Several lines of bioarchaeological research have confirmed the gradual decline in lower limb loading among past human populations, beginning with the transition to agriculture. The goal of this study was to assess whether human tibial curvature reflects this decline, with a special emphasis on the time-span during which the pace of technological change has been the most rapid. Our study is the first (1) to apply longitudinal curvature analysis in the antero-posterior (A-P) and medio-lateral (M-L) planes to the human tibia, and (2) that incorporates a broad temporal population sample including the periods of intensification of agriculture, urbanization and industrialization (from 2900 BC to the 21st century AD; N = 435) within Czech territories. Using three-dimensional geometric morphometrics, we investigated whether anterior tibial curvature mirrors assumed diminishing lower limb loading between prehistoric and industrialized societies and explored its shape in all three dimensions. Results showed the continuous trend of A-P straightening of the shaft. This straightening was associated with a relative sigmoidal curve accentuation in the M-L plane. Given the timescale involved and the known phenomenon of declining mobility, such adaptive changes in bone geometry can be interpreted in terms of the diminishing biomechanical demands on the tibia under different living conditions.

Department of Anthropology and Human Genetics Faculty of Science Charles University Prague Czech Republic

Department of Anthropology National Museum Prague Czech Republic

Department of Prehistorical Archaeology Institute of Archaeology of the Academy of Sciences Prague Czech Republic

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Shackelford LL, Trinkaus E. Late Pleistocene human femoral diaphyseal curvature. Am. J. Phys. Anthropol. 2002;118:359–370. doi: 10.1002/ajpa.10093. PubMed DOI

De Groote, I. A comprehensive analysis of long bone curvature in Neanderthals and modern humans using 3D morphometrics (Ph.D. Thesis). (University College, London, 2008).

Macintosh AA, Davies TG, Pinhasi R, Stock JT. Declining tibial curvature parallels ~6150 years of decreasing mobility in Central European agriculturalists. Am. J. Phys. Anthropol. 2015;157:260–275. doi: 10.1002/ajpa.22710. PubMed DOI

Yamanaka A, Gunji H, Ishida H. Curvature, length, and cross-sectional geometry of the femur and humerus in anthropoid primates. Am. J. Phys. Anthropol. 2005;127:46–57. doi: 10.1002/ajpa.10439. PubMed DOI

Lanyon LE. The influence of function on the development of bone curvature. An experimental study on the rat tibia. J. Zool. 1980;192:457–466. doi: 10.1111/j.1469-7998.1980.tb04243.x. DOI

Bertram J, Biewener A. Bone curvature: Sacrificing strength for load predictability? J. Theor. Biol. 1988;131:75–92. doi: 10.1016/S0022-5193(88)80122-X. PubMed DOI

Main RP, Biewener AA. Ontogenetic patterns of limb loading, in vivo bone strains and growth in the goat radius. J. Exp. Biol. 2004;207:2577–2588. doi: 10.1242/jeb.01065. PubMed DOI

Hall, S. J. Basic Biomechanics. (McGraw-Hill, 2004).

Lanyon LE, Bourn S. The influence of mechanical function on the development and remodeling of the tibia: An experimental study in sheep. J. Bone Joint Surg. Am. 1979;61:263–273. doi: 10.2106/00004623-197961020-00019. PubMed DOI

Milne N. Curved bones: an adaptation to habitual loading. J. Theor. Biol. 2016;407:18–24. doi: 10.1016/j.jtbi.2016.07.019. PubMed DOI

Frost, H. M. Laws of Bone Structure. (Charles C Thomas, 1964).

Pauwels, F. Biomechanics of the Locomotor Apparatus. (Berlin: Springer-Verlag, 1980).

Frelat MA, Katina S, Weber GW, Bookstein FL. Technical note: A novel geometric morphometric approach to the study of long bone shape variation. Am. J. Phys. Anthropol. 2012;149:628–638. doi: 10.1002/ajpa.22177. PubMed DOI

Swartz SM. Curvature of the forelimb bones of anthropoid primates: Overall allometric patterns and specializations in suspensory species. Am. J. Phys. Anthropol. 1990;83:477–498. doi: 10.1002/ajpa.1330830409. DOI

Carlson, K. J. & Marchi, D. Introduction: towards refining the concept of mobility in Reconstructing mobility: Environmental, Behavioral, and Morphological Determinants (eds Carlson, K. J. & Marchi, D.) 91–110 (Springer, 2014).

Neustupný, E. Prehistory of Bohemia 4. Eneolithic. (The Institute of Archaeology of CAS, 2008).

Price TD, Knipper C, Grupe G, Smrčka V. Strontium isotopes and prehistoric human migration: The Bell Beaker period in Central. Europe. Eur. J. Archaeol. 2004;7:9–40. doi: 10.1177/1461957104047992. DOI

Sládek V, Berner M, Sailer R. Mobility in Central European Late Eneolithic and Early Bronze Age: Tibial cross-sectional geometry. J. Archaeol. Sci. 2006;33:470–482. doi: 10.1016/j.jas.2005.09.004. PubMed DOI

Sládek V, Berner M, Sailer R. Mobility in Central European Late Eneolithic and Early Bronze Age: Femoral cross-sectional geometry. Am. J. Phys. Anthropol. 2006;130:320–332. doi: 10.1002/ajpa.20372. PubMed DOI

Kolář J, et al. Population and forest dynamics during the Central European Eneolithic (4500–2000 BC) Archaeol. Anthropol. Sci. 2018;10:1153–1164. doi: 10.1007/s12520-016-0446-5. PubMed DOI PMC

Jiráň, L. Prehistory of Bohemia 5. The Bronze Age. (The Institute of Archaeology of CAS, 2008).

Kočár P, Dreslerová D. Archaeobotanical finds of cultivated plants in the prehistory of the Czech Republic. Památky Archeologické. 2010;101:203–242.

Venclová, N. Prehistory of Bohemia 6. The Late Iron Age – The La Téne period. (The Institute of Archaeology of CAS, 2008).

Ruff C, et al. Gradual decline in mobility with the adoption of food production in Europe. Proc. Natl. Acad. Sci. USA. 2015;112:7147–7152. doi: 10.1073/pnas.1502932112. PubMed DOI PMC

Poláček, L. Great Moravia, the power centre at Mikulčice and the issue of the socioeconomic structure. In Studien zum Burgwall von Mikulčice VIII. (eds Velemínský, P. & Poláček, L.) 11–44 (Archeological Institute of CAS, 2008).

Molenda D. Mining towns in Central-Eastern Europe in feudal times. Acta Pol.Hist. 1976;34:165–188.

Horák J, Hejcman M. Use of trace elements from historical mining for alluvial sediment dating. Soil & Water Res. 2013;8:77–86. doi: 10.17221/49/2012-SWR. DOI

Pachner, P. Pohlavní rozdíly na lidské pánvi. (Czech Academy of Science, 1937).

Kujanová M, Bigoni L, Velemínská J, Velemínský P. Limb bones asymmetry and stress in Medieval and recent populations of Central. Europe. Int. J. Osteoarchaeol. 2008;18:476–491. doi: 10.1002/oa.958. DOI

Bigoni L, Krajíček V, Sládek V, Velemínský P, Velemínská J. Skull shape asymmetry and the socioeconomic structure of an Early Medieval central European society. Am. J. Phys. Anthrop. 2013;150:349–364. doi: 10.1002/ajpa.22210. PubMed DOI

Bigoni L, Žaloudková M, Velemínská J, Velemínský P, Seichert V. The occurrence of directional and fluctuating limb asymmetry in a recently identified collection of human bones. J. Natl. Mus. Nat. Hist. Ser. 2005;174:129–147.

Stránská P, Likovský J, Velemínská J. State of dental health and selected pathological conditions in the recent skulls from the Pachner’s collection. Slov. Antropol. 2005;8:127–136.

Brůžek J. A method for visual determination of sex, using the human hip bone. Am. J. Phys. Anthropol. 2002;117:157–168. doi: 10.1002/ajpa.10012. PubMed DOI

Buikstra, J. E. & Ubelaker, H. D. Standards for data collection from human skeletal remains. Proc. Sem. Field. Mus. Nat. Hist. (Arkansas Archeological Survey Research Series, 1994).

Schmitt A, Murail P, Cunha E, Rougé D. Variability of the pattern of aging on the human skeleton: Evidence from bone indicators and implications on age at death estimation. J. Forensic Sci. 2002;47:1203–1209. doi: 10.1520/JFS15551J. PubMed DOI

Brzobohatá H, Prokop J, Horák M, Jančárek A, Velemínská J. Accuracy and benefits of 3D bone surface modelling: a comparison of two methods of surface data acquisition reconstructed by laser scanning and computed tomography outputs. Coll. Antropol. 2012;36:801–806. PubMed

Adams JW, Olah A, McCurry MR, Potze S. Surface model and tomographic archive of fossil primate and other mammal holotype and paratype specimens of the Ditsong National Museum of Natural History, Pretoria, South Africa. Plos One. 2015;10:e0139800. doi: 10.1371/journal.pone.0139800. PubMed DOI PMC

Bookstein FL. Landmark methods for forms without landmarks: Morphometrics of group differences in outline shape. Med. Image Anal. 1997;1:225–243. doi: 10.1016/S1361-8415(97)85012-8. PubMed DOI

Bookstein, F. L. Morphometric Tools For Landmark Data: Geometry and Biology (Cambridge University Press, 1991).

von Cramon-Taubadel N, Frazier BC, Lahr MM. The problem of assessing landmark error in geometric morphometrics: Theory, methods, and modifications. Am. J. Phys. Anthropol. 2007;134:24–35. doi: 10.1002/ajpa.20616. PubMed DOI

De Groote I, Lockwood CA, Aiello LC. Technical note: A new method for measuring long bone curvature using 3D landmarks and semilandmarks. Am. J. Phys. Anthropol. 2010;141:658–664. PubMed

Biewener AA. Allometry of quadrupedal locomotion: The scaling of duty factor, bone curvature and limb orientation to body size. J. Exp. Biol. 1983;105:147–71. PubMed

Stern J, Jungers W, Susman R. Quantifying phalangeal curvature - an empirical comparison of alternative methods. Am. J. Phys. Anthropol. 1995;97:1–10. doi: 10.1002/ajpa.1330970102. PubMed DOI

Bruns W, Bruce M, Prescott G, Maffulli N. Temporal trends in femoral curvature and length in Medieval and modern Scotland. Am. J. Phys. Anthropol. 2002;119:224–30. doi: 10.1002/ajpa.10113. PubMed DOI

Deane AS, Kremer EP, Begun DR. New approach to quantifying anatomical curvatures using highresolution polynomial curve fitting (HR-PCF) Am. J. Phys. Anthropol. 2005;128:630–638. doi: 10.1002/ajpa.20202. PubMed DOI

Galtés I, Jordana X, Manyosa J, Malgosa A. Functional implications of radial diaphyseal curvature. Am. J. Phys. Anthropol. 2009;138:286–292. doi: 10.1002/ajpa.20926. PubMed DOI

Gunz P, Ramsier M, Kuhrig M, Hublin J-J, Spoor F. The mammalian bony labyrinth reconsidered, introducing a comprehensive geometric morphometric approach. J. Anat. 2012;220:529–543. doi: 10.1111/j.1469-7580.2012.01493.x. PubMed DOI PMC

Botton-Divet L, Houssaye A, Herrel A, Fabre A-C, Cornette R. Tools for quantitative form description: An evaluation of different software packages for semilandmark analysis. PeerJ. 2015;3:e1417. doi: 10.7717/peerj.1417. PubMed DOI PMC

Rosenberger AL, et al. 1.32 ± 0.11 Ma age for underwater remains constrain antiquity and longevity of the Dominican primate Antillothrix bernensis. J. Hum. Evol. 2015;88:85–96. doi: 10.1016/j.jhevol.2015.05.015. PubMed DOI

Wilson LAB, Humphrey LT. Voyaging into the third dimension: A perspective on virtual methods and their application to studies of juvenile sex estimation and the ontogeny of sexual dimorphism. Forensic Sci. Int. 2017;278:32–46. doi: 10.1016/j.forsciint.2017.06.016. PubMed DOI

De Groote I. Femoral curvature in Neanderthals and modern humans: A 3D geometric morphometric analysis. J. Hum. Evol. 2011;60:540–548. doi: 10.1016/j.jhevol.2010.09.009. PubMed DOI

Adams, D. C., Collyer, M. & Kaliontzopoulou, A. Geomorph: Geometric Morphometric Analyses of 2D/3D Landmark Data. R package version 3.0.6, https://CRAN.R-project.org/package=geomorph (2018).

Dryden, I. L. & Mardia, K. V. Statistical Shape Analysis. (Wiley, 1998).

Curran J. Hotelling: Hotelling’s T2 Test and Variants. R package version. 2017;1:0–4.

Peres-Neto PR, Jackson DA, Somers KM. How many principal components? Stopping rules for determining the number of non-trivial axes revisited. Comput. Stat. Data Anal. 2005;49:947–997. doi: 10.1016/j.csda.2004.06.015. DOI

Morphome 3cs 2.0 version. Department of Software and Computer Science Education, Faculty of Mathematics and Physics, Charles University, Prague, Czech Republic, http://www.morphome3cs.com.

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, http://www.R-project.org/ (2018).

Ibrová A, et al. Facial skeleton asymmetry and its relationship to mastication in the Early Medieval period (Great Moravian Empire, Mikulčice, 9–10th century) Arch. Oral. Biol. 2017;84:64–73. doi: 10.1016/j.archoralbio.2017.09.015. PubMed DOI

Havelková P, Villotte S, Velemínský P, Poláček L, Dobisíková M. Enthesopathies and activity patterns in the Early Medieval Great Moravian population: Evidence of division of labour. Int. J. Osteoarchaeol. 2011;21:487–504. doi: 10.1002/oa.1164. DOI

Komar DA, Grivas C. Manufactured populations: What do contemporary reference skeletal collections represent? A comparative study using the Maxwell Museum documented collection. Am. J. Phys. Anthropol. 2008;137:224–333. doi: 10.1002/ajpa.20858. PubMed DOI

Ruff C. Sexual dimorphism in human lower limb bone structure: Relationship to subsistence strategy and sexual division of labor. J. Hum. Evol. 1987;16:391–416. doi: 10.1016/0047-2484(87)90069-8. DOI

Brzobohatá H, Krajíček V, Horák Z, Velemínská J. Sexual dimorphism of the human tibia through time: Insights into shape variation using a surface-based approach. Plos One. 2016;11:e0166461. doi: 10.1371/journal.pone.0166461. PubMed DOI PMC

Brzobohatá H, Krajíček V, Velemínský P, Poláček L, Velemínská J. The shape variability of human tibial epiphyses in an early medieval Great Moravian population (9th–10th century AD): A geometric morphometric assessment. Antropol. Anz. 2014;71:219–236. doi: 10.1127/0003-5548/2014/0336. PubMed DOI

Brzobohatá H, Krajíček V, Horák Z, Sedlak P, Velemínská J. Diachronic changes in size and shape of human proximal tibia in Central Europe during the latest 1200 years. Homo. 2016;67:433–446. doi: 10.1016/j.jchb.2016.10.002. PubMed DOI

Ruff CB, Hayes WC. Sex differences in age-related remodeling of the femur and tibia. J. Orthop. Res. 1988;6:886–896. doi: 10.1002/jor.1100060613. PubMed DOI

Ruff, C. Biomechanical analysis of archaeological human skeletons. In Biological Anthropology of The Human Skeleton (eds Katzenberg, M. & Saunders, S.) 71–102 (Wiley-Liss, 2000).

Sparacello, V. S., Marchi, D. & Shaw, C. N. The importance of considering fibular robusticity when inferring the mobility patterns of past populations. In Reconstructing Mobility: Environmental, Behavioral and Morphological Determinants (eds Carlson, K. J. & Marchi, D.) 91–110 (Springer, 2014).

Svoboda, J., Vašků, Z. & Cílek, V. Velká kniha o klimatu zemí Koruny české. (Regia, 2003).

Wallace IJ, Tommasini SM, Judex S, Garland T, Demes B. Genetic variations and physical activity as determinants of limb bone morphology: An experimental approach using a mouse model. Am. J. Phys. Anthropol. 2012;148:24–35. doi: 10.1002/ajpa.22028. PubMed DOI

von Cramon-Taubadel N, Stock JT, Pinhasi R. Skull and limb morphology differentially track population history and environmental factors in the transition to agriculture in Europe. Proc. Biol. Sci. 2013;280:20131337. doi: 10.1098/rspb.2013.1337. PubMed DOI PMC

Auerbach BM, Gooding AF, Shaw CN, Sylvester AD. The relative position of the human fibula to the tibia influences cross-sectional properties of the tibia. Am. J. Phys. Anthropol. 2017;163:148–57. doi: 10.1002/ajpa.23196. PubMed DOI

Ruff CB, Hayes WC. Age changes in geometry and mineral content of the lower limbs. An. Biomed. Eng. 1984;12:573–584. doi: 10.1007/BF02371450. PubMed DOI

Ding M, Odgaard A, Linde F, Hvid I. Age-related variations in the microstructure of human tibial cancellous bone. J. Orthop. Res. 2002;20:615–621. doi: 10.1016/S0736-0266(01)00132-2. PubMed DOI

Ural A, Vashishth D. Interactions between microstructural and geometrical adaptation in human cortical bone. J. Orthop. Res. 2006;24:1489–1498. doi: 10.1002/jor.20159. PubMed DOI

Stevens SD, Viðarsdóttir US. Morphological changes in the shape of the non-pathological bony knee joint with age: A morphometric analysis of the distal femur and proximal tibia in three populations of known age at death. Int. J. Osteoarchaeol. 2008;18:352–371. doi: 10.1002/oa.954. DOI