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.
Similar content being viewed by others
References
Adams, M. S. & J. D. Niswander, 1970. Developmental noise and a congenital malformation. Genetic Research 10G: 313–317.
Alekoumbides, A., 1978. Hemispheric dominance for language: Quantitative aspects. Acta Neurologica Scandinavica 57: 97–140.
Anderson R. M. & R. M. May, 1982. Coevolution of hosts and parasites. Parasitology 85: 411–426.
Annett, M., 1970. A classification of hand preference by association analysis. British Journal of Psychology 61: 303–321.
Annett, M., 1985. Left, right, hand, and brain: The right shift theory. Erlbaum Press, New Jersey.
Annett, M., 1991. Annotation: Laterality and cerebral dominance. Journal of Childhood Psychology and Psychiatry 32: 219–237.
Annett, M., 1992. Phonological processing and right minus left hand skill. The Quarterly Journal of Experimental Psychology 44A: 33–46.
Annett, M. & M. Manning, 1989. The disadvantages of dextrality for intelligence. British Journal of Psychology 80: 213–226.
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.
Bishop, D. V. M., 1990. Handedness and developmental disorders. Blackwell Scientific Press, Oxford.
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.
Boucher, J., 1977. Hand preference in autistic children and their parents. Journal of Autism and Childhood Schizophrenia 7: 177–187.
Broman, S. H., P. L. Nichols & W. A. Kennedy, 1975. Preschool IQ: Prenatal and early developmental correlates. Erlbaum, Hillsdale, N. J.
Bryden, M. P., 1982. Laterality: Functional asymmetry in the intact brain. Academic Press, New York.
Bryden, M. P. & I. C. McManus, 1992. Relations between handedness and immune disorders. Journal of Clinical and Experimental Neuropsychology 14: 89.
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.
Carter-Saltzman, L., 1980. Biological and socio-cultural effects on handedness: Comparison between biological and adoptive families. Science 209: 1263–1265.
Colby, K. M. & C. Parkinson, 1977. Handedness in autistic children. Journal of Autism and Childhood Schizophrenia 7: 3–9.
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.
Corballis, M. C., 1991. The lopsided ape: Evolution of the the generative mind. Oxford, New York.
Coren, S., 1989. Left-handedness and accident risk. American Journal of Public Health 79: 1–2.
Coren, S. & D. F. Halpern, 1991. Left-handedness: A marker for decreased survival fitness. Psychological Bulletin 109: 90–106.
Coren, S. & C. Porac, 1977. Fifty centuries of right-handedness: The historical record. Science 198: 631–632.
Coren, S., A. Searleman & C. Porac, 1986. Rate of physical maturation and handedness. Developmental Neuropsychology 2: 17–23.
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.
Cummings, C., D. Flynn & M. Preus, 1982. Increased morphological variants in children with learning disabilities. Journal of Autism and Childhood Schizophrenia 12: 373–383.
Daniel, W. F. & R. A. Yeo, 1991. Left-handedness and accident rates. American Journal of Public Health 81: 1036–1037.
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.
Down, J. L. H., 1866. Observations on an ethnic classification of idiots. London Hospital and lecture Reports 3: 259–262.
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.
Falconer, D. S., 1981. Quantitative genetics, 2nd ed. Longman, New York.
Fisher, R. A., 1959. The genetical theory of natural selection. Dover, New York.
Fleminger, J. J., R. Dalton & K. F. Standage, 1977. Age as a factor in the handedness of adults. Neuropsychologia 15: 471–473.
Fraser, F. C., 1983. Association of neural tube defects and parental nonrighthandedness. American Journal of Human Genetics 35: 89.
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.
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.
Gilbert, A. N. & C. J. Wysocki, 1992. Hand preference and age in the United States. Neuropsychologia 30: 601–608.
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.
Gualtieri, T. & R. E. Hicks, 1985. An immunoreactive theory of selective male affliction. The Behavioral and Brain Sciences 8: 427–441.
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.
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.
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.
Halpern, D. F. & S. Coren, 1991. Handedness and lifespan. New England Journal of Medicine 324: 998.
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.
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.
Hepper, P. G., S. Shahidullah & R. White, 1991. Handedness in the human fetus. Neuropsychologia 28: 1107–1111.
Kertesz, A., M. Polk, J. Howell & S. E. Black, 1987. Cerebral dominance, sex, and callosal size in MRI. Neurology 37: 1385–1388.
Kat, P. W., 1982. The relationship between heterozygosity for enzyme loci and developmental of aquatic bivalves (Unenidice). American naturalist 119: 824–832.
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.
Leary, R. F., F. W. Allendorf & K. L. Knudsen, 1983. Developmental instability and enzyme heterozygosity in rainbow trout. Nature 301: 71–72.
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.
Leche, S., 1933. Handedness and bimanual dermatoglyphic differences. American Journal of Anatomy 53: 1–53.
Leidy, L. E., 1990. Early age at menopause among left-handed women. Obstetrics and Gynecology 76: 1111–1114.
Lishman, W. A. & E. R. L. McMeekan, 1976. Hand preference patterns in psychiatric patients. British Journal of Psychiatry 129: 158–166.
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.
Livshits, G. & E. Kobylianski, 1987. Dermatoglyphic traits as possible markers of developmental processes in humans. American Journal of Medical Genetics 26: 111–122.
Livshits, G. & E. Kobyliansky, 1989. Study of genetic variance in the fluctuating asymmetry of anthropomorphic traits. Annals of Human Biology 16: 121–129.
Livshits, G. & E. Kobyliansky, 1991. Fluctuating asymmetry as a possible measure of developmental homeostasis in humans: A review. Human Biology 63: 441–446.
London, W. P., 1990. Left-handedness and alcoholism, in Left-handedness: Behavioral implications and anomalies edited by S. Coren. Elsevier, New York.
Markow, T. A., 1992a. Genetics and developmental stability: An integrative conjecture on etiology and neurobiology of schizophrenia. Psychological Medicine 22: 295–305.
Markow, T. A. (1992b). Human handedness and the concept of developmental instability. Genetica 87: 87–94.
Markow, T. A. & I. I. Gottesman, 1989. Fluctuating dermatoglyphic asymmetry in psychotic twins. Psychiatry Research 29: 37–43.
Markow, T. & K. Wandler, 1986. Fluctuating asymmetry and the genetics of liability to schizophrenia. Psychiatry Research 19: 323–328.
McManus, I. C., 1985. Handedness, language dominance, and aphasia: A genetic model. Psychological Medicine, Monograph Supplement 8. Cambridge University Press, Cambridge.
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.
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.
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.
Mellor, C. S., 1992. Dermatoglyphic evidence for fluctuating asymmetry in schizophrenia. British Journal of Psychiatry 160: 467–472.
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.
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.
Newman, H. H., 1934. Dermatoglyphics and the problem of handedness. American Journal of Anatomy 55: 277–322.
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.
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.
Parsons, P. A., 1990. Fluctuating asymmetry: An epigenetic measure of stress. Biological Review 65: 131–145.
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.
Porac, C., S. Coren & P. Duncan, 1980. Life span age trends in laterality. Journal of Gerontology 35: 715–721.
Quinn, P. O. & J. L. Rapoport, 1974. Minor physical anomalies and neurologic status in hyperactive boys. Pediatrics 53: 742–747.
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.
Rife, D. C., 1940. Handedness, with special reference to twins. Genetics 25: 178–186.
Rife, D. C., 1955. Hand prints and handedness. American Journal of Human Genetics 28: 41–48.
Risch, N. & G. Pringle, 1985. Segregation analysis of human hand preference. Behavior Genetics 15: 385–400.
Satz, P., D. L. Orsini, E. Saslow & R. Henry, 1985. The pathological left-handedness syndrome. Brain and Cognition 4: 27–46.
Searleman, A., C. Porac & S. Coren, 1989. Relationship between birth order, birth stress, and lateral preference: A critical review. Psychological Bulletin 105: 397–408.
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.
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.
Soule, M. E., 1982. Allomeric variation. 1. The theory and some consequences. American Naturalist 120: 751–764.
Soule, M. E. & J. Couzin-Roudy, 1982. Allomeric variation. 2. Developmental instability of extreme phenotypes. American Naturalist 120: 765–786.
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.
Tiwari, J. L. & P. I. Terasaki, 1986. HLA and disease associations. Springer-Verlag, New York.
Tooby, J., 1982. Pathogens, polymorphism, and the evolution of sex. Journal of Theoretical Biology 97: 557–576.
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.
Van Valen, L., 1978. The control of handedness. The Behavioral and Brain Sciences 2: 320.
Von Hilsheimer, E. & J. Kurko, 1979. Minor physical anomalies in exceptional children. Journal of Learning Disabilities 12: 462–469.
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.
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.
Witelson, S. F., 1985. The brain connection: The corpus callosum is larger in left-handers. Science 229: 1223–1226.
Witelson, S. F., 1989. Hand and sex differences in the isthmus and genu of the human corpus callosum. Brain 112: 799–835.
Witelson, S. & W. Pallie, 1973. Left hemisphere specialization for language in the newborn: Neuro-anatomical evidence for asymmetry. Brain 96: 641–646.
Woods, R. P., 1986. Brain asymmetries in situs inversus. Archives of Neurology 43: 1083–1084.
Yeo, R. A., S. W. Gangestad & W. F. Daniel, (1993). Hand preference and developmental instability. Psychobiology 21: 161–168.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
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
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02424521