Life history and ancestry of the late Upper Palaeolithic infant from Grotta delle Mura, Italy.

Italy Humans Infant Fossils Female History, Ancient Radiometric Dating Male Hominidae / genetics Archaeology Tooth Genetic Variation

Journal

Nature communications

ISSN: 2041-1723

Titre abrégé: Nat Commun

Pays: England

ID NLM: 101528555

Informations de publication

Date de publication:
20 Sep 2024

Historique:

received: 14 07 2023

accepted: 30 07 2024

medline: 21 9 2024

pubmed: 21 9 2024

entrez: 20 9 2024

Statut: epublish

Résumé

The biological aspects of infancy within late Upper Palaeolithic populations and the role of southern refugia at the end of the Last Glacial Maximum are not yet fully understood. This study presents a multidisciplinary, high temporal resolution investigation of an Upper Palaeolithic infant from Grotta delle Mura (Apulia, southern Italy) combining palaeogenomics, dental palaeohistology, spatially-resolved geochemical analyses, direct radiocarbon dating, and traditional anthropological studies. The skeletal remains of the infant - Le Mura 1 - were directly dated to 17,320-16,910 cal BP. The results portray a biological history of the infant's development, early life, health and death (estimated at ~72 weeks). They identify, several phenotypic traits and a potential congenital disease in the infant, the mother's low mobility during gestation, and a high level of endogamy. Furthermore, the genomic data indicates an early spread of the Villabruna-like components along the Italian peninsula, confirming a population turnover around the time of the Last Glacial Maximum, and highlighting a general reduction in genetic variability from northern to southern Italy. Overall, Le Mura 1 contributes to our better understanding of the early stages of life and the genetic puzzle in the Italian peninsula at the end of the Last Glacial Maximum.

Identifiants

DOI: 10.1038/s41467-024-51150-x PMID: 39304646

pubmed: 39304646

doi: 10.1038/s41467-024-51150-x

pii: 10.1038/s41467-024-51150-x

doi:

Types de publication

Journal Article Historical Article

Langues

eng

Sous-ensembles de citation

Pagination

8248

Subventions

Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 Marie Skłodowska-Curie Actions (H2020 Excellent Science - Marie Skłodowska-Curie Actions)

ID : 101104566 - AROUSE

Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)

ID : 803147 RESOLUTION

ID : 101077348 - MOTHERS

Informations de copyright

Références

Lambeck, K., Rouby, H., Purcell, A., Sun, Y. & Sambridge, M. Sea level and global ice volumes from the Last Glacial Maximum to the Holocene. Proc. Natl Acad. Sci. USA 111, 15296–15303 (2014).

pmcid: 4217469 doi: 10.1073/pnas.1411762111

Bortolini, E. et al. Early Alpine occupation backdates westward human migration in Late Glacial Europe. Curr. Biol. 31, 2484–2493.e7 (2021).

doi: 10.1016/j.cub.2021.03.078

Posth, C. et al. Palaeogenomics of Upper Palaeolithic to Neolithic European hunter-gatherers. Nature 615, 117–126 (2023).

pmcid: 9977688 doi: 10.1038/s41586-023-05726-0

Lugli, F. et al. Strontium and stable isotope evidence of human mobility strategies across the Last Glacial Maximum in southern Italy. Nat. Ecol. Evol. 3, 905–911 (2019).

doi: 10.1038/s41559-019-0900-8

Wren, C. D. & Burke, A. Habitat suitability and the genetic structure of human populations during the Last Glacial Maximum (LGM) in Western Europe. PLoS One https://doi.org/10.1371/journal.pone.0217996 (2019).

Ruiz-Redondo, A. et al. Mid and Late Upper Palaeolithic in the Adriatic Basin: Chronology, transitions and human adaptations to a changing landscape. Quat. Sci. Rev. 276, 107319 (2022).

doi: 10.1016/j.quascirev.2021.107319

Modi, A. et al. Paleogenetic and morphometric analysis of a Mesolithic individual from Grotta d’Oriente: An oldest genetic legacy for the first modern humans in Sicily. Quat. Sci. Rev. 248, 106603 (2020).

doi: 10.1016/j.quascirev.2020.106603

Villalba-Mouco, V. et al. Survival of Late Pleistocene Hunter-Gatherer Ancestry in the Iberian Peninsula. Curr. Biol. 29, 1169–1177.e7 (2019).

doi: 10.1016/j.cub.2019.02.006

Villalba-Mouco, V. et al. A 23,000-year-old southern Iberian individual links human groups that lived in Western Europe before and after the Last Glacial Maximum. Nat. Ecol. Evol. 7, 597–609 (2023).

pmcid: 10089921

Lugli, F. et al. Tracing the mobility of a Late Epigravettian (~ 13 ka) male infant from Grotte di Pradis (Northeastern Italian Prealps) at high-temporal resolution. Sci. Rep. https://doi.org/10.1038/s41598-022-12193-6 (2022).

doi: 10.1038/s41598-022-12193-6 pmcid: 9584910

Nava, A. et al. Early life of Neanderthals. Proc. Natl Acad. Sci. USA 117, 28719–28726 (2020).

pmcid: 7682388 doi: 10.1073/pnas.2011765117

Nava, A. et al. Virtual histological assessment of the prenatal life history and age at death of the Upper Paleolithic fetus from Ostuni (Italy). Sci. Rep. 7, 1–10 (2017).

doi: 10.1038/s41598-017-09773-2

Teschler-Nicola, M. et al. Ancient DNA reveals monozygotic newborn twins from the Upper Palaeolithic. Commun. Biol. 3, 1–11 (2020).

doi: 10.1038/s42003-020-01372-8

Calattini, M. Scoperta di una sepoltura paleolitica a Grotta delle Mura (BA). Rassegna di archeologia: preistorica e protostorica 37–45 https://doi.org/10.1400/248076 (2002).

Stloukal, M. & Hanakova, H. Die Longe der langskonochen altslavischer Bevolkerungen unter besonderer Bercksichtigung von Wachstumsfragen. Homo 29, 53–69 (1978).

AlQahtani, S. J., Hector, M. P. & Liversidge, H. M. Brief communication: The London atlas of human tooth development and eruption. Am. J. Phys. Anthropol. 142, 481–490 (2010).

doi: 10.1002/ajpa.21258

Bronk Ramsey, C. Bayesian analysis of radiocarbon dates. Radiocarbon 51, 337–360 (2009).

doi: 10.1017/S0033822200033865

Reid, D. J. & Dean, M. C. Variation in modern human enamel formation times. J. Hum. Evol. 50, 329–346 (2006).

doi: 10.1016/j.jhevol.2005.09.003

Hillson, S. Dental Anthropology (Cambridge University Press, 1996).

Molnar, S. Human tooth wear, tooth function and cultural variability. Am. J. Phys. Anthropol. 34, 175–189 (1971).

doi: 10.1002/ajpa.1330340204

Hutchinson, D. L. & Spencer Larsen, C. Determination of Stress Episode Duration from Linear Enamel Hypoplasias: A Case Study from St. Catherines Island, Georgia. Hum. Biol. 60, 93–110 (1988).

Moorrees, C. F. A., Fanning, E. A. & Hunt, E. E. Formation and resorption of three deciduous teeth in children. Am. J. Phys. Anthropol. 21, 205–213 (1963).

doi: 10.1002/ajpa.1330210212

Sabel, N. et al. Neonatal lines in the enamel of primary teeth—A morphological and scanning electron microscopic investigation. Arch. Oral. Biol. 53, 954–963 (2008).

doi: 10.1016/j.archoralbio.2008.05.003

Nava, A., Frayer, D. W. & Bondioli, L. Longitudinal analysis of the microscopic dental enamel defects of children in the Imperial Roman community of Portus Romae (necropolis of Isola Sacra, 2nd to 4th century CE, Italy). J. Archaeol. Sci. Rep. 23, 406–415 (2019).

Reid, D. J., Beynon, A. D. & Ramirez Rozzi, F. V. Histological reconstruction of dental development in four individuals from a medieval site in Picardie, France. J. Hum. Evol. 35, 463–477 (1998).

doi: 10.1006/jhev.1998.0233

Nava, A. et al. New regression formula to estimate the prenatal crown formation time of human deciduous central incisors derived from a Roman Imperial sample (Velia, Salerno, Italy, I-II cent. CE). PLoS One 12, e0180104 (2017).

pmcid: 5507505 doi: 10.1371/journal.pone.0180104

Mahoney, P. Incremental enamel development in modern human deciduous anterior teeth. Am. J. Phys. Anthropol. 147, 637–651 (2012).

doi: 10.1002/ajpa.22029

Dean, C. Extension rates and growth in tooth height of modern human and fossil hominin canines and molars. Front. Oral Biol. 13, 68–73 (2009).

Mahoney, P. Dental fast track: Prenatal enamel growth, incisor eruption, and weaning in human infants. Am. J. Phys. Anthropol. 156, 407–421 (2015).

doi: 10.1002/ajpa.22666

Guatelli-Steinberg, D., Floyd, B. A., Dean, M. C. & Reid, D. J. Enamel extension rate patterns in modern human teeth: Two approaches designed to establish an integrated comparative context for fossil primates. J. Hum. Evol. 63, 475–486 (2012).

doi: 10.1016/j.jhevol.2012.05.006

Ortiz, A., Skinner, M. M., Bailey, S. E. & Hublin, J. J. Carabelli’s trait revisited: An examination of mesiolingual features at the enamel-dentine junction and enamel surface of Pan and Homo sapiens upper molars. J. Hum. Evol. 63, 586–596 (2012).

doi: 10.1016/j.jhevol.2012.06.003

Moorrees, C. F. A., Fanning, E. A. & Hunt, E. E. Age variation of formation stages for ten permanent teeth. J. Dent. Res. 42, 1490–1502 (1963).

doi: 10.1177/00220345630420062701

Mahoney, P. Intraspecific variation in M1 enamel development in modern humans: implications for human evolution. J. Hum. Evol. 55, 131–147 (2008).

doi: 10.1016/j.jhevol.2008.02.004

Aris, C. Enamel growth rate variation of inner, mid, and outer enamel regions between select permanent tooth types across five temporally distinct British samples. Arch Oral Biol 137, (105394, 2022).

Antoine, D., Hillson, S. & Dean, M. C. The developmental clock of dental enamel: A test for the periodicity of prism cross-striations in modern humans and an evaluation of the most likely sources of error in histological studies of this kind. J. Anat. 214, 45–55 (2009).

pmcid: 2667916 doi: 10.1111/j.1469-7580.2008.01010.x

Sawyer, S., Krause, J., Guschanski, K., Savolainen, V. & Pääbo, S. Temporal patterns of nucleotide misincorporations and DNA fragmentation in ancient DNA. PLoS One 7, (e34131, 2012).

Jones, E. R. et al. Upper Palaeolithic genomes reveal deep roots of modern Eurasians. Nat. Commun. 6, 1–8 (2015).

doi: 10.1038/ncomms9912

Fu, Q. et al. The genetic history of Ice Age Europe. Nature 534, 200–205 (2016).

pmcid: 4943878 doi: 10.1038/nature17993

Lazaridis, I. et al. Ancient human genomes suggest three ancestral populations for present-day Europeans. Nature 513, 409–413 (2014).

pmcid: 4170574 doi: 10.1038/nature13673

Scorrano, G. et al. Bioarchaeological and palaeogenomic portrait of two Pompeians that died during the eruption of Vesuvius in 79 AD. Sci. Rep. 12, 1–12 (2022).

doi: 10.1038/s41598-022-10899-1

Catalano, G. et al. A mitogenome sequence of an Equus hydruntinus specimen from Late Quaternary site of San Teodoro Cave (Sicily, Italy). Quat. Sci. Rev. 236, 106280 (2020).

doi: 10.1016/j.quascirev.2020.106280

Antonioli, F. et al. Timing of the emergence of the Europe-Sicily bridge (40-17 cal ka BP) and its implications for the spread of modern humans. Geol. Soc. Spec. Publ. 411, 111–144 (2016).

doi: 10.1144/SP411.1

Ringbauer, H., Novembre, J. & Steinrücken, M. Parental relatedness through time revealed by runs of homozygosity in ancient DNA. Nat. Commun. 12, 1–11 (2021).

doi: 10.1038/s41467-021-25289-w

Prüfer, K. et al. A high-coverage Neandertal genome from Vindija Cave in Croatia. Science 358, 655–658 (2017).

pmcid: 6185897 doi: 10.1126/science.aao1887

Petr, M., Pääbo, S., Kelso, J. & Vernot, B. Limits of long-term selection against Neandertal introgression. Proc. Natl Acad. Sci. USA 116, 1639–1644 (2019).

pmcid: 6358679 doi: 10.1073/pnas.1814338116

Moorjani, P., Amorim, C. E. G., Arndt, P. F. & Przeworski, M. Variation in the molecular clock of primates. Proc. Natl Acad. Sci. USA 113, 10607–10612 (2016).

pmcid: 5035889 doi: 10.1073/pnas.1600374113

Fenner, J. N. Cross-cultural estimation of the human generation interval for use in genetics-based population divergence studies. Am. J. Phys. Anthropol. 128, 415–423 (2005).

doi: 10.1002/ajpa.20188

Coll Macià, M., Skov, L., Peter, B. M. & Schierup, M. H. Different historical generation intervals in human populations inferred from Neanderthal fragment lengths and mutation signatures. Nat. Commun. 12, 1–11 (2021).

doi: 10.1038/s41467-021-25524-4

Cariaso, M. & Lennon, G. SNPedia: A wiki supporting personal genome annotation, interpretationand analysis. Nucleic Acids Res. 40, (D1308-12, 2012).

Sherry, S. T. et al. DbSNP: The NCBI database of genetic variation. Nucleic Acids Res. 29, 308–311 (2001).

pmcid: 29783 doi: 10.1093/nar/29.1.308

Chaitanya, L. et al. The HIrisPlex-S system for eye, hair and skin colour prediction from DNA: Introduction and forensic developmental validation. Forensic. Sci. Int. Genet. 35, 123–135 (2018).

doi: 10.1016/j.fsigen.2018.04.004

Allentoft, M. E. et al. Population Genomics of Bronze Age Eurasia. Nature 522, 167–172 (2015).

doi: 10.1038/nature14507

Christiaans, I. et al. Founder mutations in hypertrophic cardiomyopathy patients in the Netherlands. Neth. Heart J. 18, 254 (2010).

Richard, P. et al. Hypertrophic Cardiomyopathy. Circulation 107, 2227–2232 (2003).

doi: 10.1161/01.CIR.0000066323.15244.54

Tompkins, R. L. Human population variability in relative dental development. Am. J. Phys. Anthropol. 99, 79–102 (1996).

doi: 10.1002/(SICI)1096-8644(199601)99:1<79::AID-AJPA5>3.0.CO;2-V

Hodgkins, J. et al. An infant burial from Arma Veirana in northwestern Italy provides insights into funerary practices and female personhood in early Mesolithic Europe. Sci Rep 8, (23735, 2021).

Brenner, B., Seebohm, B., Tripathi, S., Montag, J. & Kraft, T. Familial hypertrophic cardiomyopathy: Functional variance among individual cardiomyocytes as a trigger of fhc-phenotype development. Front. Physiol. 5, (392, 2014).

Bagnall, R. D. et al. A Prospective Study of Sudden Cardiac Death among Children and Young Adults. N. Engl. J. Med. 374, 2441–2452 (2016).

doi: 10.1056/NEJMoa1510687

Olalde, I. et al. Derived immune and ancestral pigmentation alleles in a 7,000-year-old Mesolithic European. Nature 507, 225–228 (2014).

pmcid: 4269527 doi: 10.1038/nature12960

Günther, T. et al. Population genomics of Mesolithic Scandinavia: Investigating early postglacial migration routes and high-latitude adaptation. PLoS Biol. 16, e2003703 (2018).

pmcid: 5760011 doi: 10.1371/journal.pbio.2003703

Lévi-Strauss, C. Les Structures Élémentaires de La Parenté (Mouton de Gruyter, 1967).

Bittles, A. H. Consanguinity, genetic drift, and genetic diseases in populations with reduced numbers of founders. in Vogel and Motulsky’s Human Genetics: Problems and Approaches (Fourth Edition) 507–528 (Springer-Verlag, 2010). https://doi.org/10.1007/978-3-540-37654-5_19 .

Ceballos, F. C. et al. Human inbreeding has decreased in time through the Holocene. Curr. Biol. 31, 3925–3934.e8 (2021).

doi: 10.1016/j.cub.2021.06.027

Palma di Cesnola, A. Il Paleolitico Superiore in Italia: Introduzione (Allo Studio, 1993).

Catalano, G. et al. Late Upper Palaeolithic hunter-gatherers in the Central Mediterranean: New archaeological and genetic data from the Late Epigravettian burial Oriente C (Favignana, Sicily). Quat. Int. 537, 24–32 (2020).

doi: 10.1016/j.quaint.2020.01.025

Modi, A. et al. More data on ancient human mitogenome variability in Italy: new mitochondrial genome sequences from three Upper Palaeolithic burials. Ann. Hum. Biol. 48, 213–222 (2021).

doi: 10.1080/03014460.2021.1942549

Yu, H. et al. Genomic and dietary discontinuities during the Mesolithic and Neolithic in Sicily. iScience 25, 104244 (2022).

pmcid: 9051636 doi: 10.1016/j.isci.2022.104244

Fu, Q. et al. A revised timescale for human evolution based on ancient mitochondrial genomes. Curr. Biol. 23, 553–559 (2013).

pmcid: 5036973 doi: 10.1016/j.cub.2013.02.044

Naudinot, N. et al. Between Atlantic and Mediterranean: Changes in technology during the Late Glacial in Western Europe and the climate hypothesis. Quat. Int. 428, 33–49 (2017).

doi: 10.1016/j.quaint.2016.01.056

Boschin, F. et al. The first evidence for Late Pleistocene dogs in Italy. Sci. Rep. 10, 1–14 (2020).

doi: 10.1038/s41598-020-69940-w

Šešelj, M. Brief communication: An analysis of dental development in Pleistocene Homo using skeletal growth and chronological age. Am. J. Phys. Anthropol. 163, 531–541 (2017).

doi: 10.1002/ajpa.23228

Fewlass, H. et al. Pretreatment and gaseous radiocarbon dating of 40-100 mg archaeological bone. Sci. Rep. 9, 5342 (2019).

pmcid: 6440986 doi: 10.1038/s41598-019-41557-8

Talamo, S., Fewlass, H., Maria, R. & Jaouen, K. ‘Here we go again’: the inspection of collagen extraction protocols for 14 C dating and palaeodietary analysis. Sci. Technol. Archaeol. Res. 7, 62–77 (2021).

pmcid: 8300532

Longin, R. New method of collagen extraction for radiocarbon dating. Nature 230, 241–242 (1971).

doi: 10.1038/230241a0

Brown, T. A., Nelson, D. E., Vogel, J. S. & Southon, J. R. Improved Collagen Extraction by Modified Longin Method. Radiocarbon 30, 171–177 (1988).

doi: 10.1017/S0033822200044118

Van Klinken, G. J. Bone collagen quality indicators for palaeodietary and radiocarbon measurements. J. Archaeol. Sci. 26, 687–695 (1999).

doi: 10.1006/jasc.1998.0385

Wacker, L., Němec, M. & Bourquin, J. A revolutionary graphitisation system: Fully automated, compact and simple. Nucl. Instrum. Methods Phys. Res B 268, 931–934 (2010).

doi: 10.1016/j.nimb.2009.10.067

Kromer, B., Lindauer, S., Synal, H. A. & Wacker, L. MAMS - A new AMS facility at the Curt-Engelhorn-Centre for Achaeometry, Mannheim, Germany. Nucl. Instrum. Methods Phys. Res. B 294, 11–13 (2013).

doi: 10.1016/j.nimb.2012.01.015

Reimer, P. J. et al. The IntCal20 Northern Hemisphere Radiocarbon Age Calibration Curve (0-55 cal kBP). Radiocarbon 62, 725–757 (2020).

doi: 10.1017/RDC.2020.41

Birch, W. & Dean, M. C. A method of calculating human deciduous crown formation times and of estimating the chronological ages of stressful events occurring during deciduous enamel formation. J. Forensic Leg. Med. 22, 127–144 (2014).

doi: 10.1016/j.jflm.2013.12.002

Schindelin, J. et al. Fiji: An open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).

Müller, W. et al. Enamel mineralization and compositional time-resolution in human teeth evaluated via histologically-defined LA-ICPMS profiles. Geochim. Cosmochim. Acta 255, 105–126 (2019).

doi: 10.1016/j.gca.2019.03.005

Müller, W. & Anczkiewicz, R. Accuracy of laser-ablation (LA)-MC-ICPMS Sr isotope analysis of (bio)apatite-a problem reassessed. J. Anal. Spectrom. 31, 259–269 (2016).

doi: 10.1039/C5JA00311C

R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2023).

Cleveland, W. S., Grosse, E. & Shyu, W. M. Local Regression Models. in Statistical Models in S (eds. Chambers, J. M. & Hastie, T. J.) (Routledge, 1992). https://doi.org/10.1201/9780203738535-8 .

Vazzana, A. et al. High-accuracy methodology for the integrative restoration of archaeological teeth by using reverse engineering techniques and rapid prototyping. J Archaeol Sci Rep 44, (103511, 2022).

Willerslev, E. & Cooper, A. Ancient DNA. Proc. R. Soc. B Biol. Sci. 272, 16 (2005).

Gilbert, M. T. P., Bandelt, H. J., Hofreiter, M. & Barnes, I. Assessing ancient DNA studies. Trends Ecol. Evol. 20, 541–544 (2005).

doi: 10.1016/j.tree.2005.07.005

Kircher, M., Sawyer, S. & Meyer, M. Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform. Nucleic Acids Res. 40, e3 (2012).

Meyer, M. & Kircher, M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc. 5, pdb.prot5448 (2010).

Rohland, N., Harney, E., Mallick, S., Nordenfelt, S. & Reich, D. Partial uracil – DNA – glycosylase treatment for screening of ancient DNA. Philos. Trans. R. Soc. B Biol. Sci. 370, 20130624 (2015).

doi: 10.1098/rstb.2013.0624

Maricic, T., Whitten, M. & Pääbo, S. Multiplexed DNA Sequence Capture of Mitochondrial Genomes Using PCR Products. PLoS One 5, e14004 (2010).

pmcid: 2982832 doi: 10.1371/journal.pone.0014004

Peltzer, A. et al. EAGER: efficient ancient genome reconstruction. Genome Biol. 17, 60 (2016).

pmcid: 4815194 doi: 10.1186/s13059-016-0918-z

Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

pmcid: 2705234 doi: 10.1093/bioinformatics/btp324

Schiffels, S. GitHub - stschiff/sequenceTools. https://github.com/stschiff/sequenceTools (2020).

Mallick, S. et al. The Allen Ancient DNA Resource (AADR) a curated compendium of ancient human genomes. Sci. Data 11, 1–10 (2024).

doi: 10.1038/s41597-024-03031-7

Mallick, S. & Reich, D. The Allen Ancient DNA Resource (AADR): A curated compendium of ancient human genomes. David Reich Lab Dataverse, V8 https://doi.org/10.7910/DVN/FFIDCW (2023).

Prüfer, K. et al. A genome sequence from a modern human skull over 45,000 years old from Zlatý kůň in Czechia. Nat. Ecol. Evol. 5, 820–825 (2021).

pmcid: 8175239 doi: 10.1038/s41559-021-01443-x

Yu, H. Paleogenomics of Upper Paleolithic to Neolithic European hunter-gatherers. EDMOND, V3 https://doi.org/10.17617/3.Y1KJMF (2022).

Skoglund, P., Storå, J., Götherström, A. & Jakobsson, M. Accurate sex identification of ancient human remains using DNA shotgun sequencing. J. Archaeol. Sci. 40, 4477–4482 (2013).

doi: 10.1016/j.jas.2013.07.004

Mittnik, A., Wang, C.-C., Svoboda, J. & Krause, J. A Molecular Approach to the Sexing of the Triple Burial at the Upper Paleolithic Site of Dolní Věstonice. PLoS One 11, e0163019 (2016).

pmcid: 5051676 doi: 10.1371/journal.pone.0163019

Jónsson, H., Ginolhac, A., Schubert, M., Johnson, P. L. F. & Orlando, L. MapDamage2.0: Fast approximate Bayesian estimates of ancient DNA damage parameters. Bioinformatics 29, 1682–1684 (2013).

pmcid: 3694634 doi: 10.1093/bioinformatics/btt193

Rasmussen, M. et al. An aboriginal Australian genome reveals separate human dispersals into Asia. Science 334, 94–98 (2011).

pmcid: 3991479 doi: 10.1126/science.1211177

Korneliussen, T. S., Albrechtsen, A. & Nielsen, R. ANGSD: Analysis of Next Generation Sequencing Data. BMC Bioinforma. 15, 356 (2014).

doi: 10.1186/s12859-014-0356-4

Furtwängler, A. et al. Ratio of mitochondrial to nuclear DNA affects contamination estimates in ancient DNA analysis. Sci. Rep. 8, 14075 (2018).

pmcid: 6145933 doi: 10.1038/s41598-018-32083-0

Nakatsuka, N. et al. ContamLD: Estimation of ancient nuclear DNA contamination using breakdown of linkage disequilibrium. Genome Biol. 21, 199 (2020).

pmcid: 7418405 doi: 10.1186/s13059-020-02111-2

Renaud, G., Slon, V., Duggan, A. T. & Kelso, J. Schmutzi: Estimation of contamination and endogenous mitochondrial consensus calling for ancient DNA. Genome Biol. 16, 224 (2015).

pmcid: 4601135 doi: 10.1186/s13059-015-0776-0

Weissensteiner, H. et al. HaploGrep 2: mitochondrial haplogroup classification in the era of high-throughput sequencing. Nucleic Acids Res. 44, W58–W63 (2016).

pmcid: 4987869 doi: 10.1093/nar/gkw233

van Oven, M. PhyloTree Build 17: Growing the human mitochondrial DNA tree. Forensic Sci Int Genet Suppl Ser 5, e392–e394 (2015).

Edgar, R. C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797 (2004).

pmcid: 390337 doi: 10.1093/nar/gkh340

Ingman, M., Kaessmann, H., Pääbo, S. & Gyllensten, U. Mitochondrial genome variation and the origin of modem humans. Nature 408, 708–713 (2000).

doi: 10.1038/35047064

Briggs, A. W. et al. Targeted retrieval and analysis of five Neandertal mtDNA genomes. Science 325, 318–321 (2009).

doi: 10.1126/science.1174462

Kumar, S., Stecher, G., Li, M., Knyaz, C. & Tamura, K. MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms | Molecular Biology and Evolution | Oxford Academic. Mol. Biol. Evol. 35, 1547–1549 (2018).

pmcid: 5967553 doi: 10.1093/molbev/msy096

Posth, C. et al. Pleistocene mitochondrial genomes suggest a single major dispersal of non-africans and a late glacial population turnover in Europe. Curr. Biol. 26, 827–833 (2016).

doi: 10.1016/j.cub.2016.01.037

Guindon, S. & Gascuel, O. A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood. Syst. Biol. 52, 696–704 (2003).

doi: 10.1080/10635150390235520

Darriba, D., Taboada, G. L., Doallo, R. & Posada, D. JModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 9, https://doi.org/10.1038/nmeth.2109 (2012).

Suchard, M. A. et al. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4, vey016 (2018).

Rambaut, A., Drummond, A. J., Xie, D., Baele, G. & Suchard, M. A. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901–904 (2018).

pmcid: 6101584 doi: 10.1093/sysbio/syy032

Bouckaert, R. et al. BEAST 2.5: An advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol 15, e1006650 (2019).

Ralf, A., Montiel González, D., Zhong, K. & Kayser, M. Yleaf: Software for Human Y-Chromosomal Haplogroup Inference from Next-Generation Sequencing Data. Mol. Biol. Evol. 35, 1291–1294 (2018).

doi: 10.1093/molbev/msy032

Gamba, C. et al. Genome flux and stasis in a five millennium transect of European prehistory. Nat. Commun. 5, 5257 (2014).

doi: 10.1038/ncomms6257

Mathieson, I. et al. The genomic history of southeastern Europe. Nature 555, 197–203 (2018).

pmcid: 6091220 doi: 10.1038/nature25778

Raghavan, M. et al. Upper palaeolithic Siberian genome reveals dual ancestry of native Americans. Nature 505, 87–91 (2014).

doi: 10.1038/nature12736

Fu, Q. et al. An early modern human from Romania with a recent Neanderthal ancestor. Nature 524, 216–219 (2015).

pmcid: 4537386 doi: 10.1038/nature14558

Fu, Q. et al. Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514, 445–449 (2014).

pmcid: 4753769 doi: 10.1038/nature13810

Sikora, M. et al. Ancient genomes show social and reproductive behavior of early Upper Paleolithic foragers. Science (1979) 358, 659–662 (2017).

Skoglund, P. et al. Genomic diversity and admixture differs for stone-age Scandinavian foragers and farmers. Science (1979) 344, 747–750 (2014).

Antonio, M. L. et al. Ancient Rome: A genetic crossroads of Europe and the Mediterranean. Science 366, 708–714 (2019).

pmcid: 7093155 doi: 10.1126/science.aay6826

Seguin-Orlando, A. et al. Genomic structure in Europeans dating back at least 36,200 years. Science 346, 1113–1118 (2014).

doi: 10.1126/science.aaa0114

González-Fortes, G. et al. Paleogenomic Evidence for Multi-generational Mixing between Neolithic Farmers and Mesolithic Hunter-Gatherers in the Lower Danube Basin. Curr. Biol. 27, 1801–1810.e10 (2017).

pmcid: 5483232 doi: 10.1016/j.cub.2017.05.023

De Barros Damgaard, P. et al. 137 ancient human genomes from across the Eurasian steppes. Nature 557, 369–374 (2018).

doi: 10.1038/s41586-018-0094-2

Mathieson, I. et al. Genome-wide patterns of selection in 230 ancient Eurasians. Nature 528, 499–503 (2015).

pmcid: 4918750 doi: 10.1038/nature16152

Mittnik, A. et al. The genetic prehistory of the Baltic Sea region. Nat. Commun. 9, 1–11 (2018).

Jones, E. R. et al. The Neolithic Transition in the Baltic Was Not Driven by Admixture with Early European Farmers. Curr. Biol. 27, 576–582 (2017).

pmcid: 5321670 doi: 10.1016/j.cub.2016.12.060

McKenna, A. et al. The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).

pmcid: 2928508 doi: 10.1101/gr.107524.110

Patterson, N. et al. Ancient admixture in human history. Genetics 192, 1065–1093 (2012).

pmcid: 3522152 doi: 10.1534/genetics.112.145037

Haak, W. et al. Massive migration from the steppe was a source for Indo-European languages in Europe. Nature 522, 207–211 (2015).

Lazaridis, I. et al. Genomic insights into the origin of farming in the ancient Near East. Nature 536, 419–424 (2016).

Mafessoni, F. et al. A high-coverage neandertal genome from chagyrskaya cave. Proc. Natl Acad. Sci. USA 117, 15132–15136 (2020).

pmcid: 7334501 doi: 10.1073/pnas.2004944117

Meyer, M. et al. A high-coverage genome sequence from an archaic Denisovan individual. Science 338, 222–226 (2012).

pmcid: 3617501 doi: 10.1126/science.1224344

Sankararaman, S., Patterson, N., Li, H., Pääbo, S. & Reich, D. The Date of Interbreeding between Neandertals and Modern Humans. PLoS Genet. 8, e1002947 (2012).

pmcid: 3464203 doi: 10.1371/journal.pgen.1002947

Peter, B. M. 100,000 years of gene flow between Neandertals and Denisovans in the Altai mountains. bioRxiv, https://doi.org/10.1101/2020.03.13.990523 (2020).

Auton, A. et al. A global reference for human genetic variation. The 1000 Genomes Project Consortium. Nature 526, 68-74 (2015).

Herrero, J. et al. Ensembl comparative genomics resources. Database 2016, bav096 (2016).

pmcid: 4761110 doi: 10.1093/database/bav096

Hinch, A. G. et al. The landscape of recombination in African Americans. Nature 476, 170–175 (2011).

Montaner, D. SNPediaR: Query data from SNPedia. R package version 1.30.0, https://github.com/genometra/SNPediaR (2024).

Walsh, S. et al. DNA-based eye colour prediction across Europe with the IrisPlex system. Forensic Sci. Int. Genet. 6, 330–340 (2012).

doi: 10.1016/j.fsigen.2011.07.009

Walsh, S. et al. Developmental validation of the HIrisPlex system: DNA-based eye and hair colour prediction for forensic and anthropological usage. Forensic Sci. Int. Genet. 9, 150–161 (2014).

doi: 10.1016/j.fsigen.2013.12.006

Walsh, S. et al. Global skin colour prediction from DNA. Hum. Genet. 136, 847–863 (2017).

pmcid: 5487854 doi: 10.1007/s00439-017-1808-5