Teaching an old jaw new tricks: Diet-induced plasticity in a model organism from weaning to adulthood

Journal of Experimental Biology

Volumn 217, Issue 22, 2014, Pages 4099-4107

  Scott, Jeremiah E ^a   McAbee, Kevin R ^b   Eastman, Meghan M ^b   Ravosa, Matthew J ^b  

^a SOUTHERN ILLINOIS UNIVERSITY   (United States)

^b UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

Adaptive plasticity; Developmental window; Growth; Mammal; Masticatory apparatus; Reaction norm

Indexed keywords

ANIMALIA; MAMMALIA; ORYCTOLAGUS CUNICULUS;

ADAPTATION; ANATOMY AND HISTOLOGY; ANIMAL; ANIMAL FOOD; BIOMECHANICS; BONE REMODELING; DIET; MALE; MANDIBLE; MASTICATION; PHENOTYPE; PHYSIOLOGY; RABBIT; SKULL;

ADAPTATION, PHYSIOLOGICAL; ANIMAL FEED; ANIMALS; BIOMECHANICAL PHENOMENA; BONE REMODELING; DIET; MALE; MANDIBLE; MASTICATION; PHENOTYPE; RABBITS; SKULL;

EID: 84925778748     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.111708     Document Type: Article

References (76)

1. Agrawal, A. A. (2001). Phenotypic plasticity in the interactions and evolution of species. Science 294, 321-326.
2. Auld, J. R., Agrawal, A. A. and Relyea, R. A. (2010). Re-evaluating the costs and limits of adaptive phenotypic plasticity. Proc. Biol. Sci. 277, 503-511.
3. Bass, S., Pearce, G., Bradney, M., Hendrich, E., Delmas, P. D., Harding, A. and Seeman, E. (1998). Exercise before puberty may confer residual benefits in bone density in adulthood: Studies in active prepubertal and retired female gymnasts. J. Bone Miner. Res. 13, 500-507.
4. Benjamini, Y. and Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Stat. Soc. Series B Stat. Methodol. 57, 289-300.
5. Bernays, E. A. (1986). Diet-induced head allometry among foliage-chewing insects and its importance for graminivores. Science 231, 495-497.
6. Bertram, J. E. A. and Swartz, S. M. (1991). The 'law of bone transformation': A case of crying Wolff? Biol. Rev. Camb. Philos. Soc. 66, 245-273.
7. Biewener, A. A. (1993). Safety factors in bone strength. Calcif. Tissue Int. 53 Suppl. 1, S68-S74.
8. Biewener, A. A., Swartz, S. M. and Bertram, J. E. A. (1986). Bone modeling during growth: dynamic strain equilibrium in the chick tibiotarsus. Calcif. Tissue Int. 39, 390- 395.
9. Bouvier, M. (1988). Effects of age on the ability of the rat temporomandibular joint to respond to changing functional demands. J. Dent. Res. 67, 1206-1212.
10. Bouvier, M. and Hylander, W. L. (1981). Effect of bone strain on cortical bone structure in macaques (Macaca mulatta). J. Morphol. 167, 1-12.
11. Bouvier, M. and Hylander, W. L. (1984). The effect of dietary consistency on gross and histologic morphology in the craniofacial region of young rats. Am. J. Anat. 170, 117-126.
12. Burr, D. B. (1997). Muscle strength, bone mass, and age-related bone loss. J. Bone Miner. Res. 12, 1547-1551.
13. Congdon, K. A., Hammond, A. S. and Ravosa, M. J. (2012). Differential limb loading in miniature pigs (Sus scrofa domesticus): A test of chondral modeling theory. J. Exp. Biol. 215, 1472-1483.
14. de Jong, G. and Crozier, R. H. (2003). A flexible theory of evolution. Nature 424, 16- 17.
15. DeWitt, T. J., Sih, A. and Wilson, D. S. (1998). Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13, 77-81.
16. Dufty, A. M., Clobert, J. and Møller, A. P. (2002). Hormones, developmental plasticity and adaptation. Trends Ecol. Evol. 17, 190-196.
17. Efron, B. and Tibshirani, R. J. (1993). An Introduction to the Bootstrap. New York, NY: Chapman & Hall.
18. Engelke, K., Kemmler, W., Lauber, D., Beeskow, C., Pintag, R. and Kalender, W. A. (2006). Exercise maintains bone density at spine and hip EFOPS: A 3-year longitudinal study in early postmenopausal women. Osteoporos. Int. 17, 133-142.
19. Fischer, B., van Doorn, G. S., Dieckmann, U. and Taborsky, B. (2014). The evolution of age-dependent plasticity. Am. Nat. 183, 108-125.
20. Futuyma, D. J. (2011). Expand or revise? The evolutionary synthesis today. Q. Rev. Biol. 86, 203-208.
21. Gabriel, W. (1999). Evolution of reversible plastic responses: Inducible defenses and environmental tolerance. In The Ecology and Evolution of Inducible Defenses (ed. R. Tollrian and D. Harvell), pp. 286-305. Princeton, NJ: Princeton University Press.
22. Gomez-Mestre, I. and Buchholz, D. R. (2006). Developmental plasticity mirrors differences among taxa in spadefoot toads linking plasticity and diversity. Proc. Natl. Acad. Sci. USA 103, 19021-19026.
23. Gotthard, K. and Nylin, S. (1995). Adaptive plasticity and plasticity as an adaptation: A selective review of plasticity in animal morphology and life history. Oikos 74, 3-17.
24. Hamrick, M. W., Skedros, J. G., Pennington, C. and McNeil, P. L. (2006). Increased osteogenic response to exercise in metaphyseal versus diaphyseal cortical bone. J. Musculoskelet. Neuronal Interact. 6, 258-263.
25. Herring, S. W. (1985). The ontogeny of mammalian mastication. Am. Zool. 25, 339- 349.
26. Hinton, R. J. and McNamara, J. A. Jr (1984). Effect of age on the adaptive response of the adult temporomandibular joint. A study of induced protrusion in Macaca mulatta. Angle Orthod. 54, 154-162.
27. Hirano, T., Burr, D. B., Cain, R. L. and Hock, J. M. (2000). Changes in geometry and cortical porosity in adult, ovary-intact rabbits after 5 months treatment with LY333334 (hPTH 1-34). Calcif. Tissue Int. 66, 456-460.
28. Holmes, M. A. and Ruff, C. B. (2011). Dietary effects on development of the human mandibular corpus. Am. J. Phys. Anthropol. 145, 615-628.
29. Hoverman, J. T. and Relyea, R. A. (2007). How flexible is phenotypic plasticity? Developmental windows for trait induction and reversal. Ecology 88, 693-705.
30. Hsieh, Y. F., Robling, A. G., Ambrosius, W. T., Burr, D. B. and Turner, C. H. (2001). Mechanical loading of diaphyseal bone in vivo: The strain threshold for an osteogenic response varies with location. J. Bone Miner. Res. 16, 2291-2297.
31. Isaksson, H., Harjula, T., Koistinen, A., Iivarinen, J., Seppänen, K., Arokoski, J. P. A., Brama, P. A., Jurvelin, J. S. and Helminen, H. J. (2010). Collagen and mineral deposition in rabbit cortical bone during maturation and growth: effects on tissue properties. J. Orthop. Res. 28, 1626-1633.
32. Kannus, P., Haapasalo, H., Sankelo, M., Sievänen, H., Pasanen, M., Heinonen, A., Oja, P. and Vuori, I. (1995). Effect of starting age of physical activity on bone mass in the dominant arm of tennis and squash players. Ann. Intern. Med. 123, 27-31.
33. Kontulainen, S., Sievänen, H., Kannus, P., Pasanen, M. and Vuori, I. (2003). Effect of long-term impact-loading on mass, size, and estimated strength of humerus and radius of female racquet-sports players: A peripheral quantitative computed tomography study between young and old starters and controls. J. Bone Miner. Res. 18, 352-359.
34. Kotrschal, A. and Taborsky, B. (2010). Environmental change enhances cognitive abilities in fish. PLoS Biol. 8, e1000351.
35. Langenbach, G. E. J. and van Eijden, T. M. G. J. (2001). Mammalian feeding motor patterns. Am. Zool. 41, 1338-1351.
36. Lanyon, L. E. and Rubin, C. T. (1985). Functional adaptation in skeletal structures. In Functional Vertebrate Morphology (ed. M. Hildebrand, D. M. Bramble, K. F. Liem and D. B. Wake), pp. 1-25. Cambridge: Harvard University Press.
37. Lanyon, L. and Skerry, T. (2001). Postmenopausal osteoporosis as a failure of bone's adaptation to functional loading: A hypothesis. J. Bone Miner. Res. 16, 1937-1947.
38. Lieberman, D. E., Devlin, M. J. and Pearson, O. M. (2001). Articular area responses to mechanical loading: effects of exercise, age, and skeletal location. Am. J. Phys. Anthropol. 116, 266-277.
39. Lieberman, D. E., Pearson, O. M., Polk, J. D., Demes, B. and Crompton, A. W. (2003). Optimization of bone growth and remodeling in response to loading in tapered mammalian limbs. J. Exp. Biol. 206, 3125-3138.
40. Manly, B. F. J. (1997). Randomization, Bootstrap and Monte Carlo Methods in Biology. Boca Raton, FL: Chapman & Hall/CRC.
41. Marchinko, K. B. (2003). Dramatic phenotypic plasticity in barnacle legs (Balanus glandula Darwin): magnitude, age dependence, and speed of response. Evolution 57, 1281-1290.
42. Marshall, J. and Wrangham, R. W. (2007). Evolutionary consequences of fallback foods. Int. J. Primatol. 28, 1219-1235.
43. Masoud, I., Shapiro, F., Kent, R. and Moses, A. (1986). A longitudinal study of the growth of the New Zealand white rabbit: cumulative and biweekly incremental growth rates for body length, body weight, femoral length, and tibial length. J. Orthop. Res. 4, 221-231.
44. Menegaz, R. A., Sublett, S. V., Figueroa, S. D., Hoffman, T. J. and Ravosa, M. J. (2009). Phenotypic plasticity and function of the hard palate in growing rabbits. Anat. Rec. 292, 277-284.
45. Meyer, A. (1987). Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41, 1357-1369.
46. Muschick, M., Barluenga, M., Salzburger, W. and Meyer, A. (2011). Adaptive phenotypic plasticity in the Midas cichlid fish pharyngeal jaw and its relevance in adaptive radiation. BMC Evol. Biol. 11, 116.
47. Orr, H. A. (1999). An evolutionary dead end? Science 285, 343-344.
48. Palmer, A. R. (2004). Symmetry breaking and the evolution of development. Science 306, 828-833.
49. Pearson, O. M. and Lieberman, D. E. (2004). The aging of Wolff's "law": ontogeny and responses to mechanical loading in cortical bone. Am. J. Phys. Anthropol. 125 Suppl. 39, 63-99.
50. Pfennig, D. W., Wund, M. A., Snell-Rood, E. C., Cruickshank, T., Schlichting, C. D. and Moczek, A. P. (2010). Phenotypic plasticity's impacts on diversification and speciation. Trends Ecol. Evol. 25, 459-467.
51. Pigliucci, M., Murren, C. J. and Schlichting, C. D. (2006). Phenotypic plasticity and evolution by genetic assimilation. J. Exp. Biol. 209, 2362-2367.
52. Pigliucci, M. (1996). How organisms respond to environmental changes: From phenotypes to molecules (and vice versa). Trends Ecol. Evol. 11, 168-173.
53. Rajakumar, R., San Mauro, D., Dijkstra, M. B., Huang, M. H., Wheeler, D. E., Hiou- Tim, F., Khila, A., Cournoyea, M. and Abouheif, E. (2012). Ancestral developmental potential facilitates parallel evolution in ants. Science 335, 79-82.
54. Ravosa, M. J., Kunwar, R., Stock, S. R. and Stack, M. S. (2007). Pushing the limit: masticatory stress and adaptive plasticity in mammalian craniomandibular joints. J. Exp. Biol. 210, 628-641.
55. Ravosa, M. J., López, E. K., Menegaz, R. A., Stock, S. R., Stack, M. S. and Hamrick, M. W. (2008). Adaptive plasticity in the mammalian masticatory complex: you are what, and how, you eat. In Primate Craniofacial Function and Biology (ed. C. J. Vinyard, M. J. Ravosa and C. E. Wall), pp. 293-328. New York, NY: Springer.
56. Ravosa, M. J., Ning, J., Costley, D. B., Daniel, A. N., Stock, S. R. and Stack, M. S. (2010a). Masticatory biomechanics and masseter fiber-type plasticity. J. Musculoskelet. Neuronal Interact. 10, 46-55.
57. Ravosa, M. J., Ross, C. F., Williams, S. H. and Costley, D. B. (2010b). Allometry of masticatory loading parameters in mammals. Anat. Rec. 293, 557-571.
58. Relyea, R. A. (2003). Predators come and predators go: The reversibility of predatorinduced traits. Ecology 84, 1840-1848.
59. Rubin, C. T., Bain, S. D. and McLeod, K. J. (1992). Suppression of the osteogenic response in the aging skeleton. Calcif. Tissue Int. 50, 306-313.
60. Ruff, C. B. and Runestad, J. A. (1992). Primate limb bone structural adaptations. Annu. Rev. Anthropol. 21, 407-433.
61. Ruff, C., Holt, B. and Trinkaus, E. (2006). Who's afraid of the big bad Wolff?: "Wolff's law" and bone functional adaptation. Am. J. Phys. Anthropol. 129, 484-498.
62. Scheiner, S. M. (1993). Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35-68.
63. Schlichting, C. D. and Pigliucci, M. (1998). Phenotypic Evolution: A Reaction Norm Perspective. Sunderland, MA: Sinauer Associates.
64. Schwander, T. and Leimar, O. (2011). Genes as leaders and followers in evolution. Trends Ecol. Evol. 26, 143-151.
65. Scott, J. E., McAbee, K. R., Eastman, M. M. and Ravosa, M. J. (2014). Experimental perspective on fallback foods and dietary adaptations in early hominins. Biol. Lett. 10, 20130789.
66. Scoville, A. G. and Pfrender, M. E. (2010). Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl. Acad. Sci. USA 107, 4260- 4263.
67. Serrat, M. A. (2013). Allen's rule revisited: Temperature influences bone elongation during a critical period of postnatal development. Anat. Rec. 296, 1534-1545.
68. Standen, E. M., Du, T. Y. and Larsson, H. C. E. (2014). Developmental plasticity and the origin of tetrapods. Nature 513, 54-58.
69. Suzuki, Y. and Nijhout, H. F. (2006). Evolution of a polyphenism by genetic accommodation. Science 311, 650-652.
70. Svanbäck, R. and Schluter, D. (2012). Niche specialization influences adaptive phenotypic plasticity in the threespine stickleback. Am. Nat. 180, 50-59.
71. Taborsky, B. (2006). The influence of juvenile and adult environments on life-history trajectories. Proc. Biol. Sci. 273, 741-750.
72. Via, S. and Lande, R. (1985). Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39, 505-522.
73. Weijs, W. A. and de Jongh, H. J. (1977). Strain in mandibular alveolar bone during mastication in the rabbit. Arch. Oral Biol. 22, 667-675.
74. Weijs, W. A., Brugman, P. and Grimbergen, C. A. (1989). Jaw movements and muscle activity during mastication in growing rabbits. Anat. Rec. 224, 407-416.
75. West-Eberhard, M. J. (2005). Developmental plasticity and the origin of species differences. Proc. Natl. Acad. Sci. USA 102 Suppl. 1, 6543-6549.
76. Westerlind, K. C., Wronski, T. J., Ritman, E. L., Luo, Z.-P., An, K.-N., Bell, N. H. and Turner, R. T. (1997). Estrogen regulates the rate of bone turnover but bone balance in ovariectomized rats is modulated by prevailing mechanical strain. Proc. Natl. Acad. Sci. USA 94, 4199-4204.