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Developmental origins of variation in human hand preference

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Abstract

Though right-handedness is a prominant characteristic within all human societies, a substantial and stable proportion of individuals are left-handed. Any comprehensive approach to the origin of variation in handedness must account for substantial evidence that left-handedness is associated with reduced fitness, neurodevelopmental disorders, and reduced neuroanatomical asymmetry. In this paper we investigate the hypothesis that developmental instability in early fetal development underlies variation in handedness. In two studies we note an increased incidence of minor physical anomalies (MPAs) and fluctuating asymmetries in both left-handers and extreme right-handers. Moreover, extreme right-handers were more apt to have left-handed parents than moderate right-handers. These data suggest that deviation from moderate right-handedness reflect imprecise expression of a near-universal design due to developmental instability. Preliminary attempts to elucidate the mechanisms underlying developmental instability suggest that both polygenic homozygosity and particular HLA alleles may be important factors. These observations are discussed with respect to current genetic theories of handedness and human evolution.

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References

  • Adams, M. S. & J. D. Niswander, 1970. Developmental noise and a congenital malformation. Genetic Research 10G: 313–317.

    Google Scholar 

  • Alekoumbides, A., 1978. Hemispheric dominance for language: Quantitative aspects. Acta Neurologica Scandinavica 57: 97–140.

    Article  CAS  PubMed  Google Scholar 

  • Anderson R. M. & R. M. May, 1982. Coevolution of hosts and parasites. Parasitology 85: 411–426.

    Article  PubMed  Google Scholar 

  • Annett, M., 1970. A classification of hand preference by association analysis. British Journal of Psychology 61: 303–321.

    CAS  PubMed  Google Scholar 

  • Annett, M., 1985. Left, right, hand, and brain: The right shift theory. Erlbaum Press, New Jersey.

    Google Scholar 

  • Annett, M., 1991. Annotation: Laterality and cerebral dominance. Journal of Childhood Psychology and Psychiatry 32: 219–237.

    CAS  Google Scholar 

  • Annett, M., 1992. Phonological processing and right minus left hand skill. The Quarterly Journal of Experimental Psychology 44A: 33–46.

    Google Scholar 

  • Annett, M. & M. Manning, 1989. The disadvantages of dextrality for intelligence. British Journal of Psychology 80: 213–226.

    PubMed  Google Scholar 

  • Bakan, P., 1990. Nonright-handedness and the continuum of reproductive casualty, pp. 33–74 in Left-handedness: behavioral implications and anomalies, edited by S. Coren. Elsevier, New York.

    Google Scholar 

  • Bishop, D. V. M., 1990. Handedness and developmental disorders. Blackwell Scientific Press, Oxford.

    Google Scholar 

  • Boklage, C. E., 1987. Twinning, nonrighthandedness, and fusion malformations: Evidence for heritable causal elements held in common. American Journal of Medical Genetics 28: 67–84.

    Article  CAS  PubMed  Google Scholar 

  • Boucher, J., 1977. Hand preference in autistic children and their parents. Journal of Autism and Childhood Schizophrenia 7: 177–187.

    Article  CAS  PubMed  Google Scholar 

  • Broman, S. H., P. L. Nichols & W. A. Kennedy, 1975. Preschool IQ: Prenatal and early developmental correlates. Erlbaum, Hillsdale, N. J.

    Google Scholar 

  • Bryden, M. P., 1982. Laterality: Functional asymmetry in the intact brain. Academic Press, New York.

    Google Scholar 

  • Bryden, M. P. & I. C. McManus, 1992. Relations between handedness and immune disorders. Journal of Clinical and Experimental Neuropsychology 14: 89.

    Google Scholar 

  • Campbell, M., B. Geller, A. M. Small, T. A. Petti & S. H. Perris, 1978. Minor physical anomalies in young psychotic children. American Journal of Psychiatry 135: 573–575.

    CAS  PubMed  Google Scholar 

  • Carter-Saltzman, L., 1980. Biological and socio-cultural effects on handedness: Comparison between biological and adoptive families. Science 209: 1263–1265.

    CAS  PubMed  Google Scholar 

  • Colby, K. M. & C. Parkinson, 1977. Handedness in autistic children. Journal of Autism and Childhood Schizophrenia 7: 3–9.

    Article  CAS  PubMed  Google Scholar 

  • Connolly, K. J. & D. V. M. Bishop, 1992. The measurement of handedness: A cross-cultural comparison of samples from England and Papua New Guinea. Neuropsychologia 30: 13–26.

    Article  CAS  PubMed  Google Scholar 

  • Corballis, M. C., 1991. The lopsided ape: Evolution of the the generative mind. Oxford, New York.

    Google Scholar 

  • Coren, S., 1989. Left-handedness and accident risk. American Journal of Public Health 79: 1–2.

    Google Scholar 

  • Coren, S. & D. F. Halpern, 1991. Left-handedness: A marker for decreased survival fitness. Psychological Bulletin 109: 90–106.

    Article  CAS  PubMed  Google Scholar 

  • Coren, S. & C. Porac, 1977. Fifty centuries of right-handedness: The historical record. Science 198: 631–632.

    CAS  PubMed  Google Scholar 

  • Coren, S., A. Searleman & C. Porac, 1986. Rate of physical maturation and handedness. Developmental Neuropsychology 2: 17–23.

    Article  Google Scholar 

  • Craft, S., M. L. Gourovitch, S. B. Dowton, J. M. Swanson & S. Bonforte, 1992. Lateralized deficits in visual attention in males with developmental dopamine depletion. Neuropsychologia 30: 341–351.

    Article  CAS  PubMed  Google Scholar 

  • Cummings, C., D. Flynn & M. Preus, 1982. Increased morphological variants in children with learning disabilities. Journal of Autism and Childhood Schizophrenia 12: 373–383.

    Article  CAS  Google Scholar 

  • Daniel, W. F. & R. A. Yeo, 1991. Left-handedness and accident rates. American Journal of Public Health 81: 1036–1037.

    Google Scholar 

  • Daniel, W. F., R. A. Yeo & S. W. Gangestad, 1992. Left-handers suffer more head injuries than do right-handers. Journal of Clinical and Experimental Neuropsychology 14: 77.

    Google Scholar 

  • Down, J. L. H., 1866. Observations on an ethnic classification of idiots. London Hospital and lecture Reports 3: 259–262.

    Google Scholar 

  • Ellis, L., 1990. Left- and mixed handedness and criminality: Explanations for a probable relationship, pp. 485–508 in Left-handedness: Behavioral implications and anomalies, edited by S. Coren. Elsevier, New York.

    Google Scholar 

  • Falconer, D. S., 1981. Quantitative genetics, 2nd ed. Longman, New York.

    Google Scholar 

  • Fisher, R. A., 1959. The genetical theory of natural selection. Dover, New York.

    Google Scholar 

  • Fleminger, J. J., R. Dalton & K. F. Standage, 1977. Age as a factor in the handedness of adults. Neuropsychologia 15: 471–473.

    Article  CAS  PubMed  Google Scholar 

  • Fraser, F. C., 1983. Association of neural tube defects and parental nonrighthandedness. American Journal of Human Genetics 35: 89.

    Google Scholar 

  • Galaburda, A. M., 1991. Asymmetries of cerebral neuroanatomy, pp. 219–233 in Biological asymmetry and handedness, edited by G. R. Bock and J. Marsh. Wiley, New York.

    Google Scholar 

  • Gangestad, S. W. & R. A. Yeo, (in preparation). Parental handedness and relative hand skill: A test of the developmental instability hypothesis.

  • Gangestad, S. W., R. A. Yeo, W. F. Daniel, P. Shaw & R. Thoma, (in preparation). Association of HLA alleles and handedness.

  • Geschwind, N. W. & A. M. Galaburda, 1987. Cerebral lateralization: Biological mechanisms, associations, and pathology. MIT Press, Cambridge, MA.

    Google Scholar 

  • Gilbert, A. N. & C. J. Wysocki, 1992. Hand preference and age in the United States. Neuropsychologia 30: 601–608.

    Article  CAS  PubMed  Google Scholar 

  • Gualtieri, C. T., A. Adams, C. D. Shen & D. Loiselle, 1982. Minor physical anomalies in alcoholic and schizophrenic adults and hyperactive and autistic children. American Journal of Psychiatry 139: 640–643.

    CAS  PubMed  Google Scholar 

  • Gualtieri, T. & R. E. Hicks, 1985. An immunoreactive theory of selective male affliction. The Behavioral and Brain Sciences 8: 427–441.

    Google Scholar 

  • Guy, S. D., L. V. Majurski, C. J. Wallace & M. P. Guy, 1989. The incidence of minor physical anomalies in adult males schizophrenics. Schizophrenia Bulletin 39: 571–582.

    Google Scholar 

  • Haaland, K. & R. A. Yeo, 1989. Neuropsychological aspects of complex motor control, pp. 219–244 in Neuropsychological function and brain imaging, edited by E. D. Bigler, R. A. Yeo & E. Turkheimer. Plenum, New York.

    Google Scholar 

  • Habib, M., D. Gayraud, A. Oliva, J. Regis, G. Salamon & R. Khalh, 1991. Effects of handedness and sex on the morphology of the corpus callosum: A study with brain resonance imaging. Brain and Cognition 16: 41–61.

    Article  CAS  PubMed  Google Scholar 

  • Halpern, D. F. & S. Coren, 1991. Handedness and lifespan. New England Journal of Medicine 324: 998.

    Article  CAS  PubMed  Google Scholar 

  • Hamilton, W. D., 1982. Pathogens as causes of genetic diversity in their hot populations, pp. 269–296 in Population Biology of Infectious Diseases, edited by R. M. Anderson & R. M. May. Springer-Verlag, New York.

    Google Scholar 

  • Helm-Estabrooks, N., R. A. Yeo, N. Geschwind, M. Freidman & C. Weinstein, 1986. Stuttering: Disappearance and reappearance with acquired brain lesions. Neurology 36: 1109–1112.

    CAS  PubMed  Google Scholar 

  • Hepper, P. G., S. Shahidullah & R. White, 1991. Handedness in the human fetus. Neuropsychologia 28: 1107–1111.

    Article  Google Scholar 

  • Kertesz, A., M. Polk, J. Howell & S. E. Black, 1987. Cerebral dominance, sex, and callosal size in MRI. Neurology 37: 1385–1388.

    CAS  PubMed  Google Scholar 

  • Kat, P. W., 1982. The relationship between heterozygosity for enzyme loci and developmental of aquatic bivalves (Unenidice). American naturalist 119: 824–832.

    Article  Google Scholar 

  • Leary, R. F., F. W. Allendorf & K. L. Knudsen, 1975. Inheritance of meristic variation and the evolution of developmental instability in rainbow trout. Evolution 39: 308–314.

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Leche, S., 1933. Handedness and bimanual dermatoglyphic differences. American Journal of Anatomy 53: 1–53.

    Article  Google Scholar 

  • Leidy, L. E., 1990. Early age at menopause among left-handed women. Obstetrics and Gynecology 76: 1111–1114.

    CAS  PubMed  Google Scholar 

  • Lishman, W. A. & E. R. L. McMeekan, 1976. Hand preference patterns in psychiatric patients. British Journal of Psychiatry 129: 158–166.

    CAS  PubMed  Google Scholar 

  • Livshits, G., L. Davadi, E. Kobyliansky, D. Ben-Amital, Y. Levy & P. Merlob, 1988. Decreased developmental stability as assessed by fluctuating asymmetry of morphometric traits in preterm infants. American Journal of Human Genetics 29: 793–805.

    CAS  Google Scholar 

  • Livshits, G. & E. Kobylianski, 1987. Dermatoglyphic traits as possible markers of developmental processes in humans. American Journal of Medical Genetics 26: 111–122.

    Article  CAS  PubMed  Google Scholar 

  • Livshits, G. & E. Kobyliansky, 1989. Study of genetic variance in the fluctuating asymmetry of anthropomorphic traits. Annals of Human Biology 16: 121–129.

    Article  CAS  PubMed  Google Scholar 

  • Livshits, G. & E. Kobyliansky, 1991. Fluctuating asymmetry as a possible measure of developmental homeostasis in humans: A review. Human Biology 63: 441–446.

    CAS  Google Scholar 

  • London, W. P., 1990. Left-handedness and alcoholism, in Left-handedness: Behavioral implications and anomalies edited by S. Coren. Elsevier, New York.

    Google Scholar 

  • Markow, T. A., 1992a. Genetics and developmental stability: An integrative conjecture on etiology and neurobiology of schizophrenia. Psychological Medicine 22: 295–305.

    Article  CAS  PubMed  Google Scholar 

  • Markow, T. A. (1992b). Human handedness and the concept of developmental instability. Genetica 87: 87–94.

    Article  CAS  PubMed  Google Scholar 

  • Markow, T. A. & I. I. Gottesman, 1989. Fluctuating dermatoglyphic asymmetry in psychotic twins. Psychiatry Research 29: 37–43.

    Article  CAS  PubMed  Google Scholar 

  • Markow, T. & K. Wandler, 1986. Fluctuating asymmetry and the genetics of liability to schizophrenia. Psychiatry Research 19: 323–328.

    Article  CAS  PubMed  Google Scholar 

  • McManus, I. C., 1985. Handedness, language dominance, and aphasia: A genetic model. Psychological Medicine, Monograph Supplement 8. Cambridge University Press, Cambridge.

    Google Scholar 

  • McManus, I. C., 1991. The inheritance of handedness, pp. 251–281 in Biological asymmetry and handedness edited by G. R. Bock & J. Marsh. Wiley, New York.

    Google Scholar 

  • McManus, I. C., B. Murray, K. Doyle & S. Baron-Cohen, 1992. Handedness in childhood autism shows a dissociation of skill and preference. Cortex 28: 373–381.

    CAS  PubMed  Google Scholar 

  • Mednick, S. A., R. A. Machon & M. O. Huttenen, 1988. Adult schizophrenia following prenatal exposure to an influenza epidemic. Archives of General Psychiatry 45: 189–192.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Mitton, J. B. & M. C. Grant, 1984. Associations among protein heterozygosity, growth rate, and developmental homeostasis. Annual Review of Ecology and Systematics 15: 479–499.

    Article  Google Scholar 

  • Møller, A. P., 1991. Parasites differentially increase the degree of fluctuating assymetry in secondary sexual characters. Journal of Evolutionary Biology. (in press).

  • Nasrallah, N. A., K. Keelor & M. McCalley-Winters, 1983. Laterality shift in alcoholic males. Biological Psychiatry 18: 1056–1067.

    Google Scholar 

  • Newman, H. H., 1934. Dermatoglyphics and the problem of handedness. American Journal of Anatomy 55: 277–322.

    Article  Google Scholar 

  • O'Callaghan, E., P. Sham, N. Takei, G. Glover & R. M. Murray, 1991. Schizophrenia after prenatal exposure to 1957 A2 influenza epidemic. Lancet 337: 1248–1250.

    Article  PubMed  Google Scholar 

  • O'Callaghan, M. J., D. I. Tudehope, A. E. Dugdale, H. Mohay, Y. Burns & F. Cook, 1987. Handedness in children with birthweights below 1000g. Lancet 7: 1155.

    Article  Google Scholar 

  • Parsons, P. A., 1990. Fluctuating asymmetry: An epigenetic measure of stress. Biological Review 65: 131–145.

    CAS  Google Scholar 

  • Penrose, L. S., 1954. The distal triradius t on the hands of parents and sibs of mongol imbeciles. Annals of Human Genetics 19: 10–38.

    CAS  PubMed  Google Scholar 

  • Porac, C., S. Coren & P. Duncan, 1980. Life span age trends in laterality. Journal of Gerontology 35: 715–721.

    CAS  PubMed  Google Scholar 

  • Quinn, P. O. & J. L. Rapoport, 1974. Minor physical anomalies and neurologic status in hyperactive boys. Pediatrics 53: 742–747.

    CAS  PubMed  Google Scholar 

  • Rapoport, J. L. & P. O. Quinn, 1975. Minor physical anomalies and early developmental deviation: A major subgroup of hyperactive children. International Journal of Mental Health 4: 29–44.

    Google Scholar 

  • Rife, D. C., 1940. Handedness, with special reference to twins. Genetics 25: 178–186.

    PubMed  CAS  Google Scholar 

  • Rife, D. C., 1955. Hand prints and handedness. American Journal of Human Genetics 28: 41–48.

    Google Scholar 

  • Risch, N. & G. Pringle, 1985. Segregation analysis of human hand preference. Behavior Genetics 15: 385–400.

    Article  CAS  PubMed  Google Scholar 

  • Satz, P., D. L. Orsini, E. Saslow & R. Henry, 1985. The pathological left-handedness syndrome. Brain and Cognition 4: 27–46.

    Article  CAS  PubMed  Google Scholar 

  • Searleman, A., C. Porac & S. Coren, 1989. Relationship between birth order, birth stress, and lateral preference: A critical review. Psychological Bulletin 105: 397–408.

    Article  CAS  PubMed  Google Scholar 

  • Sham, P. C., E. O'Callaghan, N. Takei, G. K. Murray, E. H. Hare & R. M. Murray, 1992. Schizophrenia following prenatal exposure to influenza epidemics between 1939 and 1960. British Journal of Psychiatry 160: 461–466.

    Article  CAS  PubMed  Google Scholar 

  • Smart, J. L., C. Jeffrey & B. A. Richards, 1980. A retrospective study of the relationship between birth history and handedness at six years. Early Human Development 5: 79–88.

    Article  Google Scholar 

  • Soule, M. E., 1982. Allomeric variation. 1. The theory and some consequences. American Naturalist 120: 751–764.

    Article  Google Scholar 

  • Soule, M. E. & J. Couzin-Roudy, 1982. Allomeric variation. 2. Developmental instability of extreme phenotypes. American Naturalist 120: 765–786.

    Article  Google Scholar 

  • Steg, J. P. & J. L. Rapoport, 1975. Minor physical anomalies in normal, neurotic, learning disabled, and severely disturbed children. Journal of Autism and Childhood Schizophrenia 5: 299–307.

    Article  CAS  PubMed  Google Scholar 

  • Tiwari, J. L. & P. I. Terasaki, 1986. HLA and disease associations. Springer-Verlag, New York.

    Google Scholar 

  • Tooby, J., 1982. Pathogens, polymorphism, and the evolution of sex. Journal of Theoretical Biology 97: 557–576.

    Article  CAS  PubMed  Google Scholar 

  • Turkheimer, E., P. Hulick, R. A. Yeo & S. W. Gangestad, (in preparation). Left-handedness and growth: Possible differences in variance and stability.

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

    Article  Google Scholar 

  • Van Valen, L., 1978. The control of handedness. The Behavioral and Brain Sciences 2: 320.

    Article  Google Scholar 

  • Von Hilsheimer, E. & J. Kurko, 1979. Minor physical anomalies in exceptional children. Journal of Learning Disabilities 12: 462–469.

    Article  Google Scholar 

  • Waldrop, M. F. & C. F. Halverson, 1971. Minor physical anomalies and hyperactive behavior in young children, pp. 343–380 in Exceptional Infant: Studies in Abnormality, edited by I. J. Hellmuth. Brunner, Mazel, NY.

    Google Scholar 

  • Waldrop, M. F., C. F. Halverson & K. Shetterly, 1989. Manual for Assessing Minor Physical Anomalies (1989 revision). Unpublished manuscript, University of Georgia.

  • Witelson, S. F., 1980. Neuroanatomical asymmetry in left-handers: A review and implications for functional asymmetry, pp. 79–113 in The Neuropsychology of left-handedness, edited by J. Herron. Academic Press, New York.

    Google Scholar 

  • Witelson, S. F., 1985. The brain connection: The corpus callosum is larger in left-handers. Science 229: 1223–1226.

    Google Scholar 

  • Witelson, S. F., 1989. Hand and sex differences in the isthmus and genu of the human corpus callosum. Brain 112: 799–835.

    PubMed  Google Scholar 

  • Witelson, S. & W. Pallie, 1973. Left hemisphere specialization for language in the newborn: Neuro-anatomical evidence for asymmetry. Brain 96: 641–646.

    CAS  PubMed  Google Scholar 

  • Woods, R. P., 1986. Brain asymmetries in situs inversus. Archives of Neurology 43: 1083–1084.

    CAS  PubMed  Google Scholar 

  • Yeo, R. A., S. W. Gangestad & W. F. Daniel, (1993). Hand preference and developmental instability. Psychobiology 21: 161–168.

    Google Scholar 

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Yeo, R.A., Gangestad, S.W. Developmental origins of variation in human hand preference. Genetica 89, 281–296 (1993). https://doi.org/10.1007/BF02424521

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