Cases of trisomy 21 and trisomy 18 among historic and prehistoric individuals discovered from ancient DNA.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
20 Feb 2024
20 Feb 2024
Historique:
received:
02
04
2023
accepted:
19
01
2024
medline:
21
2
2024
pubmed:
21
2
2024
entrez:
20
2
2024
Statut:
epublish
Résumé
Aneuploidies, and in particular, trisomies represent the most common genetic aberrations observed in human genetics today. To explore the presence of trisomies in historic and prehistoric populations we screen nearly 10,000 ancient human individuals for the presence of three copies of any of the target autosomes. We find clear genetic evidence for six cases of trisomy 21 (Down syndrome) and one case of trisomy 18 (Edwards syndrome), and all cases are present in infant or perinatal burials. We perform comparative osteological examinations of the skeletal remains and find overlapping skeletal markers, many of which are consistent with these syndromes. Interestingly, three cases of trisomy 21, and the case of trisomy 18 were detected in two contemporaneous sites in early Iron Age Spain (800-400 BCE), potentially suggesting a higher frequency of burials of trisomy carriers in those societies. Notably, the care with which the burials were conducted, and the items found with these individuals indicate that ancient societies likely acknowledged these individuals with trisomy 18 and 21 as members of their communities, from the perspective of burial practice.
Identifiants
pubmed: 38378781
doi: 10.1038/s41467-024-45438-1
pii: 10.1038/s41467-024-45438-1
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1294Subventions
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 : 771234
Informations de copyright
© 2024. The Author(s).
Références
Waldron, T. Palaeopathology (Cambridge University Press, 2021).
Lewis, M. Paleopathology of Children: Identification of Pathological Conditions in the Human Skeletal Remains of Non-Adults (Academic Press, 2017).
Roberts, C. A. Palaeopathology and Archaeology: The Current State of Play (Archaeopress, 2002).
Gresky, J., Dorn, J., Teßmann, B. & Petiti, E. How rare is rare? A literature survey of the last 45 years of paleopathological research on ancient rare diseases. Int. J. Paleopathol. 33, 94–102 (2021).
pubmed: 33813348
doi: 10.1016/j.ijpp.2021.03.003
Daard.dainst.org. DAARD digital atlas of ancient rare diseases. https://daard.dainst.org/ (2023).
Hassold, T. J. & Jacobs, P. A. Trisomy in man. Ann. Rev. Genet. 18, 69–97 (1984).
pubmed: 6241455
doi: 10.1146/annurev.ge.18.120184.000441
Goldstein, H. & Nielsen, K. G. Rates and survival of individuals with trisomy 13 and 18. Data from a 10-year period in Denmark. Clin. Genet. 34, 366–372 (1988).
pubmed: 3233784
doi: 10.1111/j.1399-0004.1988.tb02894.x
Korenberg, J. R. et al. Down syndrome phenotypes: the consequences of chromosomal imbalance. Proc. Natl Acad. Sci. USA 91, 4997–5001 (1994).
pubmed: 8197171
pmcid: 43917
doi: 10.1073/pnas.91.11.4997
Mai, C. T. et al. Selected birth defects data from population-based birth defects surveillance programs in the United States, 2006 to 2010: featuring trisomy conditions. Birth Defects Res. A Clin. Mol. Teratol. 97, 709–725 (2013).
pubmed: 24265125
pmcid: 4636004
doi: 10.1002/bdra.23198
Korbel, J. O. et al. The genetic architecture of Down syndrome phenotypes revealed by high-resolution analysis of human segmental trisomies. Proc. Natl Acad. Sci. USA 106, 12031–12036 (2009).
pubmed: 19597142
pmcid: 2709665
doi: 10.1073/pnas.0813248106
Brothwell, D. R. A possible case of mongolism in a Saxon population. Ann. Hum. Genet. 24, 141–150 (1960).
pubmed: 13804833
doi: 10.1111/j.1469-1809.1959.tb01727.x
Czarnetzki, A. A possible trisomy 21 for the Hallstatt period. In 3rd European Meeting (Paleopathology Association, 1980).
Walker, P. L., Cook, D. C., Ward, R., Braunstein, E. & Davee, M. A. Down syndrome-like congenital disorder in a prehistoric California Indian. Am. J. Phys. Anthropol. 34, 179 (1991).
Rivollat, M., Castex, D., Hauret, L. & Tillier, A. M. Ancient Down syndrome: an osteological case from Saint-Jean-des-Vignes, northeastern France, from the 5-6th century AD. Int. J. Paleopathol. 7, 8–14 (2014).
pubmed: 29539495
doi: 10.1016/j.ijpp.2014.05.004
Cassidy, L. M. et al. A dynastic elite in monumental Neolithic society. Nature 582, 384–388 (2020).
pubmed: 32555485
pmcid: 7116870
doi: 10.1038/s41586-020-2378-6
Orlando, L. et al. Ancient DNA analysis. Nat. Rev. Methods Prim. 1, 1–26 (2021).
Kallioniemi, A. et al. Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors. Science 258, 818–821 (1992).
pubmed: 1359641
doi: 10.1126/science.1359641
Balasundaram, P. & Avulakunta, I. D. Edwards Syndrome (StatPearls, 2022).
Телл Юнаците. Эпоха бронзы. Том II, Част первая. Москва 195, 210–211 (2007).
pubmed: 17222851
Penske, S. et al. Early contact between late farming and pastoralist societies in southeastern Europe. Nature 19, 1–8 (2023).
Eustratiou, K. & Polychronakou-Sgouritsa, N. Το Mykinaiko nekrotafeio stous Lazarides Aiginas [Το Μυκηναϊκό νεκροταφείο στους Λαζάρηδες Αίγινας; The Mycenaean cemetery at Lazarides, Aegina]. ArchDelt (Αρχαιολογικόν Δελτίον) 65–66, 1–162 (2010–2011).
Prevedorou, E. A. bioarchaeological perspective on the human skeletal remains from the Mycenaean settlement and cemetery at Lazarides. To Mykinaiko nekrotafeio stous Lazarides Aiginas [Το Μυκηναϊκό νεκροταφείο στους Λαζάρηδες Αίγινας; The Mycenaen cemetery at Lazarides, Aegina] ArchDelt (Αρχαιολογικόν Δελτίον) 149–160 (2010–2011).
Maluquer de Motes, J. El Yacimiento Hallstáttico de Cortes de Navarra: Estudio Crítico. 1. Diputacion Foral de Navarra (Inst. “Principe de Viana”, 1954).
Maluquer de Motes, J. El Yacimiento Hallstático de Cortes de Navarra. Estudio Crítico Il (Inst. “Principe de Viana”, 1958).
Maluquer de Motes, J., Munilla Cabrillana, G. & Gracia Alonso, F. Alto de la Cruz (Cortes, Navarra): campañas, 1986-1988. Trabajos Arqueol. Navar. 9, 11–245 (1990).
Taracena Aguirre, B. Excavaciones en Navarra. Cortes de Navarra. Los Poblados de la Edad del Hierro, Superpuestos en el “Alto de la Cruz” (Diputación de Navarra, 1954).
Armendáriz-Martija, J. & De-Miguel-Ibáñez, M. P. Los enterramientos infantiles del poblado de Las Eretas (Berbinzana): estudio paleoantropológico. Trabajos Arqueol. Navar. 19, 5–44 (2006).
McFadden, C., Muir, B. & Oxenham, M. F. Determinants of infant mortality and representation in bioarchaeological samples: a review. Am. J. Biol. Anthropol. 177, 196–206 (2022).
doi: 10.1002/ajpa.24406
Friese, C., Becker, G. & Nachtigall, R. D. Older motherhood and the changing life course in the era of assisted reproductive technologies. J. Aging Stud. 22, 65–73 (2008).
pubmed: 18443646
pmcid: 2350202
doi: 10.1016/j.jaging.2007.05.009
Todman, D. Childbirth in ancient Rome: from traditional folklore to obstetrics. Aust. N. Z. J. Obstet. Gynaecol. 47, 82–85 (2007).
pubmed: 17355293
doi: 10.1111/j.1479-828X.2007.00691.x
Papadimitriou, A. The evolution of the age at menarche from prehistorical to modern times. J. Pediatr. Adolesc. Gynecol. 29, 527–530 (2016).
pubmed: 26703478
doi: 10.1016/j.jpag.2015.12.002
Doe, D. M. et al. Puberty in the Bronze Age: first application of a puberty estimation method to a prehistoric population. Int. J. Osteoarchaeol. 29, 1091–1099 (2019).
doi: 10.1002/oa.2822
Manifold, B. M. Skeletal preservation of children’s remains in the archaeological record. Homo 66, 520–548 (2015).
pubmed: 26391374
doi: 10.1016/j.jchb.2015.04.003
Stempfle, N., Huten, Y., Fredouille, C., Brisse, H. & Nessmann, C. Skeletal abnormalities in fetuses with Down’s syndrome: a radiographic post-mortem study. Pediatr. Radiol. 29, 682–688 (1999).
pubmed: 10460330
doi: 10.1007/s002470050675
LaCombe, J. M. & Roper, R. J. Skeletal dynamics of Down syndrome: a developing perspective. Bone 133, 115–215 (2020).
doi: 10.1016/j.bone.2019.115215
Nordstrøm, M., Retterstøl, K., Hope, S. & Kolset, S. O. Nutritional challenges in children and adolescents with Down syndrome. Lancet Child Adolesc. Health 4, 455–464 (2020).
pubmed: 32450124
doi: 10.1016/S2352-4642(19)30400-6
Brickley, M. B., Ives, R. & Mays, S. The Bioarchaeology of Metabolic Bone Disease (Academic Press, 2020).
Seow, W. K. Developmental defects of enamel and dentine: challenges for basic science research and clinical management. Aust. Dent. J. 59, 143–154 (2014).
pubmed: 24164394
doi: 10.1111/adj.12104
Slomic, A. M., Bernier, J. P., Morissette, J. & Azouz, E. M. A craniometric study of Trisomy 21 (T 21). Bull. Mem. Soc. Anthropol. Paris 2, 189–202 (1990).
doi: 10.3406/bmsap.1990.1731
Kjaer, I., Keeling, J. W. & Hansen, B. F. Pattern of malformations in the axial skeleton in human trisomy 18 fetuses. Am. J. Med. Genet. 65, 332–336 (1996).
pubmed: 8923945
doi: 10.1002/(SICI)1096-8628(19961111)65:4<332::AID-AJMG16>3.0.CO;2-V
Cereda, A. & Carey, J. C. The trisomy 18 syndrome. Orphanet J. Rare Dis. 7, 1–4 (2012).
doi: 10.1186/1750-1172-7-81
Botezatu, B. & Marinescu, B. 21 weeks fetus with trisomy 18 (Edward syndrome), bone malformations highlighted. Proc. Rom. Acad. Ser. B. 14, 191–195 (2012).
Edwards, J. H., Harnden, D. G., Cameron, A. H., Crosse, V. M. & Wolf, O. H. A new trisomic syndrome. Lancet 275, 787–790 (1960).
doi: 10.1016/S0140-6736(60)90675-9
Blazek, J. D. et al. Abnormal mineralization of the Ts65Dn Down syndrome mouse appendicular skeleton begins during embryonic development in a Dyrk1a-independent manner. Mech. Dev. 136, 133–142 (2015).
pubmed: 25556111
doi: 10.1016/j.mod.2014.12.004
Richtsmeier, J. T., Baxter, L. L. & Reeves, R. H. Parallels of craniofacial maldevelopment in Down syndrome and Ts65Dn mice. Dev. Dyn. 217, 137–145 (2000).
pubmed: 10706138
doi: 10.1002/(SICI)1097-0177(200002)217:2<137::AID-DVDY1>3.0.CO;2-N
Goodfellow, L. R., Earl, S., Cooper, C. & Harvey, N. C. Maternal diet, behaviour and offspring skeletal health. Int. J. Environ. Res. Public Health 7, 1760–1772 (2010).
pubmed: 20617058
pmcid: 2872349
doi: 10.3390/ijerph7041760
Bowden, L. S., Jones, C. J. & Ryan, S. W. Bone mineralisation in ex-preterm infants aged 8 years. Eur. J. Pediatr. 158, 658–661 (1999).
pubmed: 10445346
doi: 10.1007/s004310051171
Fidler, D. J. The emerging Down syndrome behavioral phenotype in early childhood: Implications for practice. Infants Young Child 18, 86–103 (2005).
doi: 10.1097/00001163-200504000-00003
Roper, R. J. & Reeves, R. H. Understanding the basis for Down syndrome phenotypes. PLoS Genet. 2, e50 (2006).
pubmed: 16596169
pmcid: 1420680
doi: 10.1371/journal.pgen.0020050
Tilley, L. A. Towards a Bioarchaeology of Care: A Contextualised Approach for Identifying and Interpreting Health-Related Care Provision in Prehistory [Doctoral dissertation, Australian National University]. (2013).
Tilley, L. & Oxenham, M. F. Survival against the odds: modeling the social implications of care provision to seriously disabled individuals. Int. J. Paleopathol. 1, 35–42 (2011).
pubmed: 29539340
doi: 10.1016/j.ijpp.2011.02.003
Tilley, L. & Schrenk, A. A. Introduction: new developments in the bioarchaeology of care. New developments in the bioarchaeology of care: Further case studies and expanded theory (Springer, 2017).
Altuna, M., Giménez, S. & Fortea, J. Epilepsy in Down syndrome: a highly prevalent comorbidity. J. Clin. Med. Res. 10, 2776 (2021).
Ērkšķe, A. The children are missing! Some thoughts on the underrepresentation of non-adult burials in Latvian Iron Age cemeteries. Eest. Arheol. Ajak. 24, 161–189 (2020).
Bocquet, J. P. & Masset, C. Estimateurs en paléodémographie. L’homme 1, 65–90 (1977).
Séguy, I. & Buchet, L. Handbook of Palaeodemography (Springer Science & Business Media, 2014).
Papac, L. et al. in Kinship, Sex, and Biological Relatedness. The Contribution of Archaeogenetics to the Understanding of Social and Biological Relations (eds Meller, H., Krause, J., Haak, W., Risch, R.) 263–296 (Landesamt für Denkmalpflege und Archäologie Sachsen-Anhalt, 2023).
Anastasiadou K, et al. Detection of chromosomal aneuploidy in ancient genomes. Commun. Biol. 7, 14 (2024).
Papadakis, M., Tsagris, M., Dimitriadis, M. & Fafalios, S. Rfast: a collection of efficient and extremely fast R functions. R package version 2.0.9 (CRAN, 2023).
Wolodzko, T. extraDistr: additional univariate and multivariate distributions. R package version 1.9.1 (CRAN, 2019).
Wickham, H. in ggplot2: Elegant Graphics for Data Analysis (ed. Wickham, H.) 189–201 (Springer International Publishing, 2016).
Roca-Rada, X. et al. A 1000-year-old case of Klinefelter’s syndrome diagnosed by integrating morphology, osteology, and genetics. Lancet 400, 691–692 (2022).
pubmed: 36030812
doi: 10.1016/S0140-6736(22)01476-3
Fazekas, I. G. & Kósa, F. Forensic Fetal Osteology (Akadémiai Kiadó, 1978).
Jeanty, P. Fetal limb biometry. Radiology 147, 601–602 (1983).
pubmed: 6836145
doi: 10.1148/radiology.147.2.6836145
Scheuer, J. L., Musgrave, J. H. & Evans, S. P. The estimation of late fetal and perinatal age from limb bone length by linear and logarithmic regression. Ann. Hum. Biol. 7, 257–265 (1980).
pubmed: 7425553
doi: 10.1080/03014468000004301
Baker, B. J., Dupras, T. L. & Tocheri, M. W. The Osteology of Infants and Children (Texas A&M University Press, 2005).
Schaefer, M., Black, S. M., Schaefer, M. C. & Scheuer, L. Juvenile Osteology (Academic Press, 2009).
Cunningham, C., Scheuer, L. & Black, S. Developmental Juvenile Osteology (Academic Press, 2016).
Rohrlach, A. B. Cases of trisomy 21 and trisomy 18 among historic and prehistoric individuals discovered from ancient DNA. BenRohrlach/TrisomyAncientDNAStudy. https://doi.org/10.5281/zenodo.10208185 (2023).