Toxicology and Physical Anthropology, University of Granada, Granada, Spain.
¹⁰ Department of Anthropology, University of California, Santa Cruz, CA, USA.
¹¹ Superintendency of Archaeology, Fine Arts and Landscape for the city of Cagliari and the provinces of Oristano and South Sardinia, Cagliari, Italy.
¹² Department of Anthropology, The Pennsylvania State University, University Park, PA, USA.
¹³ Department of Anthropology, University of California, Santa Barbara, CA, USA.
¹⁴ Department of Mathematics and Physics, Campania University 'Luigi Vanvitelli', Caserta, Italy.
¹⁵ Department of Biomolecular Engineering, University of California, Santa Cruz, CA, USA.
¹⁶ CIBIO-InBIO, University of Porto, Vairão, Portugal.
¹⁷ Museo Antropológico Montané, University of Havana, Havana, Cuba.
¹⁸ Matanzas University of Medical Sciences, Matanzas, Cuba.
¹⁹ Peabody Museum of Natural History, Yale University, New Haven, CT, USA.
²⁰ Facultad de Ciencias Antropológicas, Universidad Autónoma de Yucatán, Mérida, Mexico.
²¹ Department of Environmental Biology, Sapienza University of Rome, Rome, Italy.
²² National Archaeological-Anthropological Memory Management (NAAM), Willemstad, Curaçao.
²³ DANTE Laboratory of Diet and Ancient Technology, Sapienza University of Rome, Rome, Italy.
²⁴ Universidad Autónoma de Santo Domingo, San Francisco de Macorís, Dominican Republic.
²⁵ National Center of Medical Genetics, Medical University of Havana, Havana, Cuba.
²⁶ Museo del Hombre Dominicano, Santo Domingo, Dominican Republic.
²⁷ Instituto de Investigaciones Bioantropológicas y Arqueológicas, Universidad de Los Andes, Mérida, Venezuela.
²⁸ Turks and Caicos National Museum Foundation, Cockburn Town, Turks and Caicos Islands.
²⁹ AEX Bahamas Maritime Museum, Freeport, Bahamas.
³⁰ Department of Biology, University of The Bahamas, Nassau, Bahamas.
³¹ National Geographic Society, Washington, DC, USA.
³² Florida Museum of Natural History, University of Florida, Gainesville, FL, USA.
³³ Department of Evolutionary Anthropology, University of Vienna, Vienna, Austria. alfredo.coppa@uniroma1.it.
³⁴ Department of Genetics, Harvard Medical School, Boston, MA, USA. alfredo.coppa@uniroma1.it.
³⁵ Department of Environmental Biology, Sapienza University of Rome, Rome, Italy. alfredo.coppa@uniroma1.it.
³⁶ Department of Evolutionary Anthropology, University of Vienna, Vienna, Austria. ron.pinhasi@univie.ac.at.
³⁷ Department of Genetics, Harvard Medical School, Boston, MA, USA. reich@genetics.med.harvard.edu.
³⁸ Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA. reich@genetics.med.harvard.edu.
³⁹ Broad Institute of Harvard and MIT, Cambridge, MA, USA. reich@genetics.med.harvard.edu.
⁴⁰ Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA. reich@genetics.med.harvard.edu.

^# Contributed equally.

PMID: 33361817
PMCID: PMC7864882
DOI: 10.1038/s41586-020-03053-2

A genetic history of the pre-contact Caribbean

Daniel M Fernandes et al. Nature. 2021 Feb.

. 2021 Feb;590(7844):103-110.

doi: 10.1038/s41586-020-03053-2. Epub 2020 Dec 23.

Authors

Affiliations

¹ Department of Evolutionary Anthropology, University of Vienna, Vienna, Austria.
² CIAS, Department of Life Sciences, University of Coimbra, Coimbra, Portugal.
³ Department of Genetics, Harvard Medical School, Boston, MA, USA.
⁴ Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA.
⁵ Broad Institute of Harvard and MIT, Cambridge, MA, USA.
⁶ Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA.
⁷ Institute of Evolutionary Biology, CSIC-Universitat Pompeu Fabra, Barcelona, Spain.
⁸ Institutes of Energy and the Environment, The Pennsylvania State University, University Park, PA, USA.
⁹ Department of Legal Medicine, Toxicology and Physical Anthropology, University of Granada, Granada, Spain.
¹⁰ Department of Anthropology, University of California, Santa Cruz, CA, USA.
¹¹ Superintendency of Archaeology, Fine Arts and Landscape for the city of Cagliari and the provinces of Oristano and South Sardinia, Cagliari, Italy.
¹² Department of Anthropology, The Pennsylvania State University, University Park, PA, USA.
¹³ Department of Anthropology, University of California, Santa Barbara, CA, USA.
¹⁴ Department of Mathematics and Physics, Campania University 'Luigi Vanvitelli', Caserta, Italy.
¹⁵ Department of Biomolecular Engineering, University of California, Santa Cruz, CA, USA.
¹⁶ CIBIO-InBIO, University of Porto, Vairão, Portugal.
¹⁷ Museo Antropológico Montané, University of Havana, Havana, Cuba.
¹⁸ Matanzas University of Medical Sciences, Matanzas, Cuba.
¹⁹ Peabody Museum of Natural History, Yale University, New Haven, CT, USA.
²⁰ Facultad de Ciencias Antropológicas, Universidad Autónoma de Yucatán, Mérida, Mexico.
²¹ Department of Environmental Biology, Sapienza University of Rome, Rome, Italy.
²² National Archaeological-Anthropological Memory Management (NAAM), Willemstad, Curaçao.
²³ DANTE Laboratory of Diet and Ancient Technology, Sapienza University of Rome, Rome, Italy.
²⁴ Universidad Autónoma de Santo Domingo, San Francisco de Macorís, Dominican Republic.
²⁵ National Center of Medical Genetics, Medical University of Havana, Havana, Cuba.
²⁶ Museo del Hombre Dominicano, Santo Domingo, Dominican Republic.
²⁷ Instituto de Investigaciones Bioantropológicas y Arqueológicas, Universidad de Los Andes, Mérida, Venezuela.
²⁸ Turks and Caicos National Museum Foundation, Cockburn Town, Turks and Caicos Islands.
²⁹ AEX Bahamas Maritime Museum, Freeport, Bahamas.
³⁰ Department of Biology, University of The Bahamas, Nassau, Bahamas.
³¹ National Geographic Society, Washington, DC, USA.
³² Florida Museum of Natural History, University of Florida, Gainesville, FL, USA.
³³ Department of Evolutionary Anthropology, University of Vienna, Vienna, Austria. alfredo.coppa@uniroma1.it.
³⁴ Department of Genetics, Harvard Medical School, Boston, MA, USA. alfredo.coppa@uniroma1.it.
³⁵ Department of Environmental Biology, Sapienza University of Rome, Rome, Italy. alfredo.coppa@uniroma1.it.
³⁶ Department of Evolutionary Anthropology, University of Vienna, Vienna, Austria. ron.pinhasi@univie.ac.at.
³⁷ Department of Genetics, Harvard Medical School, Boston, MA, USA. reich@genetics.med.harvard.edu.
³⁸ Department of Human Evolutionary Biology, Harvard University, Cambridge, MA, USA. reich@genetics.med.harvard.edu.
³⁹ Broad Institute of Harvard and MIT, Cambridge, MA, USA. reich@genetics.med.harvard.edu.
⁴⁰ Howard Hughes Medical Institute, Harvard Medical School, Boston, MA, USA. reich@genetics.med.harvard.edu.

^# Contributed equally.

PMID: 33361817
PMCID: PMC7864882
DOI: 10.1038/s41586-020-03053-2

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 ago^1-3. 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 large^5,6. 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 world^1,8.

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Figures

**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. Colors and labels are consistent with Fig. 1. **(b)** PCA plot with ancient individuals shown as solid squares or circles (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 sub-clades, and three individuals from the site of Cueva Roja (Dominican Republic) who were excluded from clading analysis are labeled “Dominican Cueva Roja Archaic” and colored magenta. Individual PDI009, assessed elsewhere as an outlier, is denoted with an asterisk. Three previously-published ancient Caribbean individuals^, are shown as inverted triangles outlined in gray and colored for the sub-clade that encompasses the geographic 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 Fig. S17. **(c)** ADMIXTURE analysis best supports K=6 ancestral elements. Newly-reported and co-analyzed individuals are clustered by sub-clade; all newly-reported individuals are identified by a black bar to the side of the plot. The same three previously-published individuals^, shown in Extended Data Fig. 1b are included, and three modern-day populations are shown for reference (Suruí, Cabécar, Piapoco).

**Extended Data Fig. 2|. F_ST distances.**
Average pairwise FST distances and standard errors (x100) between **(a)** clades and **(b)** sites with more than two unrelated individuals, demonstrating both overall high levels of genetic similarity between the *Caribbean_Ceramic* sub-clades 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* sub-clades are shown on the same branch as modern Arawak-speaking groups (Palikur, Jamamadi). Orange arrows represent admixture events, although observations from other analyses (e.g., *qpAdm* admixture modeling) suggest that the indicated direction of admixture may be inaccurate (e.g., 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). Colors as per sub-clades, numbers denote the count of analyzed individuals. Highly consanguineous individuals with a sum of ROH>20 above 50 cM were excluded. **(b)** Same as (a) but for IBD segments 8–20cM 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) and (b) points represent maximum likelihood estimate and vertical bars represent 95% CI.

**Extended Data Fig. 5:. Conditional heterozygosity by clade.**
Conditional heterozygosity in the ancient Caribbean was similar to that of contemporaneous groups from Peru, 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 representing *Haiti_Ceramic*. Colored circles represent point estimates (color scheme matching Fig. 1); bars represent three standard errors.

**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 inter-site relationships; bottom rows correspond to relationships per individual.

**Fig. 1:. Geography and significant genetic structure.**
**(a)** Newly-reported data shown as large bordered shapes; co-analyzed data shown as small non-bordered shapes. Asterisk (*) denotes Archaic-associated site of Cueva Roja (excluded due to low-coverage); hash (#) denotes sites with admixed individuals. Andrés is represented as *SECoastDR_Ceramic* and *Dominican_Archaic*. Numbers of individuals and temporal distribution in Extended Data Fig. 1a. Map generated with the R package “maps” (R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/). (b) Relationships reconstructed from allele sharing (Supplementary Information section 8). Solid lines connect sub-groupings comprising a larger group; dashed lines represent admixture. Colored boxes represent final sub-clades with the color scheme matching Fig. 1a.

**Fig. 2:. Genetic affinities of ancient Caribbean people.**
(a) Outgroup f₃-statistics measuring the relatedness of the clades *GreaterAntilles_Archaic*, *Caribbean_Ceramic,* and *Venezuela_Ceramic* to present-day populations (squares). Map generated with the R package “maps” (R Core Team (2013). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/). (b) We computed f₄*(Mbuti, Test; LanguageGroup1Pop, LanguageGroup2Pop)* evaluating if each *Test* sub-clade is more closely related to populations belonging to one language family or another. Points represent the average Z-scores among all populations from each pair of language groups tested; horizontal lines show the range across such comparisons. Vertical lines represent a significance threshold corresponding to a 99.5% CI. (c) Admixture graph modelling of representative ancient Caribbean groupings and select non-Caribbean populations. We fit 12 groups, including the clades *LesserAntilles_Ceramic* and *GreaterAntilles_Archaic,* without mixture; the other three *Caribbean_Ceramic* sub-clades and the clade *Venezuela_Ceramic* fit as mixtures. The worst Z-score comparing observed to expected f-statistics is |3.6|, which is not significant after correcting for multiple hypothesis testing.

**Fig. 3:. Estimates of effective population size from shared haplotypes.**
Details in Supplementary Information section 7. (a) Number of generations since two chromosomes with a shared segment of a specific size shared a common ancestor, assuming a constant population size N=1000. (b) Average rate of ROH segments in different length bins after excluding highly consanguineous individuals (defined as having a sum of ROH>20 >50cM). (c) Rates of IBD segments shared on the X chromosome between pairs of males within length bins after excluding closely related individuals (defined as sum of IBD X>20 >25cM). For the N_e estimates quoted in the paper we use the pool of 12–20cM segments; for comparisons between the two major clades *SECoastDR_Ceramic* and *EasternGreaterAntilles_Ceramic* this gives N_e=3082 (95% CI 1530–8150). In (b) and (c) confidence intervals correspond to one standard deviation (68% coverage) assuming a Poisson distribution in each bin (vertical bars). Point estimates (circles) placed at the center of each 2cM bin, with jitter added for visual separation. Gray lines depict expectations for panmictic populations of various sizes.

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References

1. Rouse I. The Tainos: Rise & Decline of the People who Greeted Columbus. (Yale University Press, 1992).
1. Maggiolo MV La isla de Santo Domingo antes de Colón (Banco Central de la Republica Dominicana, 1993).
1. Keegan WF & Hofman CL The Caribbean before Columbus. (Oxford University Press, 2017).
1. Nägele K. et al. Genomic insights into the early peopling of the Caribbean. Science 369, 456–460 (2020). - PubMed
1. Cook SF & Borah W. The Aboriginal Population of Hispaniola. vol. 1 376–410 (University of California Press, 1971).

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[1] Rouse I. The Tainos: Rise & Decline of the People who Greeted Columbus. (Yale University Press, 1992).

[2] Rouse I. The Tainos: Rise & Decline of the People who Greeted Columbus. (Yale University Press, 1992).

[3] Maggiolo MV La isla de Santo Domingo antes de Colón (Banco Central de la Republica Dominicana, 1993).

[4] Maggiolo MV La isla de Santo Domingo antes de Colón (Banco Central de la Republica Dominicana, 1993).

[5] Keegan WF & Hofman CL The Caribbean before Columbus. (Oxford University Press, 2017).

[6] Keegan WF & Hofman CL The Caribbean before Columbus. (Oxford University Press, 2017).

[7] Nägele K. et al. Genomic insights into the early peopling of the Caribbean. Science 369, 456–460 (2020). - PubMed

[8] Nägele K. et al. Genomic insights into the early peopling of the Caribbean. Science 369, 456–460 (2020). - PubMed

[9] Cook SF & Borah W. The Aboriginal Population of Hispaniola. vol. 1 376–410 (University of California Press, 1971).

[10] Cook SF & Borah W. The Aboriginal Population of Hispaniola. vol. 1 376–410 (University of California Press, 1971).

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A genetic history of the pre-contact Caribbean

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A genetic history of the pre-contact Caribbean

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