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Ontogenetic Patterning of Skeletal Fluctuating Asymmetry in Rhesus Macaques and Humans: Evolutionary and Developmental Implications

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Abstract

I address the question of how fluctuating asymmetry (FA)—the distribution of random deviations from bilateral symmetry—varies ontogenetically in the mammalian skeleton. This question is significant because of the light that such patterns can shed on the causes of variation in developmental stability in bone as well as other structures. Based on large ontogenetic skeletal series of Macaca mulatta and Homo sapiens, I report that the FA variances of skeletal metric traits increase ontogenetically. Coupled with the finding that FA variances also accumulate to greater magnitudes in slower growing mammals, this result is consistent with the hypotheses that FA in bone is primarily caused by (a) cumulative effects of asymmetrical mechanical factors, (b) accumulation of variation in the (local) regulation of growth, or (c) a tendency for bone morphology to drift through undirected remodeling. I discuss the implications of these optional explanations for primate evolution and bone development.

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REFERENCES

  • Atchley, W. R., Gaskins, G. T., and Anderson, D. (1976). Statistical properties of ratios. I. empirical results. Syst. Zool. 25: 137-148.

    Google Scholar 

  • Cheverud, J. M. (1995). Morphological integration in the saddle-back tamarin (Saguinus fuscicollis) cranium. Am. Nat. 145: 63-89.

    Google Scholar 

  • Ferguson, M. M. (1985). Developmental stability of rainbow trout hybrids: Genomic coadaptation or heterozygosity. Evolution 40: 323-330.

    Google Scholar 

  • Finch, J. (1990). Longevity, Senescence and the Genome, University of Chicago Press, Chicago.

    Google Scholar 

  • Fischer, R. B., Meunier, G. F., and White, P. J. (1982). Evidence of laterality in the lowland gorilla. Perc. Motor Skills 54: 1093-1094.

    Google Scholar 

  • Frost, H. M. (1964). The Laws of Bone Structure, Charles C Thomas, Springfield, IL.

    Google Scholar 

  • Garn, S. M., Lewis, A. B., and Kerewsky, R. S. (1967). Buccolingual size asymmetry in the permanent dentition. Angle Orthod. 37: 186-193.

    Google Scholar 

  • Gavan, J. A. (1953). Growth and development of the chimpanzee: A longitudinal and comparative study. Hum. Biol. 25.

  • Gundberg, C. M., Anderson, M., and Dickson, I. (1986). Glycated osteocalcin in human and bovine bone. J. Biol. Chem. 261: 14557-14561.

    Google Scholar 

  • Hall, B. K., and Miyake, T. (1995). How do embryos measure time. In McNamara, K. J. (ed.), Evolutionary Change and Heterochrony, John Wiley & Sons, Chichester, pp. 4-20.

    Google Scholar 

  • Hallgrímsson, B. (1993a). Fluctuating asymmetry in Macaca fascicularis: A study of the etiology of developmental noise. Int. J. Primatol. 14: 421-443.

    Google Scholar 

  • Hallgrímsson, B. (1993b). Fluctuating asymmetry in Macaca fascicularis: Implications for the etiology of developmental noise. Suppl. 16: 102.

    Google Scholar 

  • Hallgrímsson, B. (1995). Fluctuating Asymmetry and Maturational Spans in Mammals: Implications for the Evolution of Prolonged Development in Primates, Ph.D. thesis, University of chicago, Chicago.

    Google Scholar 

  • Hallgrímsson, B. (1997). Fluctuating asymmetry in the mammalian skeleton: Evolutionary and developmental implications. In Hecht, M. K., and Clegg, M. T. (eds.), Evolutionary Biology, Vol. 30, pp. 187-251.

  • Herring, S. (1993). Formation of the vertebrate face: Epigenetic and functional influences. Am. Zool. 33: 472-483.

    Google Scholar 

  • Hershkovitz, I., Livshits, G., Moskona, D., Arensburg, B., and Kobyliansky, E. (1993). Variables affecting dental fluctuating asymmetry in human isolates. Am. J. Phys. Anthropol. 91: 349-365.

    Google Scholar 

  • Katz, D., and Suchey, J. M. (1986). Age determination of the male Os Pubis. 69: 427-435.

    Google Scholar 

  • Kobyliansky, E., and Livshits, G. (1989). Age dependent changes in morphometric and biochemical. Ann. Hum. Biol. 16(3): 237-247.

    Google Scholar 

  • Lande, R. (1977). On comparing coefficients of variation. Syst. Zool. 26: 214-217.

    Google Scholar 

  • Lanyon, L. E. (1992). The success and failure of the adaptive response to functional load-bearing in averting bone fracture. Bone 13: s17-s21.

    Google Scholar 

  • Livshits, G., and Kobyliansky, E. (1991). Fluctuating asymmetry as a possible measure of developmental homeostasis in humans: A review. Hum. Biol. 63: 441-466.

    Google Scholar 

  • Manly, B. F. J. (1991). Randomization and Monte Carlo Methods in Biology, Chapman and Hall, London.

    Google Scholar 

  • Manning, J. T., and Chamberlain, A. T. (1994). Fluctuating asymmetry in Gorilla canines: A sensitive indicator of environmental stress. Proc. R. Soc. Lond. B. Biol. Sci. 255(1343): 189-193.

    Google Scholar 

  • Manning, J. T., and Ockenden, L. (1994). Fluctuating asymmetry in racehorses. Nature 370: 185-186.

    Google Scholar 

  • Miyake, T., Cameron, A. M., and Hall, B. K. (1996). Detailed staging of inbred C57BL/6 mice between Theiler's [1972] stages 18 and 21 (11–13 days of gestation) based on craniofacial development. J. Craniofac. Genet. Dev. Biol. 16: 1-31.

    Google Scholar 

  • Moller, A. P. (1991). Sexual ornament size and the cost of fluctuating asymmetry. Proc. R. Soc. Lond. B 243: 59-62.

    Google Scholar 

  • Moller, A. P., and Hoglund, J. (1991). Patterns of fluctuating asymmetry in avian feather ornaments—Implications for models of sexual selection. Proc R. Soc. Lond. B 245(1312): 1-5.

    Google Scholar 

  • Moore, W. J. (1965). Masticatory function and skull growth. J. Zool. 146: 123-131.

    Google Scholar 

  • Moore, W. J. (1973). An experimental study of the functional components of growth in the rat mandible. Acta Anat. 85: 378-385.

    Google Scholar 

  • Moss, M. L. (1968). The primacy of functional components in orofacial growth. Dent. Pract. 19: 56-73.

    Google Scholar 

  • Moss, M. L. (1972a). functional cranial analysis and the functional matrix. In Schumacher, G.-H. (ed.), Morphology of the Maxillo-Mandibular Apparatus, Veb Georg Thieme, Leipzig, pp. 160-165.

    Google Scholar 

  • Moss, M. L. (1972b). The regulation of skeletal growth. In Goss, R. (ed.), Regulation of Organ and Tissue Growth, Academic Press, New York, pp. 59-66.

    Google Scholar 

  • Moss, M., and Meehan, M.-A. (1970). Functional cranial analysis of the coronoid process in the rat. Acta Anat. 77: 11-24.

    Google Scholar 

  • Nonaka, K., and Nakata, M. (1984). Genetic variation and craniofacial growth in inbred rats. J. Craniofac. Genet. Dev. Biol. 4: 271-302.

    Google Scholar 

  • Noss, J. F., Scott, G. R., Yap Potter, R. H., and Dahlberg, A. (1983). fluctuating asymmetry in molar dimensions and discrete morphological traits in Pima Indians. Am. J. Phys. Anthropol. 61: 437-445.

    Google Scholar 

  • Novak, J. M., Rhodes, O. E., Smith, M. H., and Chesser, R. K. (1993). Morphological asymmetry in mammals: Genetics and homeostasis reconsidered. Acta Theriol. 38: 7-18.

    Google Scholar 

  • Palmer, A. R., and Strobeck, C. (1986). Fluctuating asymmetry: Measurement, analysis, patterns. 17: 391-421.

    Google Scholar 

  • Patterson, B. D., and Patton, J. L. (1990). Fluctuating asymmetry and allozymic heterozygosity among natural populations of pocket gophers (Thomomys bottae'). Biol. J. Linn. Soc. 40:21-36. @ref alpha = Rawlins, R. G., and Kessler, M. J. (1986). Demography of the free-ranging Cayo Santiago macaques. In Rawlins, R. G., and Kessler, M. J. (eds.), The Cayo Santiago Macaques. State University of New York Press, Albany, pp. 47–72.

    Google Scholar 

  • Reeve, E. C. R., and Robertson, F. W. (1953). Analysis of environmental variability in quantitative inheritance. Nature 171: 874-875.

    Google Scholar 

  • Roth, V. L. (1989). Fabricational noise in elephant dentitions. Paleobiology 15: 165-179.

    Google Scholar 

  • Rothstein, M. (1985). The alteration of enzymes in aging. Modern Aging Res. 7: 53-67.

    Google Scholar 

  • Rubin, C. T., and Lanyon, L. E. (1984). Regulation of bone formation by applied dynamic loads. J. Bone Joint. Surg. 66A: 397-402.

    Google Scholar 

  • Sacher, G. A. (1959). Relation of lifespan to brain weight and body weight in mammals. GIBA Foundation Symposium on the Lifespan of Animals.

  • Sacher, G. A. (1975). Maturation and longevity in relation to cranial capacity in hominoid evolution. In Tuttle, R. H. (ed.), Primate Functional Morphology and Evolution, Mouton, The Hague, Paris, pp. 417-442.

    Google Scholar 

  • Saunders, S. R., and Mayhall, J. T. (1982). Fluctuating asymmetry of dental morphological traits: New interpretations. Hum. Biol. 54: 789-799.

    Google Scholar 

  • Schmalhausen, I. I. (1949). Factors of Evolution, University of Chicago Press, Chicago.

    Google Scholar 

  • Siegel, M. I., Mooney, M. P., and Taylor, A. B. (1992). Dental and skeletal reduction as a consequence of environmental stress. Acta Zool. Fenn. 191: 145-149.

    Google Scholar 

  • Simmons, K. (1929). Cranial capacities by both plastic and water techniques with cranial linear measurements of the Reserve collection; White and Negro. Hum. Biol. 473-498.

  • Smith, B. H. (1991). Dental development and the evolution of life history in Hominidae. Am. J. Phys. Anthropol. 86: 157-174.

    Google Scholar 

  • Sokal, R. R., and Rohlf, F. J. (1981). Biometry, W. H. Freeman;, New York.

    Google Scholar 

  • Tanner, J. M. (1978). Fetus into Man, Harvard University Press, Cambridge, MA.

    Google Scholar 

  • Van Valen, L. M. (1962). A study of fluctuation asymmetry. Evolution 16: 125-142.

    Google Scholar 

  • Van Valen, L. M. (1978). The statistics of variation. Evol. Theory 4: 33-43.

    Google Scholar 

  • Waddington, C. H. (1957). The Strategy of the Genes, Macmillan, New York.

    Google Scholar 

  • Wagenen, G. V., and Catchpole, H. R. (1956). Growth of the fetus and placenta of the monkey (Macaca mulatta). Am. J. Phys. Anthropol. 23: 23-34.

    Google Scholar 

  • Wakefield, J., Harris, K., and Markow, T. A. (1993). Parental age and developmental stability in Drosophila melanogaster. Genetica 89: 235-244.

    Google Scholar 

  • Watts, E. S. (1986). Skeletal development. In Dukelow, W., and Erwin, J. (eds.), Comparative Primate Biology, Vol. 3. Reproduction and Development, Alan R. Liss, New York, 415-439.

    Google Scholar 

  • Wayne, R. K., Modi, W. S., and O'Brien, S. J. (1986). Morphological variability and asymmetry in the cheetah (Acinonyx jubatus), A genetically uniform species. Evolution 40: 78-85.

    Google Scholar 

  • Wootton, J. T. (1986). The effects of body mass, phylogeny, habitat, and trophic level on mammalian age at first reproduction. Evolution 41: 732-749.

    Google Scholar 

  • Zakharov, V. M. (1992). Population phenogenetics: Analysis of developmental stability in natural populations. Acta Zool. Fennica 191: 7-30.

    Google Scholar 

  • Zelditch, M. L., Bookstein, F. L., and Lundrigan, B. L. (1992). Ontogeny of integrated skull growth in the cotton rat Sigmodon fulviventer. Evolution 46: 1164-1180.

    Google Scholar 

  • Zelditch, M. L., Bookstein, F. L., and Lundrigan, B. L. (1993). The ontogenetic complexity of developmental constraints. J. Evol. Biol. 6: 621-641.

    Google Scholar 

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  1. Department of Anatomy, University of Puerto Rico, Medical Sciences Campus, San Juan, Puerto Rico, 00936-5067

    Benedikt Hallgrímsson

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Hallgrímsson, B. Ontogenetic Patterning of Skeletal Fluctuating Asymmetry in Rhesus Macaques and Humans: Evolutionary and Developmental Implications. International Journal of Primatology 20, 121–151 (1999). https://doi.org/10.1023/A:1020540418554

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