Experimental assessment of the relationship between diet and mandibular morphology using a pig model: New insights for paleodietary reconstructions.
durophagy
experimental study
geometric morphometrics
mandible
paleodiet
Journal
Anatomical record (Hoboken, N.J. : 2007)
ISSN: 1932-8494
Titre abrégé: Anat Rec (Hoboken)
Pays: United States
ID NLM: 101292775
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
20
01
2022
received:
05
10
2021
accepted:
29
01
2022
pubmed:
11
2
2022
medline:
15
10
2022
entrez:
10
2
2022
Statut:
ppublish
Résumé
Dietary habits exert significant selective pressures on anatomical structures in animals, leading to substantial morphological adaptations. Yet, the relationships between the mandible and diet are still unclear, raising issues for paleodietary reconstructions notably. To assess the impact of food hardness and size on morphological structures, we used an experimental baseline using a model based on the domestic pig, an omnivorous mammal with bunodont, thick-enameled dentition, and chewing movements similar to hominids. We hypothesized that the consumption of different types of seeds would result in substantial differences in the morphology of the mandible despite similar overall diets. The experiment was conducted on four groups of juvenile pigs fed with mixed cereal and soy flours. The control group received only flours. We supplemented the four others with either 10 hazelnuts, 30 hazelnuts, 30% barley seeds, or 20% corn kernels per day. We investigated the shape differences between the controlled-fed groups using three-dimensional geometric morphometrics. Our results provide strong evidence that the supplemental consumption of a significant amount of seeds for a short period (95 days) substantially modify the mandibular morphology of pigs. Our analyses suggest that this shape differentiation is due to the size of the seeds, requiring high and repeated bite force, rather than their hardness. These results provide new perspectives for the use of mandibular morphology as a proxy in paleodietary reconstructions complementing dental microwear textures analyses.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3150-3160Informations de copyright
© 2022 American Association for Anatomy.
Références
Adams, D. C., Collyer, M. & Kaliontzopoulou, A. (2019). geomorph: Geometric morphometric analyses of 2D/3D landmark data (Version 3.1.2).
Anapol, F., & Lee, S. (1994). Morphological adaptation to diet in platyrrhine primates. American Journal of Physical Anthropology, 94, 239-261.
Anderson, P. S., Renaud, S., & Rayfield, E. J. (2014). Adaptive plasticity in the mouse mandible. BMC Evolutionary Biology, 14(1), 85.
Arbour, J. H., Curtis, A. A., & Santana, S. E. (2019). Signatures of echolocation and dietary ecology in the adaptive evolution of skull shape in bats. Nature Communications, 10(1), 2036.
Beecher, R. M., & Corruccini, R. S. (1981). Effects of dietary consistency on craniofacial and occlusal development in the rat. The Angle Orthodontist, 51(1), 61-69.
Bouvier, M., & Hylander, W. L. (1981). Effect of bone strain on cortical bone structure in 598 macaques (Macaca mulatta). Journal of Morphology, 167(1), 1-12.
Brassard, C., Merlin, M., Monchâtre-Leroy, E., Guintard, C., Barrat, B., Callou, C., Cornette, R., & Herrel, A. (2020). How does masticatory muscle architecture covary with mandibular shape in domestic dogs? Evolutionary Biology, 47(2), 133-151.
Cerling, T. E., Mbua, E., Kirera, F. M., Manthi, F. K., Grine, F. E., Leakey, M. G., Sponheimer, M., & Uno, K. T. (2011). Diet of Paranthropus boisei in the early Pleistocene of East Africa. Proceedings of the National Academy of Sciences, 108(23), 9337-9341.
Collyer, M. L., Sekora, D. J., & Adams, D. C. (2015). A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity, 115(4), 357-365.
Cornette, R., Tresset, A., & Herrel, A. (2015). The shrew tamed by Wolff's law: Do functional constraints shape the skull through muscle and bone covariation? Journal of Morphology, 276(3), 301-309.
Daegling, D. J. (1992). Mandibular morphology and diet in the genus Cebus. International Journal of Primatology, 13(5), 545-570.
Davis, M., & Pineda-Munoz, S. (2016). The temporal scale of diet and dietary proxies. Ecology and Evolution, 6(6), 1883-1897.
Delprete, C., & Sesana, R. (2014). Mechanical characterization of kernel and shell of hazelnuts: Proposal of an experimental procedure. Journal of Food Engineering, 124, 28-34.
Dinu, A. (2009). The action of the masticatory muscles and cranial changes in pigs as results of domestication. Documenta Praehistorica, 36, 207-218.
Ercisli, S., Ozturk, I., Kara, M., Kalkan, F., Seker, H., Duyar, O., & Erturk, Y. (2011). Physical properties of hazelnuts. International Agrophysics, 25(2), 115-121.
Evin, A., Cucchi, T., Cardini, A., Strand Vidarsdottir, U., Larson, G., & Dobney, K. (2013). The long and winding road: Identifying pig domestication through molar size and shape. Journal of Archaeological Science, 40(1), 735-743.
Fabre, A.-C., Perry, J. M. G., Hartstone-Rose, A., Lowie, A., Boens, A., & Dumont, M. (2018). Do muscles constrain skull shape evolution in Strepsirrhines? The Anatomical Record, 301(2), 291-310.
Frost, H. M. (2001). From Wolff's law to the Utah paradigm: Insights about bone physiology 690 and its clinical applications. The Anatomical Record, 262(4), 398-419.
Gailer, J. P., Calandra, I., Schulz-Kornas, E., & Kaiser, T. M. (2016). Morphology is not destiny: Discrepancy between form, function and dietary adaptation in bovid cheek teeth. Journal of Mammalian Evolution, 23(4), 369-383.
Grine, F. E., & Daegling, D. J. (2017). Functional morphology, biomechanics and the retrodiction of early hominin diets. Comptes Rendus Palevol, 16(5), 613-631.
Gunz, P., & Mitteroecker, P. (2013). Semilandmarks: A method for quantifying curves and surfaces. Hystrix: the Italian Journal of Mammalogy, 24(1), 103-109.
Herring, S. W. (1976). The dynamics of mastication in pigs. Archives of Oral Biology, 21(8), 473-480.
Jangi, A. N., Mortazavi, S. A., Tavakoli, M., Ghanbari, A., Tavakolipour, H., & Haghayegh, G. H. (2011). Comparison of mechanical and thermal properties between two varieties of barley (Hordeum vulgare L.) grains. Australian Journal of Agricultural Engineering, 2(5), 132-139.
Jolly, C. J. (1970). The seed-eaters: A new model of hominid differentiation based on a baboon analogy. Man, 5(1), 5-26.
Kalkan, F., Kara, M., Bastaban, S., & Turgut, N. (2011). Strength and frictional properties of popcorn kernel as affected by moisture content. International Journal of Food Properties, 14(6), 1197-1207.
Kamaluddin, S. N., Tanaka, M., Wakamori, H., Nishimura, T., & Ito, T. (2019). Phenotypic plasticity in the mandibular morphology of Japanese macaques: Captive-wild comparison. Royal Society Open Science, 10(7), 181382.
Kay, R. F. (1985). Dental evidence for the diet of Australopithecus. Annual Review of Anthropology, 14, 315-341.
Kiliaridis, S., Mejersjö, C., & Thilander, B. (1989). Muscle function and craniofacial morphology: A clinical study in patients with myotonic dystrophy. European Journal of Orthodontics, 11(2), 131-138.
Kinzey, W. G. (1992). Dietary and dental adaptations in the Pitheciinae. American Journal of Physical Anthropology, 88(4), 499-514.
Kovarovic, K., Aiello, L. C., Cardini, A., & Lockwood, C. A. (2011). Discriminant function analyses in archaeology: Are classification rates too good to be true? Journal of Archaeological Science, 38(11), 3006-3018.
Lambert, J. E., Chapman, C. A., Wrangham, R. W., & Conklin-Brittain, N. L. (2004). Hardness of cercopithecine foods: Implications for the critical function of enamel thickness in exploiting fallback foods. American Journal of Physical Anthropology, 125(4), 363-368.
Lieberman, D. E., Krovitz, G. E., Yates, F. W., Devlin, M., & St Claire, M. (2004). Effects of 803 food processing on masticatory strain and craniofacial growth in a retrognathic face. Journal of Human Evolution, 46(6), 655-677.
Liem, K. F. (1980). Adaptive significance of intra- and interspecific differences in the feeding repertoires of cichlid fishes. American Zoologist, 20(1), 295-314.
Louail, M., Ferchaud, S., Souron, A., Walker, A. E. C., & Merceron, G. (2021). Dental microwear textures differ in pigs with overall similar diets but fed with different seeds. Palaeogeography, Palaeoclimatology, Palaeoecology, 572, 110415.
Lucas, P. W. (2004). Dental functional morphology: How teeth work. Cambridge University Press.
Marcé-Nogué, J., Püschel, T. A., & Kaiser, T. M. (2017). A biomechanical approach to understand the ecomorphological relationship between primate mandibles and diet. Scientific Reports, 7(1), 8364.
Markowski, M., Majewska, K., Kwiatkowski, D., Malkowski, M., & Burdylo, G. (2010). Selected geometric and mechanical properties of barley (Hordeum vulgare L.) grain. International Journal of Food Properties, 13(4), 890-903.
Marshall, A. J., Boyko, C. M., Feilen, K. L., Boyko, R. H., & Leighton, M. (2009). Defining fallback foods and assessing their importance in primate ecology and evolution. American Journal of Physical Anthropology, 140(4), 603-614.
Meloro, C., Cáceres, N. C., Carotenuto, F., Sponchiado, J., Melo, G. L., Passaro, F., & Raia, P. (2015). Chewing on the trees: Constraints and adaptation in the evolution of the primate mandible. Evolution, 69(7), 1690-1700.
Menegaz, R., Baier, D., Metzger, K., Herring, S., & Brainerd, E. (2015). XROMM analysis of tooth occlusion and temporomandibular joint kinematics during feeding in juvenile miniature pigs. The Journal of Experimental Biology, 218, 2573-2584.
Neaux, D., Blanc, B., Ortiz, K., Locatelli, Y., Laurens, F., Baly, I., Callou, C., Lecompte, F., Cornette, R., Sansalone, G., Haruda, A., Schafberg, R., Vigne, J.-D., Debat, V., Herrel, A., & Cucchi, T. (2021). How changes in functional demands associated with captivity affect the skull shape of a wild boar (Sus scrofa). Evolutionary Biology, 48, 27-40.
Neaux, D., Blanc, B., Ortiz, K., Locatelli, Y., Schafberg, R., Herrel, A., Debat, V., & Cucchi, T. (2021). Constraints associated with captivity alter craniomandibular integration in wild boar. Journal of Anatomy, 239(2), 489-497.
Neaux, D., Sansalone, G., Lecompte, F., Haruda, A., Schafberg, R., & Cucchi, T. (2020). Examining the effect of feralization on craniomandibular morphology in pigs, Sus scrofa (Artiodactyla: Suidae). Biological Journal of the Linnean Society, 131(4), 870-879.
Norconk, M. A., & Veres, M. (2011). Physical properties of fruit and seeds ingested by primate seed predators with emphasis on sakis and bearded sakis. The Anatomical Record, 294(12), 2092-2111.
Ödman, A., Mavropoulos, A., & Kiliaridis, S. (2008). Do masticatory functional changes influence the mandibular morphology in adult rats. Archives of Oral Biology, 53(12), 1149-1154.
Peterson, A., Abella, E. F., Grine, F. E., Teaford, M. F., & Ungar, P. S. (2018). Microwear textures of Australopithecus africanus and Paranthropus robustus molars in relation to paleoenvironment and diet. Journal of Human Evolution, 119, 42-63.
Potts, R. (2004). Paleoenvironmental basis of cognitive evolution in great apes. American Journal of Primatology, 62, 209-228.
R Core Team. (2019). R: A language and environment for statistical computing (version 3.1.2). Vienna, Austria.
Raia, P., Carotenuto, F., Meloro, C., Piras, P., & Pushkina, D. (2010). The shape of contention: Adaptation, history, and contingency in ungulate mandibles. Evolution, 64(5), 1489-1503.
Rak, Y. (1978). The functional significance of the squamosal suture in Australopithecus boisei. American Journal of Physical Anthropology, 49(1), 71-78.
Rak, Y., & Hylander, W. L. (2008). What else is the tall mandibular ramus of the robust australopiths good for? In C. Vinyard, M. J. Ravosa, & C. Wall (Eds.), Primate craniofacial function and biology (pp. 431-442). Springer US.
Ramdarshan, A., Blondel, C., Brunetière, N., Francisco, A., Gautier, D., Surault, J., & Mercercon, G. (2016). Seeds, browse, and tooth wear: A sheep perspective. Ecology and Evolution, 6(16), 5559-5569.
Ravosa, M. J., Scott, J. E., McAbee, K. R., Veit, A. J., & Fling, A. L. (2015). Chewed out: An experimental link between food material properties and repetitive loading of the masticatory apparatus in mammals. PeerJ, 3, e1345.
Renaud, S., & Auffray, J.-C. (2009). Adaptation and plasticity in insular evolution of the house mouse mandible. Journal of Zoological Systematics and Evolutionary Research, 48(2), 138-150.
Robinson, B. W., & Wilson, D. S. (1998). Optimal foraging, specialization, and a solution to Liem's paradox. American Naturalist, 151, 223-235.
Robinson, J. T. (1954). Prehominid dentition and hominid evolution. Evolution, 8(4), 324-334.
Rohlf, F. J., & Slice, D. (1990). Extensions of the procrustes method for the optimal superimposition of landmarks. Systematic Biology, 39(1), 40-59.
Ross, C. F., & Iriarte-Diaz, J. (2014). What does feeding system morphology tell us about feeding? Evolutionary Anthropology, 23(3), 105-120.
Ross, C. F., Iriarte-Diaz, J., & Nunn, C. L. (2012). Innovative approaches to the relationship between diet and mandibular morphology in primates. International Journal of Primatology, 33(3), 632-660.
Schlager, S., & Jefferis, G. (2020). Morpho: Calculations and visualisations related to geometric morphometrics.
Schley, L., & Roper, T. J. (2003). Diet of wild boar Sus scrofa in Western Europe, with particular reference to consumption of agricultural crops. Mammal Review, 33(1), 43-56.
Schulz, E., Piotrowski, V., Clauss, M., Mau, M., Merceron, G., & Kaiser, T. M. (2013). Dietary abrasiveness is associated with variability of microwear and dental surface texture in rabbits. PLoS One, 8(2), e56167.
Scott, J. E., McAbee, K. R., Eastman, M. M., & Ravosa, M. J. (2014). Experimental perspective on fallback foods and dietary adaptations in early hominins. Biological Letters, 10(1), 20130789.
Scott, R. S., Teaford, M. F., & Ungar, P. S. (2012). Dental microwear texture and anthropoid diets. American Journal of Physical Anthropology, 147(4), 551-579.
Scott, R. S., Ungar, P. S., Bergstrom, T. S., Brown, C. A., Grine, F. E., Teaford, M. F., & Walker, A. (2005). Dental microwear texture analysis shows within-species diet variability in fossil hominins. Nature, 436(7051), 693-695.
Sella-Tunis, T., Pokhojaev, A., Sarig, R., O'Higgins, P., & May, H. (2018). Human mandibular shape is associated with masticatory muscle force. Scientific Reports, 8(1), 6042.
Smith, A. L., Benazzi, S., Ledogar, J. A., Tamvada, K., Pryor Smith, L. C., Weber, G. W., Spencer, M. A., Lucas, P. W., Michael, S., Shekeban, A., Al-Fadhalah, K., Almusallam, A. S., Dechow, P. C., Grosse, I. R., Ross, C. F., Madden, R. H., Richmond, B. G., Wright, B. W., Wang, Q., … Strait, D. S. (2015). The feeding biomechanics and dietary ecology of Paranthropus boisei. Anatomical Record, 298(1), 145-167.
Tamagnini, D., Meloro, C., Raia, P., & Maiorano, L. (2021). Testing the occurrence of convergence in the craniomandibular shape evolution of living carnivorans. Evolution, 75(7), 1738-1752.
Taylor, A. B. (2006). Diet and mandibular morphology in african apes. International Journal of Primatology, 27(1), 181.
Tran, T. L., DeMan, J. M., & Rasper, V. F. (1981). Measurement of corn kernel hardness. Canadian Institute of Food Science and Technology Journal, 14(1), 42-48.
Turnbull, W. D. (1970). Mammalian masticatory apparatus: Fieldiana geology (Vol. 18). Field Museum Press.
Tütken, T., Kaiser, T. M., Vennemann, T., & Merceron, G. (2013). Opportunistic feeding strategy for the earliest old world hypsodont equids: Evidence from stable isotope and dental wear proxies. PLoS One, 8(9), e74463.
Ungar, P. S., Grine, F. E., & Teaford, M. F. (2008). Dental microwear and diet of the Plio-Pleistocene hominin Paranthropus boisei. PLoS One, 3(4), e2044.
Ungar, P. S., & Daegling, D. J. (2013). The functional morphology of jaws and teeth: implications for understanding early hominin dietary adaptations. In M. Sponheimer, J. A. Lee-Thorp, K.E. Reed, & P. Ungar (Eds.), Early Hominin Paleoecology (pp. 203-250). University Press of Colorado.
Ungar, P. S., Krueger, K. L., Blumenschine, R. J., Njau, J., & Scott, R. S. (2012). Dental microwear texture analysis of hominins recovered by the Olduvai Landscape Paleoanthropology Project, 1995-2007. Journal of Human Evolution. 63, 429-437.
Ungar, P. S., & Sponheimer, M. (2011). The diets of early hominins. Science, 334(6053), 190-193.
van Casteren, A., Strait, D. S., Swain, M. V., Michael, S., Thai, L. A., Philip, S. M., Saji, S., Al-Fadhalah, K., Almusallam, A. S., Shekeban, A., McGraw, W. S., Kane, E. E., Wright, B. W., & Lucas, P. W. (2020). Hard plant tissues do not contribute meaningfully to dental microwear: Evolutionary implications. Scientific Reports, 10(1), 582.
van Casteren, A., Wright, E., Kupczik, K., & Robbins, M. M. (2019). Unexpected hard-object feeding in Western lowland gorillas. American Journal of Physical Anthropology, 170(3), 433-438.
von Cramon-Taubadel, N. (2011). Global human mandibular variation reflects differences in agricultural and hunter-gatherer subsistence strategies. Proceedings of the National Academy of Sciencesof the United States of America, 108(49), 19546-19551.
Ward, S. C., & Molnar, S. (1980). Experimental stress analysis of topographic diversity in early hominid gnathic morphology. American Journal of Physical Anthropology, 53(3), 383-395.
Wiley, D., Amenta, N., Alcantara, D., Ghosh, D., Kil, Y. J., Delson, E., W. Harcourt-Smith, F.J. Rohlf, K. St John, B. Hamann (2005). Evolutionary morphing. Proceedings of IEEE Visualization 2005 (pp. 431-438). IEEE.
Wolff, J. (1986). The law of bone remodelling. Springer-Verlag.
Wroe, S., Ferrara, T. L., McHenry, C. R., Curnoe, D., & Chamoli, U. (2010). The craniomandibular mechanics of being human. Proceedings of the Royal Society of London B: Biological Sciences, 277(1700), 3579-3586.
Zelditch, M. L., Ye, J., Mitchell, J. S., & Swiderski, D. L. (2017). Rare ecomorphological convergence on a complex adaptive landscape: Body size and diet mediate evolution of jaw shape in squirrels (Sciuridae). Evolution, 71(3), 633-649.