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Early Life of Neanderthals

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Early Life of Neanderthals Early life of Neanderthals Alessia Navaa,b,1,2, Federico Luglic,d,1,2, Matteo Romandinic,e, Federica Badinoc,f, David Evansg,h, Angela H. Helblingg,h, Gregorio Oxiliac, Simona Arrighic, Eugenio Bortolinic, Davide Delpianoi, Rossella Duchesj, Carla Figusc, Alessandra Livraghii,k, Giulia Marcianic, Sara Silvestrinic, Anna Ciprianid,l, Tommaso Giovanardid, Roberta Pinif, Claudio Tunizm,n,o, Federico Bernardinim,n, Irene Dorip,q, Alfredo Coppar,s,t, Emanuela Cristiania, Christopher Deanu,v, Luca Bondioliw,x, Marco Peresanif,i,2, Wolfgang Müllerg,h,2, and Stefano Benazzic,y,2 aDANTE–Diet and Ancient Technology Laboratory, Department of Maxillo-Facial Sciences, Sapienza University of Rome, 00161 Rome, Italy; bSkeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury CT2 7NZ, United Kingdom; cDepartment of Cultural Heritage, University of Bologna, 48121 Ravenna, Italy; dDepartment of Chemical and Geological Sciences, University of Modena and Reggio Emilia, 41125 Modena, Italy; ePradis Cave Museum, 33090 Clauzetto, Italy; fInstitute of Environmental Geology and Geoengineering–IGAG CNR, 20131 Milan, Italy; gInstitute of Geosciences, Goethe University Frankfurt, 60438 Frankfurt am Main, Germany; hFrankfurt Isotope and Element Research Center (FIERCE), Goethe University Frankfurt, 60438 Frankfurt am Main, Germany; iDepartment of Humanities, 44121 Ferrara, University of Ferrara, Italy; jPrehistory Section–MuSe, Museum of Science, 38122 Trento, Italy; kArea de Prehistoria, University Rovira i Virgili, 43002 Tarragona, Spain; lLamont-Doherty Earth Observatory of Columbia University, Palisades, NY 10964-1000; mMultidisciplinary Laboratory, Abdus Salam International Centre for Theoretical Physics, 34151 Trieste, Italy; nCentro Fermi, Museo Storico della Fisica e Centro di Studi e Ricerche Enrico Fermi, 00184 Roma, Italy; oCenter for Archaeological Science, University of Wollongong, Wollongong, NSW 2522, Australia; pSoprintendenza Archeologia, Belle Arti e Paesaggio per le province di Verona, Rovigo e Vicenza, 37121 Verona, Italy; qDepartment of Biology, Laboratory of Anthropology, University of Florence, 50122 Florence, Italy; rDepartment of Environmental Biology, Sapienza University of Rome, 00185 Rome, Italy; sDepartment of Genetics, Harvard Medical School, Boston, MA 02115; tDepartment of Evolutionary Anthropology, University of Vienna, 1090 Vienna, Austria; uDepartment of Earth Sciences, Natural History Museum, London SW7 5BD, United Kingdom; vDepartment of Cell and Developmental Biology, University College London, London WC1E 6BT, United Kingdom; wBioarchaeology Service, Museum of Civilization, 00144 Rome, Italy; xDepartment of Cultural Heritage, University of Padua, 35139 Padua, Italy; and yDepartment of Human Evolution, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany Edited by Noreen Tuross, Harvard University, Cambridge, MA, and accepted by Editorial Board Member Richard G. Klein September 21, 2020 (received for review June 8, 2020) The early onset of weaning in modern humans has been linked to growth in a 7-y-old Neanderthal from El Sidròn (Spain; 49 ka) the high nutritional demand of brain development that is inti- indicated that Neanderthals and modern humans were similar in mately connected with infant physiology and growth rate. In terms of ontogenetic development, with only small-scale dissimi- Neanderthals, ontogenetic patterns in early life are still debated, larities in acceleration or deceleration of skeletal maturation (9). ANTHROPOLOGY with some studies suggesting an accelerated development and Finally, other work suggested that the early growth of the Nean- others indicating only subtle differences vs. modern humans. Here derthal brain was as fast as in modern humans with similar en- we report the onset of weaning and rates of enamel growth using ergetic demands (10). Maps of Ba/Ca ratios of permanent tooth an unprecedented sample set of three late (∼70 to 50 ka) Nean- derthals and one Upper Paleolithic modern human from northeast- Significance ern Italy via spatially resolved chemical/isotopic analyses and histomorphometry of deciduous teeth. Our results reveal that the modern human nursing strategy, with onset of weaning at 5 The extent to which Neanderthals differ from us is the focus of EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES to 6 mo, was present among these Neanderthals. This evidence, many studies in human evolution. There is debate about their combined with dental development akin to modern humans, high- pace of growth and early-life metabolic constraints, both of lights their similar metabolic constraints during early life and ex- which are still poorly understood. Here we use chemical and cludes late weaning as a factor contributing to Neanderthals’ isotopic patterns in tandem with enamel growth rates of three demise. Neanderthal milk teeth from northeastern Italy to explore the early life of these individuals. Our study shows that these Neanderthals started to wean children at 5 to 6 months, akin to Neanderthal ontogeny | nursing strategy | dental histology | spatially modern humans, implying similar energy demands during early resolved chemical analyses | life histories infancy. Dental growth rates confirm this and follow trajecto- ries comparable with modern humans. Contrary to previous aternal physiology, breastfeeding, and the first introduc- evidence, we suggest that differences in weaning age did not Mtion of supplementary foods are key determinants of hu- contribute to Neanderthals’ demise. man growth (1). The high nutritional demands of the human brain during the first years of life has been identified as the main Author contributions: A.N., F.L., M.R., C.D., L.B., M.P., W.M., and S.B. designed research; reason for the early weaning onset in modern humans (2, 3). A.N., F.L., D.E., A.H.H., S.S., A. Cipriani, T.G., C.D., L.B., W.M., and S.B. performed research; Indeed, supplementary food is needed when an infant’s nutri- S.A., D.D., R.D., C.F., A.L., G.M., R.P., C.T., F. Bernardini, I.D., A. Coppa, and E.C. contributed new reagents/analytic tools; A.N., F.L., D.E., A.H.H., G.O., E.B., L.B., W.M., and S.B. ana- tional requirements exceed what the mother can provide through lyzed data; A.N., F.L., M.R., F. Badino, D.E., C.D., L.B., M.P., W.M., and S.B. wrote the paper; breastmilk only (4), and this dietary development can introduce M.R., D.D., R.D., A.L., and M.P. coordinated archaeological excavations; F. Badino and R.P. foods that are higher in protein, calories, and key micronutrients produced ecological framework; A.H.H. and A. Cipriani revised the manuscript; G.O., S.A., than maternal milk (4, 5). Weaning onset occurs in contempo- C.F., G.M., I.D., A. Coppa, and E.C. curated, sampled and/or described analyzed teeth; and C.T. and F. Bernardini produced the microtomographic record. rary nonindustrial human societies at a modal age of 6 mo (6). The authors declare no competing interest. At present, our knowledge about the link between the pace of This article is a PNAS Direct Submission. N.T. is a guest editor invited by the Editorial child growth, maternal behavior, and the onset of weaning among Board. Neanderthals is still limited. Previous work based on permanent Published under the PNAS license. teeth from eight Neanderthal specimens reported that Neander- 1A.N. and F.L. contributed equally to this work. thal tooth crowns tend to develop faster than in modern humans, 2To whom correspondence may be addressed. Email: [email protected], federico. suggesting infant growth was generally accelerated (7). However, a [email protected], [email protected], [email protected], or stefano. permanent first molar and a second deciduous molar from La [email protected]. Chaise (France; 127 to 116 ka and <163 ka, respectively) placed This article contains supporting information online at https://www.pnas.org/lookup/suppl/ rates of Neanderthal tooth growth within the range of modern doi:10.1073/pnas.2011765117/-/DCSupplemental. humans (8). Equally, the association between dental and skeletal First published November 2, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2011765117 PNAS | November 17, 2020 | vol. 117 | no. 46 | 28719–28726 Downloaded by guest on September 26, 2021 sections of two early Neanderthals (Payre 6, 250 ka; and Scladina, dentine junction (EDJ) by laser-ablation inductively coupled 120 ka) have been interpreted (controversially; see below) as in- plasma mass spectrometry (LA-ICPMS) (15). In order to detect dicators of weaning onset at ∼9mo(11)and7mo(12)ofage, mobility and/or potential nonlocal food sources in maternal diet, respectively, later than the modal age in contemporary humans 87Sr/86Sr isotope ratio profiles were measured by LA multi- (6). Similarly, wear-stage analyses of a large number of deciduous collector ICPMS (Materials and Methods) (16, 17). Moreover, we dentitions suggested that introduction of solid food in Neander- evaluated elemental ratio profiles in teeth from children with thals was delayed by 1 y compared to modern humans (13). known life history (SI Appendix,TextS3)(15). Here we investigate such key aspects of early life in Nean- derthals by combining new data on chemical detection of Results weaning onset with deciduous enamel growth rates. We utilize The neonatal lines marking birth were visible in all four ar- dental histomorphometry (8, 14) and spatially resolved chemical chaeological specimens, despite their worn crowns (SI Appendix, (15) and isotopic profiles (16, 17) of
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