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An integrative skeletal and paleogenomic analysis of prehistoric stature variation suggests relatively reduced health for early European farmers

Stephanie Marciniak, Christina M. Bergey, Ana Maria Silva, Agata Hałuszko, Mirosław Furmanek, Barbara Veselka, Petr Velemínský, Giuseppe Vercellotti, Joachim Wahl, Gunita Zariņa, Cristina Longhi, Jan Kolář, Rafael Garrido-Pena, Raúl Flores-Fernández, Ana M. Herrero-Corral, Angela Simalcsik, Werner Müller, Alison Sheridan, Žydrūnė Miliauskienė, Rimantas Jankauskas, Vyacheslav Moiseyev, Kitti Köhler, Ágnes Király, Beatriz Gamarra, Olivia Cheronet, Vajk Szeverényi, Viktoria Kiss, Tamás Szeniczey, Krisztián Kiss, Zsuzsanna K. Zoffmann, Judit Koós, Magdolna Hellebrandt, László Domboróczki, Cristian Virag, Mario Novak, David Reich, Tamás Hajdu, Noreen von Cramon-Taubadel, Ron Pinhasi, George H. Perry
doi: https://doi.org/10.1101/2021.03.31.437881
Stephanie Marciniak
1Department of Anthropology, Pennsylvania State University
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  • For correspondence: ghp3@psu.edu szm316@psu.edu
Christina M. Bergey
1Department of Anthropology, Pennsylvania State University
2Department of Genetics, Human Genetics Institute of New Jersey, Rutgers, The State University of New Jersey
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Ana Maria Silva
3CIAS, Department of Life Sciences, University of Coimbra; UNIARQ, University of Lisbon; CEF, University of Coimbra
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Agata Hałuszko
4Institute of Archaeology, University of Wroclaw
5Archeolodzy.org Foundation
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Mirosław Furmanek
4Institute of Archaeology, University of Wroclaw
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Barbara Veselka
6Department of Chemistry, Analytical Environmental and Geo-Chemistry Research Unit, Vrije Univeristeit Brussel
7Department of Art Studies and Archaeology, Maritime Cultures Research Institute, Vrije Univeristeit Brussel
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Petr Velemínský
8Department of Anthropology, Prague Natural History Museum
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Giuseppe Vercellotti
9Department of Anthropology, Ohio State University
10Institute for Research and Learning in Archaeology and Bioarchaeology
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Joachim Wahl
11Institute for Scientific Archaeology, WG Palaeoanthropology, University of Tübingen
12State Office for Cultural Heritage Management Baden-Württemberg, Osteology
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Gunita Zariņa
13Institute of Latvian History, University of Latvia
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Cristina Longhi
14Soprintendenza Archeologia, Belle Arti e Paesaggio
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Jan Kolář
15Department of Vegetation Ecology, Institute of Botany of the Czech Academy of Sciences
16Institute of Archaeology and Museology, Masaryk University
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Rafael Garrido-Pena
17Department of Prehistory and Archaeology, Universidad Autónoma de Madrid
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Raúl Flores-Fernández
18Independent archaeologist
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Ana M. Herrero-Corral
19Department of Prehistory, Universidad Complutense de Madrid
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Angela Simalcsik
20Olga Necrasov Center for Anthropological Research, Romanian Academy, Iasi branch
21Orheiul Vechi Cultural-Natural Reserve
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Werner Müller
22Laboratoire d’archéozoologie, Université de Neuchâtel
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Alison Sheridan
23Department of Scottish History & Archaeology, National Museums Scotland
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Žydrūnė Miliauskienė
24Department of Anatomy, Histology and Anthropology, Vilnius University
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Rimantas Jankauskas
24Department of Anatomy, Histology and Anthropology, Vilnius University
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Vyacheslav Moiseyev
25Department of Physical Anthropology, Kunstkamera, Peter the Great Museum of Anthropology and Ethnography, Russian Academy of Sciences
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Kitti Köhler
26Institute of Archaeology, Research Centre for the Humanities, Hungarian Academy of Sciences
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Ágnes Király
26Institute of Archaeology, Research Centre for the Humanities, Hungarian Academy of Sciences
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Beatriz Gamarra
27Institut Català de Paleoecologia Humana i Evolució Social (IPHES-CERCA)
28Universitat Rovira i Virgili, Departament d’Història i Història de l’Art
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Olivia Cheronet
29Department of Evolutionary Anthropology, University of Vienna
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Vajk Szeverényi
30Déri Múzeum, Debrecen
31Institute of Archaeology, Research Centre for the Humanities, Budapest
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Viktoria Kiss
31Institute of Archaeology, Research Centre for the Humanities, Budapest
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Tamás Szeniczey
32Department of Biological Anthropology, Eötvös Loránd University
33Department of Anthropology, Hungarian Natural History Museum
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Krisztián Kiss
32Department of Biological Anthropology, Eötvös Loránd University
33Department of Anthropology, Hungarian Natural History Museum
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Zsuzsanna K. Zoffmann
33Department of Anthropology, Hungarian Natural History Museum
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Judit Koós
34Herman Ottó Museum, Miskolc
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Magdolna Hellebrandt
34Herman Ottó Museum, Miskolc
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László Domboróczki
35István Dobó Castle Museum, Eger
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Cristian Virag
36Satu Mare County Museum
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Mario Novak
37Centre for Applied Bioanthropology, Institute for Anthropological Research, Zagreb
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David Reich
38Department of Genetics, Harvard Medical School
39The Max Planck-Harvard Research Center for the Archaeoscience of the Ancient Mediterranean
40Department of Human Evolutionary Biology, Harvard University
41Broad Institute of Harvard and MIT
42Howard Hughes Medical Institute, Harvard Medical School
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Tamás Hajdu
32Department of Biological Anthropology, Eötvös Loránd University
33Department of Anthropology, Hungarian Natural History Museum
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Noreen von Cramon-Taubadel
43Buffalo Human Evolutionary Morphology Lab, Department of Anthropology, University at Buffalo
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Ron Pinhasi
29Department of Evolutionary Anthropology, University of Vienna
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George H. Perry
1Department of Anthropology, Pennsylvania State University
44Department of Biology, Pennsylvania State University
45Huck Institutes of the Life Sciences, Pennsylvania State University
46DFG Center for Advanced Studies, University of Tübingen
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  • For correspondence: ghp3@psu.edu szm316@psu.edu
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Abstract

Human culture, biology, and health were shaped dramatically by the onset of agriculture ~12,000 years before present (BP). Subsistence shifts from hunting and gathering to agriculture are hypothesized to have resulted in increased individual fitness and population growth as evidenced by archaeological and population genomic data alongside a simultaneous decline in physiological health as inferred from paleopathological analyses and stature reconstructions of skeletal remains. A key component of the health decline inference is that relatively shorter statures observed for early farmers may (at least partly) reflect higher childhood disease burdens and poorer nutrition. However, while such stresses can indeed result in growth stunting, height is also highly heritable, and substantial inter-individual variation in the height genetic component within a population is typical. Moreover, extensive migration and gene flow were characteristics of multiple agricultural transitions worldwide. Here, we consider both osteological and ancient DNA data from the same prehistoric individuals to comprehensively study the trajectory of human stature variation as a proxy for health across a transition to agriculture. Specifically, we compared ‘predicted’ genetic contributions to height from paleogenomic data and ‘achieved’ adult osteological height estimated from long bone measurements on a per-individual basis for n=160 ancient Europeans from sites spanning the Upper Paleolithic to the Iron Age (~38,000-2,400 BP). We found that individuals from the Neolithic were shorter than expected (given their individual polygenic height scores) by an average of −4.47 cm relative to individuals from the Upper Paleolithic and Mesolithic (P=0.016). The average osteological vs. expected stature then increased relative to the Neolithic over the Copper (+2.67 cm, P=0.052), Bronze (+3.33 cm, P=0.032), and Iron Ages (+3.95 cm, P=0.094). These results were partly attenuated when we accounted for genome-wide genetic ancestry variation in our sample (which we note is partly duplicative with the individual polygenic score information). For example, in this secondary analysis Neolithic individuals were −3.48 cm shorter than expected on average relative to individuals from the Upper Paleolithic and Mesolithic (P=0.056). We also incorporated observations of paleopathological indicators of non-specific stress that can persist from childhood to adulthood in skeletal remains (linear enamel hypoplasia, cribra orbitalia, and porotic hyperostosis) into our model. Overall, our work highlights the potential of integrating disparate datasets to explore proxies of health in prehistory.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵† Deceased

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY 4.0 International license.
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An integrative skeletal and paleogenomic analysis of prehistoric stature variation suggests relatively reduced health for early European farmers
Stephanie Marciniak, Christina M. Bergey, Ana Maria Silva, Agata Hałuszko, Mirosław Furmanek, Barbara Veselka, Petr Velemínský, Giuseppe Vercellotti, Joachim Wahl, Gunita Zariņa, Cristina Longhi, Jan Kolář, Rafael Garrido-Pena, Raúl Flores-Fernández, Ana M. Herrero-Corral, Angela Simalcsik, Werner Müller, Alison Sheridan, Žydrūnė Miliauskienė, Rimantas Jankauskas, Vyacheslav Moiseyev, Kitti Köhler, Ágnes Király, Beatriz Gamarra, Olivia Cheronet, Vajk Szeverényi, Viktoria Kiss, Tamás Szeniczey, Krisztián Kiss, Zsuzsanna K. Zoffmann, Judit Koós, Magdolna Hellebrandt, László Domboróczki, Cristian Virag, Mario Novak, David Reich, Tamás Hajdu, Noreen von Cramon-Taubadel, Ron Pinhasi, George H. Perry
bioRxiv 2021.03.31.437881; doi: https://doi.org/10.1101/2021.03.31.437881
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An integrative skeletal and paleogenomic analysis of prehistoric stature variation suggests relatively reduced health for early European farmers
Stephanie Marciniak, Christina M. Bergey, Ana Maria Silva, Agata Hałuszko, Mirosław Furmanek, Barbara Veselka, Petr Velemínský, Giuseppe Vercellotti, Joachim Wahl, Gunita Zariņa, Cristina Longhi, Jan Kolář, Rafael Garrido-Pena, Raúl Flores-Fernández, Ana M. Herrero-Corral, Angela Simalcsik, Werner Müller, Alison Sheridan, Žydrūnė Miliauskienė, Rimantas Jankauskas, Vyacheslav Moiseyev, Kitti Köhler, Ágnes Király, Beatriz Gamarra, Olivia Cheronet, Vajk Szeverényi, Viktoria Kiss, Tamás Szeniczey, Krisztián Kiss, Zsuzsanna K. Zoffmann, Judit Koós, Magdolna Hellebrandt, László Domboróczki, Cristian Virag, Mario Novak, David Reich, Tamás Hajdu, Noreen von Cramon-Taubadel, Ron Pinhasi, George H. Perry
bioRxiv 2021.03.31.437881; doi: https://doi.org/10.1101/2021.03.31.437881

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