Original articleHibernation in hominins from Atapuerca, Spain half a million years agoHibernation des hominidés d’Atapuerca, en Espagne, il y a un demi-million d’années☆
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:
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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;
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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;
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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
References (200)
- et al.
The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study
J. Hum. Evol.
(1997) - et al.
Craniosynostosis
Clin. Radiol.
(2002) - et al.
Homo antecessor: the state of the art eighteen years later
Quat. Int.
(2017) - et al.
Multiple skeletal complications in a case of chronic renal failure treated by kidney homotransplantation
Am. J. Med.
(1971) - et al.
New bracketing luminescence ages constrain the Sima de los Huesos hominin fossils (Atapuerca, Spain) to MIS 12
J. Hum. Evol.
(2019) - et al.
Oral manifestations of secondary hyperparathyroidism related to long-term hemodialysis therapy
Oral Surg. Oral Med. Oral Pathol.
(1977) - et al.
Metric and morphological study of the upper cervical spine from the Sima de los Huesos site (Sierra de Atapuerca, Burgow, Spain
J. Hum. Evol.
(2007) - et al.
The adrenal cortex during activity and hibernation in the male little brown bat, Myotis lucifugus ludifugus: annual rhythm of plasma cortisol levels
Gen. Comp. Endocrinol.
(1981) - et al.
Periarticular erosions in the hands and wrists in haemodialysis patients
Clin. Radiol.
(1982) - et al.
MIS 21 and the Mid-Pleistocene climate transition: climate and sea-level variation from a sediment core in Osaka Bay, Japan
Palaeogeogr. Palaeoclimatol. Palaeoecol.
(2011)
Paleoecology of Bears from MIS 8–MIS 3 Deposits of Biśnik Cave Based on Stable Isotopes (δ13C, δ18O) and Dental Cementum Analyses
Quat. Int.
Radiology of Rickets and Osteomalacia
Bone Diseases
Neanderthals, energetics and evolution. Symposium 150 years of Neanderthal discoveries
Terra Nostra
Early Arctic settlements in North America
Sci. Am.
Evolution of Uric Acid Metabolism in Humans
Neanderthal roots: cranial and chronological evidence from Sima de los Huesos
Science
Postcranial morphology of the middle Pleistocene humans from Sima de los Huesos, Spain
PNAS
Human Paleopathology
Human dental development and vitamin D
Hibernation, puberty and chronic kidney disease in troglodytes from Spain half a million years ago
PeerJPreprints
The eye injury of King Philip II and the skeletal evidence from the Royal Tomb II at Vergina
Science
Brown tumor as a complication of secondary hyperparathyroidism in severe long-lasting vitamin D deficiency rickets
Eur. J. Pediatr.
The Atapuerca sites and their contribution to the knowledge of human evolution in Europe
Evol. Anthrop.
Patterns of dental development in Lower and Middle Pleistocene Hominins from Atapuerca (Spain)
The Sima de los Huesos Middle Pleistocene hominin site (Burgos, Spain). Estimation of the number of individuals
Anat. Rec.
The lore and the lure o’ the lamina dura
Radiology
H2S induces a suspended animation-like state in mice
Science
Tropical heterothermy is “cool”: the expression of daily torpor and hibernation in primates
Evol. Anthropol.
Etiologic and positive diagnosis of craniosynostosis. ISSN
Zur Anatomie, Pathologie und Histologie der Zahne und der Kiefer von Ursus spelaeus
Molecular adaptations in mammalian hibernators: unique adaptations or generalized responses?
J. Appl. Physiol.
The bioarchaeology of metabolic bone disease
Renal function in anesthetized dormant and active bears
Am. J. Physiol.
Sizing the Jurassic Theropod Dinosaur Allosaurus: assessing growth strategy and evolution of ontogenetic scaling of limbs
J. Morphol.
Pedriatic X-Ray Diagnosis
Mammalian hibernation: cellular and molecular responses to depressed metabolism and low temperature
Physiol. Rev.
Adaptation and evolution in Gallotia lizards from the Canary islands: age, growth, maturity and longevity
Amphibia-Reptilia
Effects of 1,25-dihydroxyvitamin-D3 on renal function, mineral balance, and growth in children with severe chronic renal failure
Pediatrics
Polar dinosaur histology
J. Vert. Paleont.
The role of endocrines in the self-regulation of mammalian populations
Recent Prog. Hormone Res.
Serum markers of bone metabolism show bone loss in hibernating bears
Clin. Orthop. Rel. Res.
Craniosynostosis update 1987
Am. J. Med. Genet. Suppl.
Age estimation of pteropodid bats (Megachiroptera) from hard tissue parameters
Aust. Wildlife Res.
Fossil population structure and mortality of the cave bear from the Mokrica cave (North Slovenia)
Acta Carsol.
Medical problems from cold exposure
Am. Fam. Physician
Social responses during severe food shortages and famine
Curr. Anthropol.
Primary hyperparathyroidism and articular cartilage calcification
Am. J. Roentgenol.
Parathyroid hormone may maintain bone formation in hibernating black bears (Ursus americanus) to prevent disuse osteoporosis
J Exp Biol
Serum markers of bone metabolism show bone loss in hibernating bears
Clin. Orthop. Rel. Res.
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A preliminary report of thispaper has appeared as a preprintin PeerJ: Bartsiokas A & Arsuaga JL 2018. Hibernation, puberty and chronic kidney disease in troglodytes from Spain half a million years ago. PeerJPreprints 6:e27370vl https://doi.org/10.7287/peerj.preprints.27370vl.