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Genetic continuity and change among the Indigenous peoples of California

Abstract

Before the colonial period, California harboured more language variation than all of Europe, and linguistic and archaeological analyses have led to many hypotheses to explain this diversity1. We report genome-wide data from 79 ancient individuals from California and 40 ancient individuals from Northern Mexico dating to 7,400–200 years before present (bp). Our analyses document long-term genetic continuity between people living on the Northern Channel Islands of California and the adjacent Santa Barbara mainland coast from 7,400 years bp to modern Chumash groups represented by individuals who lived around 200 years bp. The distinctive genetic lineages that characterize present-day and ancient people from Northwest Mexico increased in frequency in Southern and Central California by 5,200 years bp, providing evidence for northward migrations that are candidates for spreading Uto-Aztecan languages before the dispersal of maize agriculture from Mexico2,3,4. Individuals from Baja California share more alleles with the earliest individual from Central California in the dataset than with later individuals from Central California, potentially reflecting an earlier linguistic substrate, whose impact on local ancestry was diluted by later migrations from inland regions1,5. After 1,600 years bp, ancient individuals from the Channel Islands lived in communities with effective sizes similar to those in pre-agricultural Caribbean and Patagonia, and smaller than those on the California mainland and in sampled regions of Mexico.

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Fig. 1: Summary of data.
Fig. 2: Neighbour-joining tree of groups.
Fig. 3: Northwest Mexico-related ancestry at different regions over time from qpAdm.
Fig. 4: ROHs in all ancient peoples from California and Mexico.

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Data availability

All sequencing data newly generated in this study are available from the European Nucleotide Archive (ENA) under accession number PRJEB66319. Genotype data obtained by random sampling of sequences at approximately 1.24 million analysed positions are available from Harvard Dataverse under accession number Z2JD58. The data we are publishing in this study are the DNA libraries for each of the ancient individuals we analysed, which are molecular copies of the original molecules extracted from the ancient individuals whose remains in many cases may no longer be available for scientific study. The data we report are therefore not only stored after publication in digital form (the sequences we uploaded) but in molecular form for as long as the libraries are maintained in freezers. This means that more sequences may be generated by those who can support generating a higher quality digital readout of the library, with permission to generate such sequences covered by the current publication. These libraries can only be requested for scholarly use and cannot be used for commercial purposes. If the relevant Indigenous communities request them to be repatriated or reburied, they will no longer be available. In addition, we used the following publicly available datasets: ref. 14 (ENA: PRJEB25445); ref. 34 (ENA: PRJEB37446 and PRJEB39010); ref. 16 (ENA: PRJEB28961); ref. 36 (ENA: PRJEB3555); ref. 70 (ENA: PRJNA470966); ref. 71 (ENA: PRJEB9586 and ERP010710); ref. 79 (NCBI Sequence Read Archive database identifier: SRP029640); and ref. 19 (ENA: PRJEB29074). The hg19 human genome reference sequence was used for all analyses, available at https://www.ncbi.nlm.nih.gov/datasets/genome/GCF_000001405.25/. The author-accepted version of this article (that is, the version not reflecting proofreading and editing and formatting changes at Nature following the article’s acceptance), is subject to the Howard Hughes Medical Institute (HHMI) Open Access to Publications policy, as HHMI lab heads have previously granted a nonexclusive CC BY 4.0 license to the public and a sublicensable license to HHMI in their research articles. Pursuant to those licenses, the author-accepted manuscript (not Nature’s version of record) can be made freely available under a CC BY 4.0 license immediately upon publication.

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Acknowledgements

We acknowledge and thank the ancient individuals whose remains were analysed in this study, and the present-day Indigenous communities who supported this study and provided cultural contextualization that we sought to reflect in the final paper, particularly representatives from the Chumash, Tongva, Ohlone and Esselen groups; staff at the Consejo de Arqueología and the Instituto Nacional de Antropología e Historia for the permits and facilities granted for the study of the samples from Mexico; expert linguists J. Yee (member of the Barbareño Chumash tribe), L. Campbell, M. Mithun, M. Walworth, J. W. Powell, P. Munro and D. Shaul for their comments and suggestions regarding how best to discuss the implications of our genetic results for linguistic debates; H. Ringbauer for advice on the ROH analyses; I. Lazaridis for determining Y chromosome haplogroups; M. Armenta, I. Lazaridis, M. Lipson, I. Olalde and N. Patterson for critical comments and helpful discussions; N. Adamski, R. Bernardos, M. Ferry, G. Fisher, I. Greenslade, K. Mable, K. Stewardson, Z. Zhang, staff at the American Museum of Natural History and the Peabody Museum of Archaeology and Ethnology for support with wet laboratory work or bioinformatics or sample management; and archaeologist G. S. Breschini, who would have been an author on this paper had he not passed away in 2018. Support for analysis of DNA from ancient individuals from Monterey County was provided by the late E. Rodriguez (Most Likely Descendant; Rumsen tribe) and provided for this study by the late G. Breschini. N.N. was supported by a National Institutes of General Medical Sciences fellowship. The PIPANOM Project, sampling individuals from Northern Mexico, was supported by a grant from the National Geographic Society to J.L.P.D. The ancient DNA data collection and statistical analyses were supported by a grant from the National Human Genome Research Institute (R01-HG012287), the John Templeton Foundation (grant 61220), by a private gift from Jean-Francois Clin, by the Allen Discovery Center programme, a Paul G. Allen Frontiers Group advised programme of the Paul G. Allen Family Foundation, and by the Howard Hughes Medical Institute (D.R.).

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Authors and Affiliations

Authors

Contributions

N.N. performed population genetics analyses. N.N., B.H., J.S., P.E.L., J.C., C.G.-M., D.M., J.M.-R., A.P.-M., V.T., M.E.V.-C., A.V.H., J.L.P.D., J.R.J. and D.R. interpreted the data. J.S., P.E.L., J.C., C.G.-M., D.M., J.M.-R., A.P.-M., V.T., M.E.V.-C., A.V.H., J.L.P.D. and J.R.J. collected and described archaeological material and site contexts. K.C., E.C., A.K., L.I., A.M.L., M.M., J.N.W., J.O., L.Q., F.Z. and N.R. performed or supervised sample preparations. N.R. and A.M.L. generated genetic data. N.N., J.R.J., J.L.P.D., J.R.J. and D.R. conceived the study. T.K.H. and B.J.C. performed or supervised accelerator mass spectrometry radiocarbon dating analyses and marine correction. N.R., S.M., M. Mah, A.M. and D.R. performed bioinformatics analyses. N.N., B.H., J.S., J.L.P.D., J.R.J. and D.R. wrote the paper with the assistance of the other co-authors. J.R.J. and D.R. directed the study together.

Corresponding authors

Correspondence to Nathan Nakatsuka, John R. Johnson or David Reich.

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Extended data figures and tables

Extended Data Fig. 1 ADMIXTURE plot at different K values.

Purple=Central California, red=Southern California mainland, dark red=Northern Channel Islands, orange=Southern Channel Islands and nearby mainland, light blue=Baja California, blue=Mexico excluding Baja California.

Extended Data Fig. 2 MDS plot of groups created using a matrix of inverted outgroup-f3 statistics (distances = 1-f3(Mbuti; Group1, Group2)).

Purple=Central California, red=Southern California mainland, dark red=Northern Channel Islands, orange=Southern Channel Islands and nearby mainland, light blue=Baja California, blue=Mexico excluding Baja California.

Extended Data Fig. 3 Heatmap of pairwise FST.

FST between groups was estimated using smartpca. Only groups with at least 2 individuals of greater than 100,000 SNP coverage were used. Heatmap and dendrogram were created in R with symm=T. Supplementary Data File 3 shows FST values. Purple=Central California, red=Southern California mainland, dark red=Northern Channel Islands, orange=Southern Channel Islands and nearby mainland, light blue=Baja California, blue=Mexico excluding Baja California.

Extended Data Fig. 4 Map of statistics of the form f4(Mbuti, Test; USA-CA_Carmel_600BP, USA-CA_PacificGrove_5200BP).

Dots in red show greater genetic affinity to PacificGrove_5200BP relative to Carmel_600BP, while dots in black and blue have greater affinity to Carmel_600BP. Points are jittered to allow better visualization. Figure is generated with open source data and software in R with ggplot2 and the ‘fields’ and ‘RcolorBrewer’ libraries.

Extended Data Fig. 5 Admixture graphs.

A) Example admixture graph testing for attraction to Canada_Lucier_4800-500 BP. This graph fits with a maximum |Z-score| of 2.81. We tested all subsequent graphs replacing CA_Ojai_1400BP with another ancient California group (Supplementary Data File 4). B) Admixture graph consistent with relationships between ancient California and Mexico groups. This graph fits with a maximum |Z-score| of 2.98. All graphs we explore require a lineage more basal than that of Chile_LosRieles_12000 BP to fit the Mexico individuals, although we caution that the total space of admixture graph topologies is too large to explore exhaustively so we are making no claim that these particular graphs are correct (only that they are plausible and not ruled out by the data). The basal ancestry into Canada_Lucier_4800-500 BP is present to account for known European contamination.

Extended Data Fig. 6 ROH in California and Mexico.

A) Average rate of ROH segments in different length bins after filtering out individuals with a sum of ROH segments of ≥20 cM of 100 cM or more and B) after filtering out individuals using a lower stringency threshold of 50 cM or more. Points with no ROH fragments present in those bins were filtered out. C) Average rate of ROH segments in different length bins after filtering out individuals over 1600 BP and D) after filtering out individuals with summed 20 cM over 100 cM or E) over 50 cM. F) ROH over time where each data point represents the average sum of ROH between 4–20 cM of individuals in a bin of its corresponding time-period (8000-6000 BP, 6000-4000 BP, 4000-1500 BP, and <1500 BP); the number of individuals for each of these time bins is (0,1,1,10) for Central California, (2,2,2,12) for Southern California Mainland, (3,0,4,7) for Northern Channel Islands, (0,2,3,9) for Southern Channel Islands), and (0,0,3,23) for Mexico. G) ROH over time after filtering out individuals with a sum of ROH segments of ≥20 cM of 100 cM or more; the number of individuals for each of these time bins is (0,1,1,10) for Central California, (2,2,2,12) for Southern California Mainland, (2,0,2,7) for Northern Channel Islands, (0,0,2,8) for Southern Channel Islands), and (0,0,3,22) for Mexico. H) ROH over time after filtering out individuals with a sum of ROH segments of ≥20 cM of 50 cM or more; the number of individuals for each of these time bins is (0,1,1,9) for Central California, (1,2,1,11) for Southern California Mainland, (1,0,1,7) for Northern Channel Islands, (0,0,1,7) for Southern Channel Islands), and (0,0,3,21) for Mexico. For all figures, data are presented as mean values ± 1 standard error (no standard errors are presented for points with fewer than 3 individuals).

Extended Data Fig. 7 Conditional heterozygosity of groups.

Ancient Californian, Mexican, Peruvian, Brazilian, Caribbean, and Patagonian groups and present-day Mexican, Brazilian and Peruvian groups are shown. Only groups with at least 2 individuals could be included in these analyses.

Supplementary information

Supplementary Information

Reporting Summary

Supplementary Data 1

(A) Meta-data about individuals newly sequenced or previously published from California or Northwest Mexico. (B) Technical information on each ancient DNA library built for all samples newly sequenced in this study as well as failed samples. (C) Meta-data of individuals previously published from other world regions that we co-analysed with those from California and Northwest Mexico.

Supplementary Data 2

qpWave, showing genetic homogeneity within groups.

Supplementary Data 3

FST between different groups.

Supplementary Data 4

f4 results as tests of admixture and qpgraph worst-fit Z-scores.

Supplementary Data 5

qpAdm estimates of ancestry.

Supplementary Data 6

qpWave analyses of migration into the Andes.

Supplementary Data 7

Inferred Ne from ROHs.

Supplementary Data 8

Frequently asked questions document prepared for Indigenous community members and others about the paper.

Peer Review File

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Nakatsuka, N., Holguin, B., Sedig, J. et al. Genetic continuity and change among the Indigenous peoples of California. Nature 624, 122–129 (2023). https://doi.org/10.1038/s41586-023-06771-5

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  • DOI: https://doi.org/10.1038/s41586-023-06771-5

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