Elsevier

L'Anthropologie

Volume 124, Issue 5, December 2020, 102797
L'Anthropologie

Original article
Hibernation in hominins from Atapuerca, Spain half a million years agoHibernation des hominidés d’Atapuerca, en Espagne, il y a un demi-million d’années

https://doi.org/10.1016/j.anthro.2020.102797Get rights and content

Abstract

Both animal hibernation and human renal osteodystrophy are characterized by high levels of serum parathyroid hormone. To test the hypothesis of hibernation in an extinct human species, we examined the hominin skeletal collection from Sima de los Huesos, Cave Mayor, Atapuerca, Spain, for evidence of hyperparathyroidism after a thorough review of the literature. We studied the morphology of the fossilized bones by using macrophotography, microscopy, histology and CT scanning. We found trabecular tunneling and osteitis fibrosa, subperiosteal resorption, ‘rotten fence post’ signs, brown tumours, subperiosteal new bone, chondrocalcinosis, rachitic osteoplaques and empty gaps between them, craniotabes, and beading of ribs mostly in the adolescent population of these hominins. Since many of the above lesions are pathognomonic, these extinct hominins suffered annually from renal rickets, secondary hyperparathyroidism, and renal osteodystrophy associated with Chronic Kidney Disease - Mineral and Bone Disorder (CKD-MBD). We suggest these diseases were caused by poorly tolerated hibernation in dark cavernous hibernacula. This is particularly evidenced by the rachitic osteoplaques and the gaps between them in some of the adolescent individuals along with the evidence of healing mainly in the adults. The sublayers in the rachitic osteoplaques indicate bouts of arousal from hibernation. The strong projection of the external lip of the femoral trochlea, the rachitic osteoplaques with the empty gaps between them, the “rotten fence post" sign, and the evidence of annual healing also point to the presence of annually intermittent puberty in this extinct human species. The hypothesis of hibernation is consistent with the genetic evidence and the fact that the SH hominins lived during an extreme glaciation. Alternative hypotheses are examined. The present work will provide a new insight into the physiological mechanism of early human metabolism which could help in determining the life histories and physiologies of extinct human species.

Résumé

Les périodes d’hibernation chez l’animal et l’ostéodystrophie rénale en pathologie humaine sont associées à des taux sériques élevés d’hormone parathyroïdienne. Après une revue approfondie de la littérature, nous avons examiné la collection de squelettes d’hominidés de Sima de los Huesos, Cave Mayor, Atapuerca, Espagne, pour y rechercher des traces d’hypersécrétion parathyroïdienne. L’étude a été réalisée en associant macrophotographie, analyses microscopiques, histologiques et imagerie par tomodensitométrie. Nous avons observé principalement dans la population adolescente de ces homininés des aspects de tunnelisation osseuse trabéculaire, d’ostéite fibreuse, de résorption sous-périostée métaphysaire, de tumeurs brunes, d’ossification sous-périosté, de chondrocalcinose, des ostéophytes disséminés, de craniotabès et de perles costales. Plusieurs de ces lésions sont pathognomoniques et montrent que ces hominines étaient atteints chaque année d’ostéomalacie, d’hyperparathyroïdie secondaire et d’ostéodystrophie rénale. Nous estimons que ces troubles sont consécutifs à une hibernation dans des grottes sombres. Ceci est particulièrement mis en évidence par la présence de plaques osseuses rachitiques disséminées chez certains des adolescents, et de lésions cicatrisées principalement chez les adultes. Les sous-couches dans les plaques osseuses rachitiques indiquent des épisodes de suractivité liée à l’hibernation. La forte saillie de la lèvre externe de la trochlée fémorale, les plaques osseuses rachitiques séparées par des zones normales, les zones de résorption sous-périostée et les preuves de guérison annuelle indiquent également la présence d’une puberté intermittente chaque année chez cette espèce humaine disparue. Notre hypothèse rattachant ces lésions osseuses aux conséquences de l’hibernation est cohérente avec les arguments génétiques et le fait que les hominidés de SH ont vécu pendant une glaciation extrême. Des hypothèses alternatives sont examinées. Le présent travail apporte une approche novatrice des mécanismes physiologique du métabolisme des premiers humains qui pourrait aider à déterminer le cycle de vie et la physiologie des espèces humaines éteintes.

Section snippets

Abbreviations

    ROD

    Renal Osteodystrophy

    PTH

    Parathyroid Hormone

    2HPT

    Secondary Hyperparathyroidism

    1HPT

    Primary Hyperparathyroidism

    OF

    Osteitis Fibrosa Cystica

    OM

    Osteomalacia

    SH

    Sima de los Huesos

    LD

    Lamina dura

    CKD-MBD

    Chronic Kidney Disease - Mineral and Bone Disorder

    BT

    Brown Tumor

    BAT

    Brown Adipose Tissue

    BeAT

    Beige Adipose Tissue

    GI

    Gastrointestinal

    PNB

    Subperiosteal new bone

    SPR

    Subperiosteal resorption

    ROP

    Rachitic Osteoplaque

    CPPD

    Calcium pyrophosphate dihydrate disease

    HZAG

    Hibernational Zone of Arrested Growth

Materials and Methods

We used most of the Sima de los Huesos (SH) enormous collection of fossilized bones. SH has been excavated since 1983 with every year producing more human fossils. So far, more than 7,500 fossil human skeletal remains have been found. A large number of them were inspected and sorted out regarding the presence of any metabolic diseases. Only a few of them have been presented here with the most interesting and representative lesions (Table 1). No quantitative data can be presented as it is not

Results and Discussion

The results are summarized in Table 1, Table 2, and Fig. 1, Fig. 2, Fig. 3, Fig. 4, Fig. 5, Fig. 6, Fig. 7, Fig. 8, Fig. 9, Fig. 10, Fig. 11, Fig. 12, Fig. 13, Fig. 14, Fig. 15, Fig. 16, Fig. 17, Fig. 18. A detail description and identification of the lesions follows.

Evidence for CKD-MBD

Most of the lesions we mentioned in SH are pathognomonic. For instance, Osteitis Fibrosa (OF) in the trabeculae is pathognomonic of 2HPT, ROD and CKD-MBD. Rachitic hyperostosis is pathognomonic of rickets. The supraorbital area (Fig. 4, Fig. 5) bears 4 osteoplaques evidence of episodic disease. These are rachitic osteoplaques (ROPs) but their detailed histology is different from that presented by Schultz (2003) as in essence he refers to one spongy osteophyte whereas here the osteoplaques

The climate in the Iberian peninsula would not be severe enough to encourage hibernation in a hominin such as that of SH

The SH hominins lived during the Marine Isotope Stage (MIS) 12 and have an age of 448 ± 15ka (Demuro et al., 2019). This severe glacial period was the most extreme glaciation during the last 1 million years characterized by aridification of Iberia, low vegetation cover and rapid snowmelt (Demuro et al., 2019) which all imply food scarcity of the SH hominins. These conditions would have been even more pronounced in the high elevation of the SH locality of at least 1000 masl. Thus, the above

The physiological mechanism and the reconstruction of life history in the SH hominins

The rachitic metaphysis and the gaps (HZAGs) are evidence of hypocalcemia, osteoid formed in constant darkness due to cavernous conditions and hypercortisolism due to cold. The resultant increases in PTH may account for the pathologies described in fossil bears, living hibernators, and the SH hominins.

Thus, the simplified mechanism in poorly tolerated hibernation for cave-overwintering hominins during extreme glacial times as in SH would have been as follows: frigid conditions and food scarcity

Conclusions

Because:

  • the SH hominins lived in high-altitude caves during the most severe glaciation in the last 1 million years and their genetics is consistent with this;

  • the SH bears were hibernatiing in order to survive in that frigid environment, the SH hominins would have to do the same since they were found in the same fossil horizon (LU-6) and context with that of the SH bears;

  • hibernating cave conditions, such as constant darkness, winter famine and cold can trigger a series of metabolic pathways

Acknowledgments

Our thanks are due to the late Don Ortner, who confirmed our diagnosis of rickets in Cranium 9. Drs Ana Gracia-Téllez and Jose Miguel Carretero for their assistance. The Department of History & Ethnology of the Democritus University of Thrace for granting one of us (A.B.) a sabbatical for the spring semester of 2006 in order to undertake this study. This study was financed by Ministerio de Economía y Competitividad, Spain Project PGC2018-093925-B-C33 (MCIU/AEI/FEDER, UE). The field work at the

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