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Fluctuating Asymmetry in the Mammalian Skeleton

Evolutionary and Developmental Implications

  • Chapter
Evolutionary Biology

Part of the book series: Evolutionary Biology ((EBIO,volume 30))

Abstract

The study of developmental instability is an increasingly important topic in the study of the relationship between genotype and phenotype (Graham et al., 19936) as well as that between the developmental and evolutionary processes. The most common measure of developmental instability, fluctuating asymmetry (FA) (Van Valen, 1962), refers to normally distributed deviations across planes of organismal symmetry. Studies of FA have focused on its associations with environmental stress, pathologies and teratologies, phenotypic extremeness, heterozygosity, selection intensity, and sexual selection. These studies have generated a great deal of enthusiasm for the use of FA to infer stress (Clarke and Brand, 1986; Graham et al., 1993a,c,d; Leary and Allendorf, 1989; Manning and Chamberlain, 1994; Noss et al., 1983; Parsons, 1992, 1993), selection intensity (Jones, 1987; Møller and Pomiankowski, 19936), heterozygosity (McManus, 1992; Palmer, 1986), and patterns of sexual selection (Manning and Chamberlain, 1993, 1994; Møller, 1990, 1991, 1992a,c; Møller and Hoglund, 1991; Møller and Pomiankowski, 1993a; Packer and Pusey, 1993; Polak, 1993; Polak and Markow, 1995; Swaddle, 1996; Swaddle and Witter, 1995; Thornhill, 1992a, b; Thornhill and Gangestad, 1996; Thornhill et al., 1995; Watson and Thornhill, 1994) in natural populations. Yet the mechanisms that underlie developmental instability remain largely unknown.

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References

  • Adams, M. S., and Niswander, J. D., 1967, Developmental “noise” and a congenital malformation, Genet Res. 10:131–317.

    Article  Google Scholar 

  • Adkins, R. M., and Honeycutt, R. L., 1992, A molecular examination of archontan and chiropteran monophyly, in: Primates and their Relatives in Phylogenetic perspective (R. D. E. McPhee, ed.), pp. 227–250. New York and London: Plenum Press.

    Google Scholar 

  • Alibert, P., Renaud, S., Dod, B., Bonhomme, F., and Auufray, J.-C., 1994, Fluctuating asymmetry in the Mus musculus hybrid zone: a heterotic effect in disrupted co-adapted genomes, Proc. R. Soc. Lond. Biol, 258:53–59.

    Article  CAS  Google Scholar 

  • Arrieta, M. I., Martinez, B., Nunes, M., Gil, A., Criado, B., Telez, M., and Lostao, C. M., 1995, a-b ridge count in a Basque population: Fluctuating asymmetry and comparison with other populations, Hum. Biol. 67:121–133.

    PubMed  CAS  Google Scholar 

  • Atchley, W. R., and Hall, B. K., 1991, A model for development and evolution of complex morphological structures and its application to the mammalian mandible, Biol. Rev. 66:101–157.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Bader, R.S., 1965, Fluctuating asymmetry in the dentition if the house mouse, Growth 29:291–300.

    PubMed  CAS  Google Scholar 

  • Begun, D. R., 1992, Miocene fossil hominids and the chimp-human clade, Science 257:1929–1933.

    Article  PubMed  CAS  Google Scholar 

  • Begun, D. R., 1994, Relations among the great apes and humans: New interpretations based on the fossil great ape Dryopithecus, Yearb. Phys. Anthropol. 37:11–63.

    Article  Google Scholar 

  • Ben-David, Y., Hershkovitz, I., Rupin, D., and Moscona, D., 1989, Inbreeding effects on tooth size, eruption age, and dental directional and fluctuating asymmetry among South Sinai Bedouins, in: Proceedings, VII International Symposium on Dental Morphology, pp. 5–9.

    Google Scholar 

  • Bertram, J. E. A., and Biewener, A. A., 1988, Bone curvature: Sacrificing strength for load predictability? J. Theor. Biol. 131:75–92.

    Article  PubMed  CAS  Google Scholar 

  • Biemont, C., 1983, Homeostasis, enzymatic heterozygosity and inbreeding depression in natural populations of Drosophila melanogaster, Genetica 61:179–189.

    Google Scholar 

  • Biewener, A. A., and Taylor, C. R., 1986, Bone strain: A determinant of gait and speed? J. Exp. Biol. 123:383–400.

    PubMed  CAS  Google Scholar 

  • Buckler, J., 1990, A Longitudinal Study of Adolescent Growth. Springer-Verlag, London.

    Book  Google Scholar 

  • Cheverud, J. M., Dow, M. M., and Leutenegger, W., 1985, The quantitative assessment of phylogenetic constraints in comprative analyses: Sexual dimorphism in body weight among primates, Evolution 39:1335–1351.

    Article  Google Scholar 

  • Clarke, G. M., 1992, Fluctuating asymmetry: A technique for measuring developmental stress of genetic and environmental origin, Acta Zool. Fenn. 191:31–25.

    Google Scholar 

  • Clarke, G. M., 1993a, Fluctuating asymmetry of invertebrate populations as a biological indicator of environmental quality, Environ. Poll. 82:207–211.

    Article  CAS  Google Scholar 

  • Clarke, G. M., 1993b, The genetic basis of developmental stability. I. Relationships between stability, heterozygosity and genomic coadaptation, Genetica 89:15–23.

    Article  Google Scholar 

  • Clarke, G. M., 1995a, The genetic basis of developmental stability. 2. Asymmetry of extreme phenotypes revisited. Am. Nat. 146:708–725.

    Article  Google Scholar 

  • Clarke, G. M., 1995b, Relationships between developmental stability and fitness: Application for conservation biology, Conserv. Biol. 9:18–24.

    Article  Google Scholar 

  • Clarke, G. M., and Brand, G. W., 1986, Fluctuating asymmetry: A technique for measuring developmental stress caused by inbreeding, Aust. J. Biol. Sci. 39:145–153.

    Google Scholar 

  • Clarke, G. M., and Oldroyd, B. P., 1992, The genetic basis of developmental stability in Apis Mellifera: Heterozygosity versus genie imbalance, Evolution 46:753–762.

    Article  Google Scholar 

  • Collins, J. P., Zerba, K. E., and Sredl, M. J., 1993, Shaping intraspecific variation: Development, ecology and the evolution of morphology and life history variation in tiger salamanders, Genetica 89:167–183.

    Article  Google Scholar 

  • Derting, T. L., 1986, Variation in life-history traits: Relationships between metabolic rate, thyroid gland activity, food processing, growth, and reproduction in the cotton rat (Sigmodon hispidus). Doctoral Dissertation, Indiana University, Bloomington.

    Google Scholar 

  • Dixson, A. F., Gardner, J. S., and Bonney, R. C., 1980, Puberty in the male owl monkey (Aotus trivirgatus griseimembrd): A study of physical and hormonal development, Int. J. Primatol. 1:129–139.

    Article  Google Scholar 

  • Dobzhansky, T., and Wallace, B., 1953, The genetics of homeostasis in Drosophila, Proc. Natl. Acad. Sci. USA 39:162–171.

    Article  CAS  Google Scholar 

  • Doyle, W. J., and Kelley C., 1977, The effects of audiogenic stress on the growth of long bones in the laboratory rat (Rattus norvegiens), Growth 41:183–189.

    CAS  Google Scholar 

  • Druzinsky, R. E., 1993, The time allometry of mammalian chewing movements: Chewing frequency scales with body mass in mammals, J. Theor. Biol. 160:427–440.

    Article  PubMed  CAS  Google Scholar 

  • DuMond, F. W., 1968, The squirrel monkey in a seminatural environment, in: The Squirrel Monkey (L. A. Rosenblum and R. W. Cooper, eds.), pp. 88–146. Academic Press, New York.

    Google Scholar 

  • Emlen, J. M., Freeman, D. C., and Graham, J. H., 1993, Nonlinear growth dynamics and the origin of fluctuating asymmetry, Genetica 89:77–86.

    Article  Google Scholar 

  • Escos, J., Alados, C. L., Emlen, J. M., and Alderstein, S., 1995, Developmental instability in the Pacific hake parasitized by Myxospore and Kudoa spp, Transact. Am. Fisheries Soc. 124:943–945.

    Article  Google Scholar 

  • Falconer, D. S., 1989, Introduction to Quantitative Genetics; John Wiley & Sons, New York.

    Google Scholar 

  • Felsenstein, J., 1985, Phylogenies and the comparative method, Am. Nat. 125:1–15.

    Article  Google Scholar 

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

    Article  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.

    Article  Google Scholar 

  • Fossey, D., 1982, Reproduction among free-living mountain gorillas, Am. J. Primatol. Supplement 1:97–104.

    Article  Google Scholar 

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

    Google Scholar 

  • Frost, H. M., 1983, The skeletal intermediary organization, Met. Bone Dis. Rel. Dis. 4:281–290.

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Garn, S. M., Smith, B. H., and Moyers, R. E., 1980, Structured (patterned) dimensional and developmental dental asymmetry, Proc. Fim. Dent. Soc. 77(l-3):33–36.

    Google Scholar 

  • Gavan, J. A., 1953, Growth and development of the chimpanzee: A longitudinal and comparative study, Hum. Biol. 25:93–145.

    PubMed  CAS  Google Scholar 

  • Gavan, J. A., 1971, Longitudinal, postnatal growth in chimpanzee, in: The Chimpanzee: Behavior, Growth, and Pathology of Chimpanzees (G. H. Bourne, ed.), pp. 47–103. University Park Press, Baltimore.

    Google Scholar 

  • Gijzen, A., and Tijskens, J., 1971, Growth in weight of the lowland gorilla (Gorilla gorilla gorilla) and of the mountain gorilla (Gorilla gorilla beringei), Int. Zool. Yearb. 11:182–193.

    Google Scholar 

  • Gileva, E. A., and Kosereva, N. L., 1994, Decrease in fluctuating asymmetry among house mice in territories polluted with chemical and radioactive mutagens, Russ. J. Ecol. 25:225–228.

    Google Scholar 

  • Gittleman, J. L., and Kot, M., 1990, Adaptation: Statistics and a null model for estimating phylogenetic effects. Sys. Zool. 39:227–241.

    Article  Google Scholar 

  • Goodman, M., Tagle, D. A., Fitch, D. H., Bailey, W., Czelusniak, J., Koop, B. F., Benson, P., and Slightom, J. L., 1990, Primate evolution at the DNA level and a classification of hominoids, J. Mol. Evol. 30:260–266.

    Article  PubMed  CAS  Google Scholar 

  • Graham, J. H., 1992, Genomic coadaptation and developmental stability in hybrid zones, Acta Zool. Fenn. 191:121–131.

    Google Scholar 

  • Graham, J. H., and Felley, J. D., 1985, Genomic coadaptation and developmental stability within introgressed populations of Enneacanthus gloriosus and E. Obesus (Pisces, Centrarchidae), Evolution 39:104–114.

    Article  Google Scholar 

  • Graham, J. H., Emlen, J. H., and Freeman, D.C 1993a Developmental stability and its applications in ecotoxicology, Ecotoxicology 2:175–184.

    Article  Google Scholar 

  • Graham, J. H., Freeman, D. C., and Emlen, J. M., 1993b, Antisymmetry, directional asymmetry, and dynamic morphogenesis, Genetica 89:121–137.

    Article  Google Scholar 

  • Graham, J. H., Freeman, D. C., and Emlen, J. M., 1993c, Developmental stability: A sensitive indicator of populations under stress, in: Environmental Toxicology and Risk Assessment (W. G. Landis, J. S. Hughes, and M. A. Lewis, eds.), pp. 136–158. American Society for Tesing and Materials, Philadelphia.

    Chapter  Google Scholar 

  • Graham, J. H., Roe, K. E., and West, T. B., 1993d, Effects of lead and benzene on the developmental stability of Drosophila melanogaster, Ecotoxicology 2:185–195.

    Article  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Hallgrimsson, B., 1993, Fluctuating asymmetry in Macaca fascicularis: A study of the etiology of developmental noise, Int. J. Primatol. 14:421–443.

    Article  Google Scholar 

  • Hallgrmsson, B., (in press), Ontogenetic patterning of fluctuating asymmetry mammalian bone.

    Google Scholar 

  • Hartl, G. B., Lang, G., Klein, F., and Willing, R., 1991, Relationships between allozymes, heterozygosity, and morphological characters in red deer (Cervus elaphus), and the influence of selective hunting on allele frequency distributions, Heredity 66:343–350.

    Article  PubMed  Google Scholar 

  • Harvey, P. H., and Pagel, M. D., 1991, The Comparative Method in Evolutionary Biology. Oxford University Press, Oxford.

    Google Scholar 

  • Haugen, A. O., 1975, Reproductive performance of white-tailed deer in Iowa, J. Mamm. 56:151–159.

    Article  CAS  Google Scholar 

  • Henneberg, M., and Louw, G. J., 1995, Average menarcheal age of higher socioeconomic status urban cape coloured girls assessed by means of status quo and recall methods, Am. J. Phys. Anthropol. 96:1–5.

    Article  PubMed  CAS  Google Scholar 

  • Herring, S. W., 1985, The ontogeny of mammalian mastication, Am. Zool. 25:339–349.

    Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Horai, S., Satta, Y., Hayasaka, K., Kondo, R., Inoue, T., Ishida, T., Hayashi, S., and Takahata, N., 1992, Man’s place in Hominoidea revealed by mitochondrial DNA genealogy, J. Mol. Evol. 35:32–43.

    Article  PubMed  CAS  Google Scholar 

  • Jokela, P., and Portin, P., 1991, Effect of extra Y chromosome on number and fluctuating asymmetry of sternopleural bristles in Drosophila melanogaster, Hereditas 114:177–187.

    Article  PubMed  CAS  Google Scholar 

  • Jones, J. S., 1987, An asymmetrical view of fitness, Science 325:298–299.

    Google Scholar 

  • Jungers, W. L., 1985, Body size and scaling of limb proportions in primates, in: Size and Scaling in Primate Biology (W. L. Jungers, ed.), pp. 345–382. Plenum Press, New York.

    Google Scholar 

  • Kaack, B., Walker, L., and Brizzee, K. R., 1979, The growth and development of the squirrel monkey (Saimiri sciureus), Growth 43:116–135.

    PubMed  CAS  Google Scholar 

  • Keller, L., and Passera, L., 1993, Incest avoidance, fluctuating asymmetry, and the consequences of inbreeding in Iridomyrmex humilis, an ant with multiple queen colonies, Behav. Ecol. Sociobiol. 33:191–199.

    Article  Google Scholar 

  • Kiebzak, G. M., 1991, Age-related bone changes, Exp. Gerontol. 26:171–187.

    Article  PubMed  CAS  Google Scholar 

  • Kieser, J., and Groenwald, H. T., 1991, Fluctuating odontometric asymmetry, morphological variability, and genetic monomorphism in the cheetah Acinonyx jubatus. Evolution 45:1175–1183.

    Article  Google Scholar 

  • Kieser, J. A., Groenveld, H. T., and Preston, C. N., 1986, Fluctuating dental asymmetry as a measure of ontogenetic canalization in man, Am. J. Phys. Anthropol. 71:437–444.

    Article  PubMed  CAS  Google Scholar 

  • Kirk, J. H., 1972, Growth of maturing Macaca mulatta, Lab. Anim. Sci. 22:573–575.

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kohn, L. A., and Bennet, K. A., 1986, Fluctuating asymmetry in fetuses of diabetic Rhesus Macaques, Am. J. Phys. Anthropol. 71:477–483.

    Article  PubMed  CAS  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.

    Article  Google Scholar 

  • Leamy, L., 1984, Morphometric studies of inbred and hybrid house mice. V. Directional and fluctuating asymmetry, Am. Nat. 123:579–593.

    Article  Google Scholar 

  • Leamy, L., 1992, Morphometric studies of inbred and hybrid house mice. VII. Heterosis in fluctuating asymmetry at different ages, Acta Zool. Fenn. 191:111–119.

    Google Scholar 

  • Leamy, L., 1993, Morphological integration of fluctuating asymmetry in the mouse mandible, Genetica 89:139–153.

    Article  Google Scholar 

  • Leary, R. F., and Allendorf, F. W., 1989, Fluctuating asymmetry as an indicator of stress: Implications for conservation biology, TREE 4:214–217.

    PubMed  CAS  Google Scholar 

  • Leary, R. L., Allendorf, F. W., and Knudsen, K. L., 1983, Developmental stability and enzyme heterozygosity in rainbow trout, Nature 301:71–72.

    Article  PubMed  CAS  Google Scholar 

  • Leary, R. F., Allendorf, F. W., and Knudsen, K. L., 1984, Superior developmental stability of heterozygotes at enzyme loci in salmonid fishes, Am. Nat. 124:540–551.

    Article  Google Scholar 

  • Leary, R. F., Allendorf, F. W., and Knudsen, K. L., 1985, Inheritance of meristic variation and the evolution of developmental stability in the rainbow trout, Evolution 39(2):308–314.

    Article  Google Scholar 

  • Leary, R. F., Allendorf, F. W., and Knudsen, K. L., 1992, Genetic, environmental, and developmental causes of meristic variation in rainbow trout, Acta Zool. Fenn. 191:79–95.

    Google Scholar 

  • Leberg, P., Smith, M. H., and Brisbin, I. L., 1991, Influence of sex, habitat, and genotype on the growth patterns of white-tailed deer, in: The Biology of Deer (R. D. Brown, ed.), pp. 343–350. Springer Verlag, New York.

    Google Scholar 

  • Lerner, I. M., 1954, Genetic Homeostasis. John Wiley & Sons, New York.

    Google Scholar 

  • Levin, D. A., 1970, Developmental instability in species and hybrids of Liatris, Evolution 24:613–624.

    Article  Google Scholar 

  • Livshits, G., and Kobyliansky, E., 1987, Dermatoglyphic traits as possible markers of developmental processes in humans, Am. J. Med. Genet. 26:111–122.

    Article  PubMed  CAS  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.

    PubMed  CAS  Google Scholar 

  • Livshits, G., and Smouse, P. E., 1993, Relationship between fluctuating asymmetry, morphological modality and heterozygosity in an elderly Isreali population, Genetica 89:155–166.

    Article  Google Scholar 

  • Livshits, G., Davidi, L., Kobyliansky, E., Ben-Amitai, D., Levi, Y., and Merlob, P., 1988, Decreased developmental stability as assessed by fluctuating asymmetry of morphometric traits in preterm infants. Am. J. Med. Genet. 29:793–805.

    Article  PubMed  CAS  Google Scholar 

  • Long, J. O., and Cooper, R. W., 1968, Physical growth and dental eruption in captive-bred squirrel monkeys, Saimiri sciureus (Leticia, Columbia), in: The Squirrel Monkey (I. A. Rosenblum and R. W. Cooper, eds.), pp. 193–205. Academic Press, New York.

    Google Scholar 

  • Manning, J. T., and Chamberlain, A. T., 1993, Fluctuating asymmetry, sexual selection and canine teeth in primates, Proc. R. Soc. Lond. [Biol.] 251:83–87.

    Article  CAS  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. [Biol.] 255:189–193.

    Article  CAS  Google Scholar 

  • Manning, J. T., and Ockenden, L., 1994, Fluctuating asymmetry in racehorsesm, Nature 370:185–186.

    Article  PubMed  CAS  Google Scholar 

  • Markow, T. A., and Gottesman, I. I., 1993, Behavioral phenodeviance: A Lerneresque approach, Genetica 89:287–305.

    Google Scholar 

  • Markow, T. A., and Martin, J. F., 1993, Inbreeding and developmental stability in a small human population, Ann. Hum. Biol. 20:389–394.

    Article  PubMed  CAS  Google Scholar 

  • Markow, T. A., and Ricker, J. P., 1991, Developmental stability in hybrids between the sibling species pair, Drosophila melanogaster and Drosophila simulans, Genetica. 84:115–121.

    Article  PubMed  CAS  Google Scholar 

  • Markow, T. A., and Wandler, K., 1986, Fluctuating dermatoglyphic asymmetry and the genetics of liability to schizophrenia, Psychiatr. Res. 19:323–328.

    Article  CAS  Google Scholar 

  • McManus, I. C., 1992, Are paw preference differences in HI and LO mice the result of specific genes or of heterosis and fluctuating asymmetry? Behav. Genet. 22:435–451.

    Article  PubMed  CAS  Google Scholar 

  • McNab, B. K., and Eisenberg, J. F., 1989, Brain size and its relation to the rate of metabolism in mammals, Am. Nat. 133:157–167.

    Article  Google Scholar 

  • Mellor, C. S., 1992, Dermatoglyphic evidence of fluctuating asymmetry in schizophrenia, Br. J. Psychiatry. 160:467–472.

    Article  PubMed  CAS  Google Scholar 

  • Meritt, D. A., 1980, Captive reproduction and husbandry of the Douroucouli (Aotus trivirgatus) and the titi monkey (Callicebus sp.), Int. Zoo Yearb. 20:52–59.

    Article  Google Scholar 

  • Mitton, J. B., 1993, Enzyme heterozygosity, metabolism, and developmental stability, Genetica 89:47–65.

    Article  CAS  Google Scholar 

  • Modi, W. S., Wayne, R. K., and O’Brien, S.J., 1987, Analysis of fluctuating asymmetry in cheetahs, Evolution 41:227–228.

    Article  Google Scholar 

  • Mohan, S., and Baylink, D. J., 1991, Bone growth factors, Clin. Orthop. Rel. Res. 263:30–48.

    Google Scholar 

  • Møller, A. P., 1990, Fluctuating asymmetry in male sexual ornaments may reliably reveal male quality, Anim. Behav. 40:1185–1187.

    Article  Google Scholar 

  • Møller, A. P., 1991, Sexual ornament size and the cost of fluctuating asymmetry, Proc. R. Soc. Lond. [Biol.] 243:59–62.

    Article  Google Scholar 

  • Møller, A. P., 1992a, Female swallow preference for symmetrical male sexual ornaments, Nature 357:238–240.

    Article  PubMed  Google Scholar 

  • Møller, A. P., 1992b, Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters, J. Evol. Biol. 5:691–699.

    Article  Google Scholar 

  • Møller, A. P., 1992c, Patterns of fluctuating asymmetry in weapons: Evidence for reliable signalling of quality in beetle horns and bird spurs, Proc. R. Soc. Lond. [Biol.] 248:199–206.

    Article  Google Scholar 

  • Møller, A. P., 1995a, Developmental stability and ideal despotic distribution of blackbirds in a patchy environment, Oikos 72:228–234.

    Article  Google Scholar 

  • Møller, A. P., 1995b, Patterns of fluctuating asymmetry in sexual ornaments of birds from marginal and central populations, Am. Nat. 145:316–327.

    Article  Google Scholar 

  • Møller, A. P., and Hoglund, J., 1991, Patterns of fluctuating asymmetry in avian feather ornaments—Implications for models of sexual selection, Proc R. Soc. Lond. [Biol.] 245:1–5.

    Article  Google Scholar 

  • Møller, A. P., and Pomiankowski, A., 1993a, Fluctuating asymmetry and sexual selection, Genetica 89:267–279.

    Article  Google Scholar 

  • Møller, A. P., and Pomiankowski, A., 1993b, Punctuated equilibria or gradual evolution: Fluctuating asymmetry and variation in the rate of evolution, J. Theor. Biol. 161:359–367.

    Article  PubMed  Google Scholar 

  • Molnar, J. A., Albert, N., Burke, J. F., and Young, V. R., 1986, Regulation of cellular antibody synthesis. Cellular 7S production and longevity of antigen sensitive cells in the absence of antibody feedback, Biochem. J. 240:431–435.

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Moore, W. J., 1967, Muscular function and skull growth in the laboratory rat (Rattus norvegius), J. Zool. 152:287–296.

    Article  Google Scholar 

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

    Article  PubMed  CAS  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: Morphology of the Maxillo-Mandibular Apparatus (G. H. Schumacher, ed.), pp. 160–165. Georg Thieme, Leipzig.

    Google Scholar 

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

    Google Scholar 

  • Moss, M. L., 1975, A functional analysis of centric relation, Den. Clin. North Am. 19:431–442.

    CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Nevo, E., Beiles, A., and Ben-Shlomo, R., 1983, The evolutionary significance of genetic diversity: Ecological, demographic and life history correlates, in: Evolutionary Dynamics of Genetic Diversity (G. S. Mani, ed.), pp. 13–212. Springer-Verlag, Berlin.

    Google Scholar 

  • Newell-Morris, L. L., Fahrenbuch, C. E., and Sackett, G. P., 1989, Prenatal psychological stress, dermatoglyphic asymmetry and pregnancy outcome in the pigtailed macaque (Macaca nemestrina), Biol. Neonate 56:61–75.

    Article  PubMed  CAS  Google Scholar 

  • Niswander, J. D., and Chung, C. S., 1965, The effects of inbreeding on tooth size in Japanese children, Am. J. Hum. Genet. 17:390–399.

    PubMed  CAS  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.

    Article  PubMed  CAS  Google Scholar 

  • Novacek, M. J., 1990, Morphology, paleontology, and the higher clades of mammals, in: Current Mammalogy (H. Genoways, ed.), pp. 46–88. Columbia University Press, New York.

    Google Scholar 

  • Novacek, M. J., 1992, Mammalian phylogeny: Shaking the tree, Nature 356:121–125.

    Article  PubMed  CAS  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 Theriolog. 38:7–18.

    Google Scholar 

  • Opitz, J. M., and Gilbert-Barness, E. F., 1990, Reflections on the pathogenesis of Down syndrome. Am. J. Med. Genet. Suppl. 7:38–51.

    PubMed  CAS  Google Scholar 

  • Packer, C., and Pusey, A. E., 1993, Should a lion change its spots, Nature 362:595.

    Article  PubMed  CAS  Google Scholar 

  • Pagel, M. D., and Harvey, P. H., 1988, Recent developments in the analysis of comparative data, Q. Rev. Biol. 63:413–440.

    Article  PubMed  CAS  Google Scholar 

  • Pagel, M. D., and Harvey, P. H., 1989, Comparative methods for examining adaptation depend on evolutionary models, Fol. Primatol. 53:203–220.

    Article  CAS  Google Scholar 

  • Palmer, A. R., 1986, Inferring levels of genetic variablity in fossils: The link between heterozygosity and fluctuating asymmetry, Paleobiology 12:1–5.

    Google Scholar 

  • Palmer, A. R., 1994, Fluctuating asymmetry analyses: A primer, in: (T. A. Markow, ed.), pp. 355–364. Kluwer Academic Publishers, Dordrecht.

    Google Scholar 

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

    Google Scholar 

  • Palmer, A. R., and Strobeck, C., 1992, Fluctuating asymmetry as a measure of developmental stability: Implications of non-normal distributions and power of statistical tests, Acta Zool. Fenn. 191:57–72.

    Google Scholar 

  • Palmer, A. R., Strobeck, C., and Chippindale, A. K., 1993, Bilateral variation and the evolutionary origin of macroscopic asymmetries, Genetica 89:201–218.

    Article  Google Scholar 

  • Pankakoski, E., Koivisto, I., and Hyrvarinen, H., 1992, Reduced developmental stability as an indicator of heavy metal pollution in the common shrew Sorex araneus. Acta Zool. Fenn. 191:137–144.

    Google Scholar 

  • Parker, L. T., and Leamy, L., 1991. Fluctuating asymmetry of morphometric characters in house mice: The effects of age, sex, and phenotypical extremeness in a randombred population, J. Hered. 82:145–150.

    PubMed  CAS  Google Scholar 

  • Parsons, P. A., 1961, Fly size, emergence time and sternopleural bristle number in Drosophila melanogaster. Heredity 16:455–473.

    Article  Google Scholar 

  • Parsons, P. A., 1962, Maternal age and developmental variability, J. Exp. Biol. 35:251–260.

    Google Scholar 

  • Parsons, P. A., 1992, Fluctuating asymmetry: a biological monitor of environmental and genomic stress. Heredity 68:361–364.

    Article  PubMed  Google Scholar 

  • Parsons, P. A., 1993, Developmental variability and the limits of adaptation: Interactions with stress, Genetica 89:245–253.

    Article  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.

    Article  Google Scholar 

  • Pennisi, E., 1995, Imperfect match: Do ideal mates come in symmetrical packages. Sci. News 147:60–61.

    Article  Google Scholar 

  • Polak, M., 1993, Parasites increase fluctuating asymmetry of male Drosophila nigrospiracula: Implications for sexual selection, Genetica 89:255–265.

    Article  Google Scholar 

  • Polak, M., and Markow, T. A., 1995, Effect of ectoparasitic mites on sexual selection in a Sonoran desert fruit fly, Evolution 49:660–669.

    Article  Google Scholar 

  • Poznanski, A. K., Garn, S. M., Kuhns, L. R., and Shaw, H. A., 1977, Disharmonic skeletal maturation in the congenital malformation syndromes, Birth Defects 13:45–65.

    PubMed  CAS  Google Scholar 

  • Rawlins, R. G., and Kessler, M. J., 1986, Demography of the free-ranging Cayo Santiago macaques, in: The Cayo Santiago Macaques, (R. G. Rawlins and M. J. Kessler, eds.), pp. 47–72. State University of New York Press, Albany.

    Google Scholar 

  • Reeve, E. C. R., 1960, Some genetic tests on asymmetry of sternopleural chaeta number in Drosophila, Genet Res. 1:151–172.

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Riesen, A. H., 1971, Nissen’s observations on the development of sexual behavior in captive-born, nursery-reared chimpanzees, in: The Chimpanzee: Behavior, Growth, and Pathology of Chimpanzees (G. H. Bourne, ed.), pp. 1–18. University Park Press, Baltimore.

    Google Scholar 

  • Riesenfeld, A., Siegel, M. I., Mooney, M. P., Seroky, J. T., and Taylor, A. B., 1991, Effects of perinatal alcohol exposure and dietary calcium supplements on skeletal and dental growth in rats, Acta Anat. 140:1–7.

    Article  PubMed  CAS  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, Mod. Aging Res. 7:53–67.

    CAS  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.

    PubMed  CAS  Google Scholar 

  • Rubin, C. T., and Lanyon, L. E., 1985, Regulation of bone mass by mechanical strain magnitude, Calc. Tissue Int. 37:411–417.

    Article  CAS  Google Scholar 

  • Rubin, C. T., Bain, S. D., and McLeod, K. J., 1992, Suppression of the osteogenic response in the aging skeleton, Calcif. Tissue. Int. 50:306–13.

    Article  PubMed  CAS  Google Scholar 

  • Ruvolo, M., Disotell, T. R., Allard, M. W., Brown, W. M., and Honeycutt, R. L., 1991, Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence, Proc. Natl. Acad. Sci. USA 88:1570–1574.

    Article  PubMed  CAS  Google Scholar 

  • Sacher, G. A., 1959, Relation of lifespan to brain weight and body weight in mammals, CIBA Foundation Symposium on the Lifespan of Animals. Vol. 5: The Lifespan of Animals (G. E. W. Wolstenholme and M. O’Connor, eds.), Churchill: London, pp. 115–133.

    Google Scholar 

  • Sacher, G. A., 1975, Maturation and longevity in relation to cranial capacity in hominoid evolutio, in: Primate Functional Morphology and Evolution, Sacher, G. A., ed.), pp. 417–442. Mouton Paris.

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Sciulli, P. W., Doyle, W. J., Kelley, C., Siegel, P., and Siegel, 1979, The interaction of stressors in the induction of increased levels of fluctuating asymmetry in the laboratory rat, Am. J. Phys. Anthropol. 50:279–284.

    Article  PubMed  CAS  Google Scholar 

  • Shapiro, B. L., 1992, Development of human autosomal aneuploid phenotypes (with an emphasis on Down’s syndrome), Acta Zool. Fenn. 191:97–105.

    Google Scholar 

  • Sibley, C. G., Comstock, J. A., and Ahlquist, J. E., 1990, DNA hybridization evidence of hominoid phylogeny: A reanalysis of the data, J. Mol. Evol. 30:202–236.

    Article  PubMed  CAS  Google Scholar 

  • Siegel, M. I., and Doyle, W. J., 1975a, The differential effects of prenatal postnatal audiogenic stress on fluctuating asymmetry, J. Exp. Zool. 191:211–214.

    Article  PubMed  CAS  Google Scholar 

  • Siegel, M. I., and Doyle, W. J., 1975b, Stress and fluctuating limb asymmetry in various species of rodents, Growth 39:363–369.

    PubMed  CAS  Google Scholar 

  • Siegel, M. I., and Smookler, H. H., 1973, Fluctuating dental asymmetry and audiogenic stress, Growth 37:35–39.

    PubMed  CAS  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 

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

    Article  Google Scholar 

  • Sokal, R. R., and Rholf, F. J., 1981, Biometry. W. H. Freeman, New York.

    Google Scholar 

  • Soulé, M. E., 1979, Heterozygosity and developmental stability: Another look, Evolution 33:396–401.

    Article  Google Scholar 

  • Soulé, M. E., 1982, Allomeric variation 1: The theory and some consequences, Am. Nat. 120(6):751–764.

    Article  Google Scholar 

  • Soulé, M. E., and Cuzin-Roudy, J., 1982, Allomeric variation 2: Developmental instability of extreme phenotypes, Am. Nat. 120:765–786.

    Article  Google Scholar 

  • Sreenivasan, M. A., Bhat, H. R., and Geevarghese, G., 1974, Observations on the reproductive cycle of Cynopterus sphinx sphinx Vahl 1979 (Chiroptera, Pteropidae), J. Mamm. 55:200–202.

    Article  CAS  Google Scholar 

  • Stearns, S. C., 1983, The influence of size and phylogeny on patterns of covariation among life-history traits in mammals, Oikos 41:173–187.

    Article  Google Scholar 

  • Suchentrunk, F., 1993, Variability of minor tooth traits and allozymic diversity in brown hare Lepus europaeus populations, Acta Therio. 38:59–69.

    Google Scholar 

  • Sutoo, D., Akiyama, K., and Takita, H., 1991, Behavioral changes in cold-stressed mice related to a central calcium-dependent catecholamine-synthesizing system. Pharm. Biochem. Behav. 40:423–428.

    Article  CAS  Google Scholar 

  • Swaddle, J. P., 1996, Reproductive success and symmetry in zebra finches, Anim. Behav. 51:203–210.

    Article  Google Scholar 

  • Swaddle, J. P., and Witter, M. S., 1995, Chest plumage, dominance and fluctuating asymmetry in female starlings, Proc. R. Soc. Lond. [Biol.] 260:219–223.

    Article  Google Scholar 

  • Tanner, J. M., and Whitehouse, R. H., 1976, Clinical longitudinal standards for height, weight, height velocity and weight velocity and the stages of puberty, Arch. Dis. Child. 51:170–179.

    Article  PubMed  CAS  Google Scholar 

  • Thornhill, R., 1992a, Female preference for the pheromone of males with low fluctuating asymmetry in the Japanese scorpionfly (Panorpa japonica: Mecoptera), Behav. Ecol. 3:277–283.

    Article  Google Scholar 

  • Thornhill, R., 1992b, Fluctuating asymmetry, interspecific aggression and male mating tactics in two species of Japanese scorpionflies, Behav. Ecol. Sociobiol. 30:357–363.

    Article  Google Scholar 

  • Thornhill, R., and Gangestad, S. W., 1996, The evolution of human sexuality, TREE 11:A98–A102.

    PubMed  CAS  Google Scholar 

  • Thornhill, R., Gangestad, S. W., and Comer, R., 1995, Human female orgasm and mate fluctuating asymmetry, Anim. Behav. 50:1601–1615.

    Article  Google Scholar 

  • Valentine, D. W., and Soule, M. E., 1973, Effects of pp’-DDT on developmental stability of pectoral fin rays in the Grunion, Leuresthes tennuis, Fishery Bull. 71:921–926.

    Google Scholar 

  • Van Valen, L. M., 1962, A study of fluctuating asymmetry, Evolution 16:125–142.

    Article  Google Scholar 

  • Van Valen, L., 1965, The study of morphological integration, Evolution 19:347–349.

    Article  Google Scholar 

  • Vethukhiv, M., 1954, Integration of the genotype in local populations of three speceis of Drosophila, Evolution 8:241–251.

    Google Scholar 

  • Vrijenhoek, R. C., and Lerman, S., 1982, Heterozygosity and developmental stability under sexual selection and asexual breeding systems, Evolution 36:768–776.

    Article  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 mulatto). Am. J. Phys. Anthropol. 23:23–34.

    Article  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 

  • Watson, G. F., 1972, The Litoria ewingi complex (Anura: Hylidae) in south-eastern Australia II. Genetic incompatibility and delimitation of a narrow hybrid zone between L. ewingi and L. paraewingiAust. J. Zool. 20:423–433.

    Article  Google Scholar 

  • Watson, P. J., and Thornhill, R., 1994, Fluctuating asymmetry and sexual selection, TREE 9:21–25.

    PubMed  CAS  Google Scholar 

  • Watts, E. S., 1986, Skeletal development, in: Comparative Primate Biology, Volume 3: Reproduction and Development (W. Dukelow and J. Erwin, eds.), pp. 415–439. Alan R. Liss, New York.

    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.

    Article  Google Scholar 

  • Wilber, E., Newell-Morris, L. L., and Pytkowicz Streissguth, A., 1993, Dermatoglyphic asymmetry in fetal alcohol syndrome, Biol. Neonate 64:1–6.

    Article  PubMed  CAS  Google Scholar 

  • Willig, M. R., and Owen, R. D., 1987, Fluctuating asymmetry in the cheetah: Methodological and interpretive concerns, Evolution 41:225–227.

    Article  Google Scholar 

  • Wooten, M. C., and Smith, M. H., 1986, Fluctuating asymmetry and genetic variability in a natural population of Mus musculus, J. Mamm. 67:725–732.

    Article  Google Scholar 

  • Wootton, J. T., 1986, The effects of body mass, phylogeny, habitat, and trophic level on mammalian age at first reproduction, Evolution 41:132–149.

    Google Scholar 

  • Wright, S., 1977, Evolution and the Genetics of Populations, Volume 3: Experimental Results and Evolutionary Deductions. University of Chicago Press, Chicago.

    Google Scholar 

  • Yablokov, A. V., 1966, Variability of Mammals. Amerind, New Delhi.

    Google Scholar 

  • Zakharov, V. M., 1992, Population phenogenetics: Analysis of developmental stability in natural populations, Acta Zool. Fenn. 191:7–30.

    Google Scholar 

  • Zakharov, V. M., and Graham, J. H. (eds.), 1992, Development stability in natural populations, Acta Zool. Fenn. 191

    Google Scholar 

  • Zakharov, V. M., and Yablokov, A. V., 1990, Skull asymmetry in the baltic grey seal: Effects of environmental pollution, Ambio 19:266–269.

    Google Scholar 

  • Zakharov, V. M., Pankakoski, E., Sheftel, B. I., Peltonen, A., and Hanski, I., 1991, Developmental stability and population dynamics in the common shrew, Sorex Araneus, Am. Nat. 138:797–810.

    Article  Google Scholar 

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

    Benedikt Hallgrímsson

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  1. Queens College, City University of New York, Flushing, New York, USA

    Max K. Hecht

  2. Cornell University, Ithaca, New York, USA

    Ross J. Macintyre

  3. University of California, Riverside, Riverside, California, USA

    Michael T. Clegg

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Hallgrímsson, B. (1988). Fluctuating Asymmetry in the Mammalian Skeleton. In: Hecht, M.K., Macintyre, R.J., Clegg, M.T. (eds) Evolutionary Biology. Evolutionary Biology, vol 30. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-1751-5_6

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