The monophyodont molar teeth, prismatic enamel and the complexity of enamel microarchitecture are regarded as essential dental apomorphies of mammals. As prominent background factors of feeding efficiency and individual longevity these characters are crucial components of mammalian adaptive dynamics. Little is known, however, to which degree these adaptations are influenced by the crystallographic properties of elementary hydroxyapatite crystallites, the only inorganic component of enamel. In a miniature pig where individual molars differ significantly in duration of their development and in enamel resistance to attrition stress, we found highly significant differences between the molars in the size of crystallites, amount of microstrain, crystallinity and in enamel stiffness and elasticity, all clearly scaled with the duration of tooth calcification. The same pattern was found also in red deer bearing different molar type. The results suggest that the prolongation of tooth development is associated with an increase of crystallinity, i.e. the atomic order of enamel hydroxyapatite, an obvious component of micromechanical property of mature enamel. This relation could contribute to prolongation of dental development, characteristic of mammals in general. The aspects of enamel crystallinity, omitted in previous studies on mammalian and vertebrate dental evolution, are to be taken in account in these topics.

Department of Inorganic Chemistry Faculty of Science Charles University Hlavova 2030 8 Prague 2 Czech Republic

Department of Zoology Faculty of Science Charles University Viničná 7 Prague 2 Czech Republic

Institute of Geochemistry Mineralogy and Mineral Resources Faculty of Science Charles University Albertov 6 Prague 2 Czech Republic

Institute of Geology of the CAS v v i Rozvojová 269 Prague 6 Czech Republic

Institute of Macromolecular Chemistry of the CAS v v i Heyrovského náměstí 2 Prague 6 Czech Republic

Zobrazit více v PubMed

Pasteris JD, Pasteris JB, Valsami-Jones E. Bone and tooth mineralization: Why apatite? Elements. 2008;4:97–104. doi: 10.2113/GSELEMENTS.4.2.97. DOI

Nanci, A. & Smith, C. Development and calcification of enamel in Calcification in Biological Systems (ed. Bonucci, E.) 314–343 (CRC press, Florida, USA, 1992).

Ruan Q, Moradian-Oldak J. Amelogenin and enamel biomimetics. J. Mater. Chem. B. 2015;3:3112–3129. doi: 10.1039/C5TB00163C. PubMed DOI PMC

Hu JC, Sun X, Zhang C, Simmer JP. A comparison of enamelin and amelogenin expression in developing mouse molars. Eur. J. Oral Sci. 2001;109:125–132. doi: 10.1034/j.1600-0722.2001.00998.x. PubMed DOI

Iwasaki K, et al. Amelotin – a novel secreted, ameloblast-specific protein. J. Dent. Res. 2005;84:1127–1132. doi: 10.1177/154405910508401207. PubMed DOI

Moradian-Oldak J. Protein-mediated enamel mineralization. Front. Biosci. 2012;17:1996–2023. doi: 10.2741/4034. PubMed DOI PMC

Butler P. The ontogeny of molar pattern. Biol. Rev. 1956;31:30–69. doi: 10.1111/j.1469-185X.1956.tb01551.x. DOI

Jernvall J. Mammalian molar cusp patterns: Development mechanisms of diversity. Acta Zool. Fennica. 1995;198:1–61.

Horáček, I. & Špoutil, F. Why tribosphenic? On variation and constraint in developmental dynamics of chiropteran molars in Evolutionary History of Bats: Fossils, Molecules and Morphology (eds Gunnell, G. F. & Simmons, N. B.) 410–455 (Cambridge University Press, 2012).

Fortelius M. Ungulate cheek teeth: Developmental, functional, and evolutionary interrelations. Acta Zool. Fennica. 1985;180:1–76.

Thenius, E. Zähne und Gebiß der Säugetiere (W. de Gruyter Berlin, 1989).

Strait SG. Differences in occlusal morphology and molar size in frugivores and faunivores. J. Hum. Evol. 1993;25:471–484. doi: 10.1006/jhev.1993.1062. DOI

Koenigswald, W. v. Brief survey of enamel diversity at the schmelzmuster level in Cenozoic placental mammals in Tooth Enamel Microstructure (eds Koenigswald, W. & Sander, P.) 137–161 (Rotterdam: A. A. Balkema, 1997).

Kallistová A, Horáček I, Šlouf M, Skála R, Fridrichová M. Mammalian enamel maturation: Crystallographic changes prior to tooth eruption. PLoS ONE. 2017;12:e0171424. doi: 10.1371/journal.pone.0171424. PubMed DOI PMC

Ungár T. Microstructural parameters from X-ray diffraction peak broadening. Scr. Mater. 2004;51:777–781. doi: 10.1016/j.scriptamat.2004.05.007. DOI

Termine JD, Posner AS. Infra-red determinaion of the percentage of crystallinity in apatitic calcium phosphates. Nature. 1966;211:268–270. doi: 10.1038/211268a0. PubMed DOI

Allegra G, et al. Definitions of terms relating to crystalline polymers (Recommendations 1988) Pure Appl. Chem. 1989;61:769–785. doi: 10.1351/pac198961040769. DOI

Rey C, Shimizu M, Collins B, Glimcher MJ. Resolution-enhanced Fourier transform infrared spectroscopy study of the environment of phosphate ions in the early deposits of a solid phase of calcium-phosphate in bone and enamel, and their evolution with age. I: Investigations in the ν4 PO4 domain. Calcif. Tissue Int. 1990;46:384–394. doi: 10.1007/BF02554969. PubMed DOI

Roche D, Ségalen L, Balan E, Delattre S. Preservation assessment of Miocene–Pliocene tooth enamel from Tugen Hills (Kenyan Rift Valley) through FTIR, chemical and stable-isotope analyses. J. Archaeol. Sci. 2010;37:1690–1699. doi: 10.1016/j.jas.2010.01.029. DOI

Asscher Y, Weiner S, Boaretto E. Variations in atomic disorder in biogenic carbonate hydroxyapatite using the infrared spectrum grinding curve method. Adv. Funct. Mater. 2011;21:3308–3313. doi: 10.1002/adfm.201100266. DOI

Tonge C, McCance R. Normal development of the jaws and teeth in pigs, and the delay and malocclusion produced by calorie deficiencies. J. Anat. 1973;115:1–22. PubMed PMC

Wang F, et al. Morphology and chronology of diphyodont dentition in miniature pigs, Sus Scrofa. Oral Dis. 2014;20:367–379. doi: 10.1111/odi.12126. PubMed DOI

Oltramari PVP, Navarro RL, Henriques JFC, Capelozza ALA, Granjeiro JM. Dental and skeletal characterization of the BR-1 minipig. Vet. J. 2007;173:399–407. doi: 10.1016/j.tvjl.2005.11.001. PubMed DOI

McAnulty, P. A. et. al. The Minipig in Biomedical Research (eds McAnulty, P. A., Dayan, A. D., Ganderup, N. Ch. & Hastings, K. L.) (CRC press, 2011).

Grant, A. The use of tooth wear as a guide to the age of domestic ungulates in Ageing and Sexing Animal Bone from Archaeological Sites, vol. 109 (eds Wilson, B., Gigson, C. & Payne, S.) 91–108 (B.A.R: Oxford, 1982).

Kallistová A, Skála R, Horáček I, Miyajima N, Malková R. Influence of sample preparation on the microstructure of tooth enamel apatite. J. Appl. Crystallogr. 2015;48:763–768. doi: 10.1107/S1600576715005208. DOI

Koenigswald, W. v. & Sander, P. Glossary of terms used for enamel microstructures in Tooth Enamel Microstructure (eds Koenigswald, W. & Sander, P.) 267–280 (Rotterdam: A. A. Balkema, 1997).

Ungar, P. S. Mammal Teeth: Origin, Evolution, and Diversity (The Johns Hopkins University Press, Baltimore, 2010).

Hall EO. The deformation and ageing of mild steel: II characteristics of the lüders deformation. Proc. Phys. Soc. Section B. 1951;64:742–753. doi: 10.1088/0370-1301/64/9/302. DOI

Petch NJ. The cleavage strength of polycrystals. J. Iron Steel Inst. 1953;174:25–28.

Nieh T, Wadsworth J. Hall-Petch relation in nanocrystalline solids. Scr. Metall. Mater. 1991;25:955–958. doi: 10.1016/0956-716X(91)90256-Z. DOI

Ostafinska A, et al. Synergistic effects in mechanical properties of PLA/PCL blends with optimized composition, processing, and morphology. RSC Advances. 2015;5:98971–98982. doi: 10.1039/C5RA21178F. DOI

Williamson G, Smallman R. III. Dislocation densities in some annealed and cold-worked metals from measurements on the X-ray debye-scherrer spectrum. Philos. Mag. 1956;1:34–46. doi: 10.1080/14786435608238074. DOI

Šlouf M, Vacková T, Nevoralová M, Pokorný D. Micromechanical properties of one-step and sequentially crosslinked UHMWPEs for total joint replacements. Polym. Test. 2015;41:191–197. doi: 10.1016/j.polymertesting.2014.12.003. DOI

Koenigswald Wv, Clemens WA. Levels of complexity in the microstructure of mammalian enamel and their application in studies of systematics. Scanning Microsc. 1992;6:195–217. PubMed

He LH, Swain MV. Influence of enviroment on the mechanical behaviour of mature human enamel. Biomaterials. 2007;28:4512–4520. doi: 10.1016/j.biomaterials.2007.06.020. PubMed DOI

He LH, Swain MV. Understanding the mechanical behaviour of human enamel from its structural and compositional characteristics. J. Mech. Behav. Biomed. 2008;I:18–29. doi: 10.1016/j.jmbbm.2007.05.001. PubMed DOI

Xie Z, Swain MV, Munroe P, Hoffman M. On the critical parameters that regulate the deformation behaviour of tooth enamel. Biomaterials. 2008;29:2697–2703. doi: 10.1016/j.biomaterials.2008.02.022. PubMed DOI

Yahyazadehfar M, Arola D. The role of organic proteins on the crack growth resistance of human enamel. Acta Biomater. 2015;19:33–45. doi: 10.1016/j.actbio.2015.03.011. PubMed DOI PMC

Cuy JL, Mann AB, Livi JL, Teaford MF, Weihs TP. Nanoindentation mapping of the mechanical properties of human molar tooth enamel. Arch. Oral. Biol. 2002;47:281–291. doi: 10.1016/S0003-9969(02)00006-7. PubMed DOI

Braly A, Darnell LA, Mann AB, Teaford MF, Weihs TP. The effect of prism orientation on the indentation testing of human molar enamel. Arch. Oral. Biol. 2007;52:856–860. doi: 10.1016/j.archoralbio.2007.03.005. PubMed DOI PMC

Fonseca RB, et al. Radiodensity and hardness of enamel and dentin of human and bovine teeth, varying bovine teeth age. Arch. Oral. Biol. 2008;53:1023–1029. doi: 10.1016/j.archoralbio.2008.06.012. PubMed DOI

Robinson, C., Kirkham, J., Brookes, S. J. & Shore, R. C. Chemistry of mature enamel in Dental enamel: formation to destruction (eds Robinson, C., Kirkham, J. & Shore, R.) 167–191 (CRC press, 1995).

Helfman PM, Bada JL. Aspartic acid racemization in tooth enamel from living humans. P. Natl. Acad. Sci. 1975;72(8):2891–2894. doi: 10.1073/pnas.72.8.2891. PubMed DOI PMC

Park S, Wang DH, Zhang D, Romberg E, Arola D. Mechanical properties of human enamel as a function of age and location in the tooth. J. Mater. Sci: Mater. Med. 2008;19:2317–2324. PubMed

Nanci, A. Enamel: composition, formation, and structure in Ten Cate’s oral histology: Development, structure, and function. 122–164 (Elsevier: Mosby, Missouri, USA, 2008).

Vodička P, et al. The miniature pig as an animal model in biomedical research. Ann. N. Y. Acad. Sci. 2005;1049:161–171. doi: 10.1196/annals.1334.015. PubMed DOI

Baxa M, et al. A transgenic minipig model of Huntington’s disease. J Huntington’s Dis. 2013;2:47–68. PubMed

Planska D, Burocziova M, Strnadel J, Horak V. Immunohistochemical analysis of collagen IV and laminin expression in spontaneous melanoma regression in the melanoma-bearing Lib ěchov minipig. Acta Histochem. Cytochem. 2015;48:15. doi: 10.1267/ahc.14020. PubMed DOI PMC

Weaver ME, Jump EB, McKean CF. The eruption pattern of permanent teeth in miniature swine. Arch. Oral Biol. 1969;14:323–331. doi: 10.1016/0003-9969(69)90235-0. PubMed DOI

Rodrguez-Carvajal J. Recent developments of the program FULLPROF. Commission on powder diffraction, Newsletter. 2001;26:12–19.

Rönholm E. The amelogenesis of human teeth as revealed by electron microscopy. II - The development of the enamel crystallites. J. Ultrastruct. Res. 1962;6:249–303. doi: 10.1016/S0022-5320(62)80036-7. PubMed DOI

Daculsi G, Kerebel B. High–resolution electron microscope study of human enamel crystallites: size, shape, and growth. J. Ultrastruct. Res. 1978;65:163–172. doi: 10.1016/S0022-5320(78)90053-9. PubMed DOI

Cuisinier FJG, Steuer P, Senger B, Voegel JC, Frank RM. Human amelogenesis: high resolution electron microscopy of nanometer–sized particles. Cell Tissue Res. 1993;273:175–182. doi: 10.1007/BF00304624. PubMed DOI

Popa NC. The (hkl) dependence of diffraction-line broadening caused by strain and size for all Laue groups in Rietveld refinement. J. Appl. Cryst. 1998;31:176–180. doi: 10.1107/S0021889897009795. DOI

Scardi P, Leoni M. Fourier modelling of the anisotropic line broadening of X-ray diffraction profiles due to line and plane lattice defects. J. Appl. Cryst. 1999;32:671–682. doi: 10.1107/S002188989900374X. DOI

Stephens PW. Phenomenological model of anisotropic peak broadening in powder diffraction. J. Appl. Cryst. 1999;32:281–289. doi: 10.1107/S0021889898006001. DOI

Popa NC, Balzar D. Size-broadening anisotropy in whole powder pattern fitting. Application to zinc oxide and interpretation of the apparent crystallites in terms of physical models. J. Appl. Cryst. 2008;41:615–627. doi: 10.1107/S0021889808012223. DOI

Oliver WC, Pharr GM. Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology. J. Mater. Res. 2004;19:3–20. doi: 10.1557/jmr.2004.19.1.3. DOI

Poduska KM, et al. Decoupling local disorder and optical effects in infrared spectra: differentiating between calcites with different origins. Adv. Mater. 2011;23:550–554. doi: 10.1002/adma.201003890. PubMed DOI

Weiner S, Bar-Yosef O. States of preservation of bones from prehistoric sites in the Near East: a survey. J. Archaeol. Sci. 1990;17:187–196. doi: 10.1016/0305-4403(90)90058-D. DOI

OMNIC software 9.2.98. Thermo Fisher Scientific Inc. (1992–2012).