Testing Times: Challenges in Disentangling Admixture Histories in Recent and Complex Demographies
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic
Typ dokumentu preprinty, časopisecké články
Grantová podpora
R35 GM146886
NIGMS NIH HHS - United States
PubMed
38014190
PubMed Central
PMC10680674
DOI
10.1101/2023.11.13.566841
PII: 2023.11.13.566841
Knihovny.cz E-zdroje
- Klíčová slova
- aDNA, admixture, archaeogenetics, f-statistics, paleogenomics, qpAdm,
- Publikační typ
- časopisecké články MeSH
- preprinty MeSH
Paleogenomics has expanded our knowledge of human evolutionary history. Since the 2020s, the study of ancient DNA has increased its focus on reconstructing the recent past. However, the accuracy of paleogenomic methods in answering questions of historical and archaeological importance amidst the increased demographic complexity and decreased genetic differentiation within the historical period remains an open question. We used two simulation approaches to evaluate the limitations and behavior of commonly used methods, qpAdm and the f3-statistic, on admixture inference. The first is based on branch-length data simulated from four simple demographic models of varying complexities and configurations. The second, an analysis of Eurasian history composed of 59 populations using whole-genome data modified with ancient DNA conditions such as SNP ascertainment, data missingness, and pseudo-haploidization. We show that under conditions resembling historical populations, qpAdm can identify a small candidate set of true sources and populations closely related to them. However, in typical ancient DNA conditions, qpAdm is unable to further distinguish between them, limiting its utility for resolving fine-scaled hypotheses. Notably, we find that complex gene-flow histories generally lead to improvements in the performance of qpAdm and observe no bias in the estimation of admixture weights. We offer a heuristic for admixture inference that incorporates admixture weight estimate and P-values of qpAdm models, and f3-statistics to enhance the power to distinguish between multiple plausible candidates. Finally, we highlight the future potential of qpAdm through whole-genome branch-length f2-statistics, demonstrating the improved demographic inference that could be achieved with advancements in f-statistic estimations.
Department of Biology and Ecology Faculty of Science University of Ostrava Ostrava Czechia
Department of Human Evolutionary Biology Harvard University Cambridge MA USA
Pennsylvania State University Department of Biology University Park PA 16802 USA
Zobrazit více v PubMed
Adrion J. R., Cole C. B., Dukler N., Galloway J. G., Gladstein A. L., et al., 2020. A community-maintained standard library of population genetic models. PubMed PMC
Agranat-Tamir L., Waldman S., Martin M. A. S., Gokhman D., Mishol N., et al., 2020. The Genomic History of the Bronze Age Southern Levant. Cell 181: 1146–1157.e11. PubMed PMC
Alexander D. H., Novembre J., and Lange K., 2009. Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19: 1655–1664. PubMed PMC
Antonio M. L., Gao Z., Moots H. M., Lucci M., Candilio F., et al., 2019. Ancient Rome: A genetic crossroads of Europe and the Mediterranean. Science 366: 708–714. PubMed PMC
Arning N., and Wilson D. J., 2020. The past, present and future of ancient bacterial DNA. Microb Genom 6. PubMed PMC
Ávila-Arcos M. C., Raghavan M., and Schlebusch C., 2023. Going local with ancient DNA: A review of human histories from regional perspectives. Science 382: 53–58. PubMed
Barros Damgaard P. de, Martiniano R., Kamm J., Moreno-Mayar J. V., Kroonen G., et al., 2018. The first horse herders and the impact of early Bronze Age steppe expansions into Asia. Science 360. PubMed PMC
Bartash V., 2020. The Early Dynastic Near East, in Oxford University Press.
Baumdicker F., Bisschop G., Goldstein D., Gower G., Ragsdale A. P., et al., 2021. Efficient ancestry and mutation simulation with msprime 1.0. Genetics 220: iyab229. PubMed PMC
Bergström A., Stanton D. W. G., Taron U. H., Frantz L., Sinding M.-H. S., et al., 2022. Grey wolf genomic history reveals a dual ancestry of dogs. Nature 607: 313–320. PubMed PMC
Boyle K., and Renfrew C., 2000. Archaeogenetics : DNA and the population prehistory of Europe, in Published in 2000 in Cambridge by McDonald institute for archaeological research, Cambridge: : McDonald Institute for Archaeological Research.
Broushaki F., Thomas M. G., Link V., López S., van Dorp L., et al., 2016. Early Neolithic genomes from the eastern Fertile Crescent. Science 353: 499–503. PubMed PMC
Brunson K., and Reich D., 2019. The Promise of Paleogenomics Beyond Our Own Species. Trends in Genetics 35: 319–329. PubMed
Carlhoff S., Duli A., Nägele K., Nur M., Skov L., et al., 2021. Genome of a middle Holocene hunter-gatherer from Wallacea. Nature 596: 543–547. PubMed PMC
Changmai P., Jaisamut K., Kampuansai J., Kutanan W., Altınışık N. E., et al., 2022a. Indian genetic heritage in Southeast Asian populations. PLoS Genet. 18: e1010036. PubMed PMC
Changmai P., Pinhasi R., Pietrusewsky M., Stark M. T., Ikehara-Quebral R. M., et al., 2022b. Ancient DNA from Protohistoric Period Cambodia indicates that South Asians admixed with local populations as early as 1st-3rd centuries CE. Sci. Rep. 12: 22507. PubMed PMC
Clemente F., Unterländer M., Dolgova O., Amorim C. E. G., Coroado-Santos F., et al., 2021. The genomic history of the Aegean palatial civilizations. Cell 184: 2565–2586.e21. PubMed PMC
De Schepper S., Ray J. L., Skaar K. S., Sadatzki H., Ijaz U. Z., et al., 2019. The potential of sedimentary ancient DNA for reconstructing past sea ice evolution. ISME J. 13: 2566–2577. PubMed PMC
Durand E. Y., Patterson N., Reich D., and Slatkin M., 2011. Testing for ancient admixture between closely related populations. Mol. Biol. Evol. 28: 2239–2252. PubMed PMC
Elise Lauterbur M., Cavassim M. I. A., Gladstein A. L., Gower G., Pope N. S., et al., 2022 Expanding the stdpopsim species catalog, and lessons learned for realistic genome simulations. bioRxiv 2022.10.29.514266. PubMed PMC
Fernandes D. M., Mittnik A., Olalde I., Lazaridis I., Cheronet O., et al., 2020. The spread of steppe and Iranian-related ancestry in the islands of the western Mediterranean. Nat Ecol Evol 4: 334–345. PubMed PMC
Flegontov P., Işıldak U., Maier R., Yüncü E., Changmai P., et al., 2023. Modeling of African population history using f-statistics is biased when applying all previously proposed SNP ascertainment schemes. PLoS Genet. 19: e1010931. PubMed PMC
Fu Q., Posth C., Hajdinjak M., Petr M., Mallick S., et al., 2016. The genetic history of Ice Age Europe. Nature 534: 200–205. PubMed PMC
Gower G., Ragsdale A. P., Bisschop G., Gutenkunst R. N., Hartfield M., et al., 2022. Demes: a standard format for demographic models. Genetics 222. PubMed PMC
Green R. E., Krause J., Briggs A. W., Maricic T., Stenzel U., et al., 2010. A draft sequence of the Neandertal genome. Science 328: 710–722. PubMed PMC
Haak W., Lazaridis I., Patterson N., Rohland N., Mallick S., et al., 2015. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522: 207–211. PubMed PMC
Haber M., Mezzavilla M., Xue Y., and Tyler-Smith C., 2016. Ancient DNA and the rewriting of human history: be sparing with Occam’s razor. Genome Biol. 17: 1. PubMed PMC
Haber M., Doumet-Serhal C., Scheib C., Xue Y., Danecek P., et al., 2017. Continuity and Admixture in the Last Five Millennia of Levantine History from Ancient Canaanite and Present-Day Lebanese Genome Sequences. Am. J. Hum. Genet. 101: 274–282. PubMed PMC
Haber M., Nassar J., Almarri M. A., Saupe T., Saag L., et al., 2020. A Genetic History of the Near East from an aDNA Time Course Sampling Eight Points in the Past 4,000 Years. Am. J. Hum. Genet. PubMed PMC
Harney É., May H., Shalem D., Rohland N., Mallick S., et al., 2018. Ancient DNA from Chalcolithic Israel reveals the role of population mixture in cultural transformation. Nat. Commun. 9: 3336. PubMed PMC
Harney É., Patterson N., Reich D., and Wakeley J., 2021. Assessing the performance of qpAdm: a statistical tool for studying population admixture. Genetics. PubMed PMC
Harris A. M., and DeGiorgio M., 2017. Admixture and Ancestry Inference from Ancient and Modern Samples through Measures of Population Genetic Drift. Hum. Biol. 89: 21–46. PubMed
Hollfelder N., Breton G., Sjödin P., and Jakobsson M., 2021. The deep population history in Africa. Hum. Mol. Genet. 30: R2–R10. PubMed PMC
Jónsson H., Sulem P., Kehr B., Kristmundsdottir S., Zink F., et al., 2017. Parental influence on human germline de novo mutations in 1,548 trios from Iceland. Nature 549: 519–522. PubMed
Jukes T. H., and Cantor C. R., 1969. CHAPTER 24 - Evolution of Protein Molecules, pp. 21–132 in Mammalian Protein Metabolism, edited by Munro H. N. Academic Press.
Kamm J., Terhorst J., Durbin R., and Song Y. S., 2020. Efficiently inferring the demographic history of many populations with allele count data. J. Am. Stat. Assoc. 115: 1472–1487. PubMed PMC
Kelleher J., Etheridge A. M., and McVean G., 2016. Efficient Coalescent Simulation and Genealogical Analysis for Large Sample Sizes. PLoS Comput. Biol. 12: e1004842. PubMed PMC
Koptekin D., Yüncü E., Rodríguez-Varela R., Altınışık N. E., Psonis N., et al., 2023. Spatial and temporal heterogeneity in human mobility patterns in Holocene Southwest Asia and the East Mediterranean. Curr. Biol. 33: 41–57.e15. PubMed PMC
Kristiansen K., 2016. Interpreting Bronze Age Trade and Migration, pp. 154–180 in Human Mobility and Technological Transfer in the Prehistoric Mediterranean, Cambridge University Press.
Lazaridis I., Nadel D., Rollefson G., Merrett D. C., Rohland N., et al., 2016. Genomic insights into the origin of farming in the ancient Near East. Nature 536: 419–424. PubMed PMC
Lazaridis I., Mittnik A., Patterson N., Mallick S., Rohland N., et al., 2017. Genetic origins of the Minoans and Mycenaeans. Nature 548: 214–218. PubMed PMC
Lazaridis I., Alpaslan-Roodenberg S., Acar A., Açıkkol A., Agelarakis A., et al., 2022a. The genetic history of the Southern Arc: A bridge between West Asia and Europe. Science 377: eabm4247. PubMed PMC
Lazaridis I., Alpaslan-Roodenberg S., Acar A., Açıkkol A., Agelarakis A., et al., 2022b. A genetic probe into the ancient and medieval history of Southern Europe and West Asia. Science 377: 940–951. PubMed PMC
Lee J., Miller B. K., Bayarsaikhan J., Johannesson E., Ventresca Miller A., et al., 2023. Genetic population structure of the Xiongnu Empire at imperial and local scales. Sci Adv 9: eadf3904. PubMed PMC
Librado P., Khan N., Fages A., Kusliy M. A., Suchan T., et al., 2021. The origins and spread of domestic horses from the Western Eurasian steppes. Nature 598: 634–640. PubMed PMC
Lipson M., Loh P.-R., Levin A., Reich D., Patterson N., et al., 2013. Efficient moment-based inference of admixture parameters and sources of gene flow. Mol. Biol. Evol. 30: 1788–1802. PubMed PMC
Lipson M., Loh P.-R., Patterson N., Moorjani P., Ko Y.-C., et al., 2014. Reconstructing Austronesian population history in Island Southeast Asia. Nat. Commun. 5: 4689. PubMed PMC
Liu Y., Mao X., Krause J., and Fu Q., 2021. Insights into human history from the first decade of ancient human genomics. Science 373: 1479–1484. PubMed
Llamas B., Willerslev E., and Orlando L., 2017. Human evolution: a tale from ancient genomes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372. PubMed PMC
van de Loosdrecht M., Bouzouggar A., Humphrey L., Posth C., Barton N., et al., 2018. Pleistocene North African genomes link Near Eastern and sub-Saharan African human populations. Science 360: 548–552. PubMed
Maier R., Flegontov P., Flegontova O., Isildak U., Changmai P., et al., 2023. On the limits of fitting complex models of population history to f-statistics. PubMed PMC
Mallick S., Micco A., Mah M., Ringbauer H., Lazaridis I., et al., 2023. The Allen Ancient DNA Resource (AADR): A curated compendium of ancient human genomes. bioRxiv 2023.04.06.535797. PubMed PMC
Marchi N., Winkelbach L., Schulz I., Brami M., Hofmanová Z., et al., 2022. The genomic origins of the world’s first farmers. Cell 185: 1842–1859.e18. PubMed PMC
Marcus J. H., Posth C., Ringbauer H., Lai L., Skeates R., et al., 2020. Genetic history from the Middle Neolithic to present on the Mediterranean island of Sardinia. Nat. Commun. 11: 939. PubMed PMC
Maróti Z., Neparáczki E., Schütz O., Maár K., Varga G. I. B., et al., 2022. The genetic origin of Huns, Avars, and conquering Hungarians. Curr. Biol. 32: 2858–2870.e7. PubMed
Martin S. H., Davey J. W., and Jiggins C. D., 2015. Evaluating the use of ABBA-BABA statistics to locate introgressed loci. Mol. Biol. Evol. 32: 244–257. PubMed PMC
Mathieson I., Alpaslan-Roodenberg S., Posth C., Szécsényi-Nagy A., Rohland N., et al., 2018. The genomic history of southeastern Europe. Nature 555: 197–203. PubMed PMC
McVean G., 2009. A genealogical interpretation of principal components analysis. PLoS Genet. 5: e1000686. PubMed PMC
Mitchell K. J., and Rawlence N. J., 2021. Examining Natural History through the Lens of Palaeogenomics. Trends Ecol. Evol. 36: 258–267. PubMed
Moots H. M., Antonio M., Sawyer S., Spence J. P., Oberreiter V., et al., 2023. A genetic history of continuity and mobility in the Iron Age central Mediterranean. Nat Ecol Evol 7: 1515–1524. PubMed
Narasimhan V. M., Patterson N., Moorjani P., Rohland N., Bernardos R., et al., 2019. The formation of human populations in South and Central Asia. Science. PubMed PMC
Nelson D., Kelleher J., Ragsdale A. P., Moreau C., McVean G., et al., 2020. Accounting for long-range correlations in genome-wide simulations of large cohorts. PLoS Genet. 16: e1008619. PubMed PMC
Nielsen S. V., Vaughn A. H., Leppälä K., Landis M. J., Mailund T., et al., 2023. Bayesian inference of admixture graphs on Native American and Arctic populations. PLoS Genet. 19: e1010410. PubMed PMC
Ning C., Li T., Wang K., Zhang F., Li T., et al., 2020. Ancient genomes from northern China suggest links between subsistence changes and human migration. Nat. Commun. 11: 2700. PubMed PMC
Olalde I., Mallick S., Patterson N., Rohland N., Villalba-Mouco V., et al., 2019. The genomic history of the Iberian Peninsula over the past 8000 years. Science 363: 1230–1234. PubMed PMC
Oliveira S., Nägele K., Carlhoff S., Pugach I., Koesbardiati T., et al., 2022. Ancient genomes from the last three millennia support multiple human dispersals into Wallacea. Nat Ecol Evol 6: 1024–1034. PubMed PMC
Papac L., Ernée M., Dobeš M., Langová M., Rohrlach A. B., et al., 2021. Dynamic changes in genomic and social structures in third millennium BCE central Europe. Sci Adv 7. PubMed PMC
Patterson N., Price A. L., and Reich D., 2006. Population Structure and Eigenanalysis. PLoS Genet. 2: e190. PubMed PMC
Patterson N., Moorjani P., Luo Y., Mallick S., Rohland N., et al., 2012. Ancient admixture in human history. Genetics 192: 1065–1093. PubMed PMC
Patterson N., Isakov M., Booth T., Büster L., Fischer C.-E., et al., 2022. Large-scale migration into Britain during the Middle to Late Bronze Age. Nature 601: 588–594. PubMed PMC
Peter B. M., 2016. Admixture, Population Structure, and F-Statistics. Genetics 202: 1485–1501. PubMed PMC
Peter B. M., 2022. A geometric relationship of F2, F3 and F4-statistics with principal component analysis. PHILOSOPHICAL TRANSACTIONS B. PubMed PMC
Pickrell J. K., and Pritchard J. K., 2012. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 8: e1002967. PubMed PMC
Reich D., Price A. L., and Patterson N., 2008. Principal component analysis of genetic data. Nat. Genet. 40: 491–492. PubMed
Reich D., Thangaraj K., Patterson N., Price A. L., and Singh L., 2009. Reconstructing Indian population history. Nature 461: 489–494. PubMed PMC
Reich D., Patterson N., Campbell D., Tandon A., Mazieres S., et al., 2012. Reconstructing Native American population history. Nature 488: 370–374. PubMed PMC
Salazar L., Burger R., Forst J., Barquera R., Nesbitt J., et al., 2023. Insights into the genetic histories and lifeways of Machu Picchu’s occupants. Sci Adv 9: eadg3377. PubMed PMC
Schmid C., and Schiffels S., 2023. Estimating human mobility in Holocene Western Eurasia with large-scale ancient genomic data. Proc. Natl. Acad. Sci. U. S. A. 120: e2218375120. PubMed PMC
Schuenemann V. J., Peltzer A., Welte B., van Pelt W. P., Molak M., et al., 2017. Ancient Egyptian mummy genomes suggest an increase of Sub-Saharan African ancestry in post-Roman periods. Nat. Commun. 8: 15694. PubMed PMC
Sirak K. A., Fernandes D. M., Lipson M., Mallick S., Mah M., et al., 2021. Social stratification without genetic differentiation at the site of Kulubnarti in Christian Period Nubia. Nat. Commun. 12: 7283. PubMed PMC
Skoglund P., Thompson J. C., Prendergast M. E., Mittnik A., Sirak K., et al., 2017. Reconstructing Prehistoric African Population Structure. Cell 171: 59–71.e21. PubMed PMC
Skourtanioti E., Erdal Y. S., Frangipane M., Balossi Restelli F., Yener K. A., et al., 2020. Genomic History of Neolithic to Bronze Age Anatolia, Northern Levant, and Southern Caucasus. Cell 181: 1158–1175.e28. PubMed
Skourtanioti E., Ringbauer H., Gnecchi Ruscone G. A., Bianco R. A., Burri M., et al., 2023. Ancient DNA reveals admixture history and endogamy in the prehistoric Aegean. Nat Ecol Evol 7: 290–303. PubMed PMC
Slatkin M., and Racimo F., 2016. Ancient DNA and human history. Proc. Natl. Acad. Sci. U. S. A. 113: 6380–6387. PubMed PMC
Soraggi S., and Wiuf C., 2019. General theory for stochastic admixture graphs and F-statistics. Theor. Popul. Biol. 125: 56–66. PubMed
Spyrou M. A., Bos K. I., Herbig A., and Krause J., 2019. Ancient pathogen genomics as an emerging tool for infectious disease research. Nat. Rev. Genet. 20: 323–340. PubMed PMC
Taylor W. T. T., Librado P., American Horse C. J., Shield Chief Gover C., Arterberry J., et al., 2023. Early dispersal of domestic horses into the Great Plains and northern Rockies. Science 379: 1316–1323. PubMed
Tricou T., Tannier E., and de Vienne D. M., 2022. Ghost Lineages Highly Influence the Interpretation of Introgression Tests. Syst. Biol. 71: 1147–1158. PubMed PMC
Wang C.-C., Reinhold S., Kalmykov A., Wissgott A., Brandt G., et al., 2019. Ancient human genome-wide data from a 3000-year interval in the Caucasus corresponds with eco-geographic regions. Nat. Commun. 10: 590. PubMed PMC
Wang K., Mathieson I., O’Connell J., and Schiffels S., 2020. Tracking human population structure through time from whole genome sequences. PLoS Genet. 16: e1008552. PubMed PMC
Wang C.-C., Yeh H.-Y., Popov A. N., Zhang H.-Q., Matsumura H., et al., 2021. Genomic insights into the formation of human populations in East Asia. Nature 591: 413–419. PubMed PMC
Wibowo M. C., Yang Z., Borry M., Hübner A., Huang K. D., et al., 2021. Reconstruction of ancient microbial genomes from the human gut. Nature 594: 234–239. PubMed PMC
Williams M., and Teixeira J., 2020. A genetic perspective on human origins. Biochem. 42: 6–10.
Wood S. N., 2004. Stable and Efficient Multiple Smoothing Parameter Estimation for Generalized Additive Models. J. Am. Stat. Assoc. 99: 673–686.
Yang M. A., Fan X., Sun B., Chen C., Lang J., et al., 2020. Ancient DNA indicates human population shifts and admixture in northern and southern China. Science 369: 282–288. PubMed
Yüncü E., Işıldak U., Williams M. P., Huber C. D., Flegontova O., et al., 2023. False discovery rates of qpAdm-based screens for genetic admixture. bioRxiv 2023.04.25.538339.
Zheng Y., and Janke A., 2018. Gene flow analysis method, the D-statistic, is robust in a wide parameter space. BMC Bioinformatics 19: 10. PubMed PMC