Behave: The Biology of Humans at Our Best and Worst

by Robert M. Sapolsky

  ADHD and autism: D. McFadden et al., “Physiological Evidence of Hypermasculination in Boys with the Inattentive Subtype of ADHD,” Clinical Neurosci Res 5 (2005): 233; M. Martel et al., “Masculinized Finger-Length Ratios of Boys, but Not Girls, Are Associated with Attention-Deficit/Hyperactivity Disorder,” Behavioral Neuroscience 122 (2008): 273; J. Manning et al., “The 2nd to 4th Digit Ratio and Autism,” Development Medicine Child Neurology 43 (2001): 160.

  Depression and anxiety: A. Bailey et al., “Depression in Men Is Associated with More Feminine Finger Length Ratios,” Pers Individ Diff 39 (2005): 829; M. Evardone et al., “Anxiety, Sex-linked Behavior, and Digit Ratios,” Arch Sex Behav. 38 (2009): 442–55.

  Dominance: N. Neave et al., “Second to Fourth Digit Ratio, Testosterone and Perceived Male Dominance,” Proc Royal Society B 270 (2003): 2167.

  Handwriting: J. Beech et al., “Do Differences in Sex Hormones Affect Handwriting Style? Evidence from Digit Ratio and Sex Role Identity as Determinants of the Sex of Handwriting,” Pers Individ Diff 39 (2005): 459.

  Sexual orientation: K. Hirashi et al., “The Second to Fourth Digit Ratio in a Japanese Twin Sample: Heritability, Prenatal Hormone Transfer, and Association with Sexual Orientation,” Arch Sex Behav 41 (2012): 711; A. Churchill et al., “The Effects of Sex, Ethnicity, and Sexual Orientation on Self-Measured Digit Ratio,” Arch Sex Behav 36 (2007): 251.

  Findings from females regarding autism: J. Manning et al., “The 2nd to 4th Digit Ratio and Autism,” Dev Med Child Neurol 43 (2001): 160.

  Anorexia: S. Quinton et al., “The 2nd to 4th Digit Ratio and Eating Disorder Diagnosis in Women,” Pers Individ Diff 51 (2011): 402.

  Handedness: B. Fink et al., “2nd to 4th Digit Ratio and Hand Skill in Austrian Children,” Biol Psychology 67 (2004): 375.

  Sexual orientation and sexual behavior: T. Grimbos et al., “Sexual Orientation and the 2nd to 4th Finger Length Ratio: A Meta-Analysis in Men and Women,” Behav Neurosci 124 (2010): 278; W. Brown et al., “Differences in Finger Length Ratios Between Self-Identified ‘Butch’ and ‘Femme’ Lesbians,” Arch Sex Behav 31 (2002): 123.

  73.Footnote: A. Lamminmaki et al., “Testosterone Measured in Infancy Predicts Subsequent Sex-Typed Behavior in Boys and in Girls,” Horm Behav 61 (2012): 611; G. Alexander and J. Saenz, “Early Androgens, Activity Levels and Toy Choices of Children in the Second Year of Life,” Horm Behav 62 (2012): 500.

  74.B. Heijmans et al., “Persistent Epigenetic Differences Associated with Prenatal Exposure to Famine in Humans,” PNAS 105 (2008): 17046.

  75.For a great review, see D. Moore, The Developing Genome: An Introduction to Behavioral Genetics. (Oxford: Oxford University Press, 2015).

  76.Weaver et al., “Epigenetic Programming by Maternal Behavior,” Nature Neurosci 7 (2004): 847; R. Sapolsky, “Mothering Style and Methylation,” Nature Neurosci 7 (2004): 791; D. Francis et al., “Nongenomic Transmission Across Generations of Maternal Behavior and Stress Response in the Rat,” Science 286 (2004): 1155.

  77.N. Provencal et al., “The Signature of Maternal Rearing in the Methylome in Rhesus Macaque Prefrontal Cortex and T Cells,” J Neurosci 32 (20120: 15626; T. L. Roth et al., “Lasting Epigenetic Influence of Early-Life Adversity on the BDNF Gene,” BP 65 (2009): 760; E. C. Braithwaite et al., “Maternal Prenatal Depressive Symptoms Predict Infant NR3C1 1F and BDNF IV DNA Methylation,” Epigenetics 10 (2015): 408; C. Murgatroyd et al., “Dynamic DNA Methylation Programs Persistent Adverse Effects of Early-Life Stress,” Nat Nsci 12 (2009): 1559; M. J. Meaney and M. Szyf, “Environmental Programming of Stress Responses Through DNA Methylation: Life at the Interface Between a Dynamic Environment and a Fixed Genome,” Dialogues in Clin Neuroscience 7 (2005): 103; P. O. McGowan et al., “Broad Epigenetic Signature of Maternal Care in the Brain of Adult Rats,” PLoS ONE 6 (2011): e14739; D. Liu et al., “Maternal Care, Hippocampal Glucocorticoid Receptors, and Hypothalamic-Pituitary-Adrenal Responses to Stress,” Sci 277 (1997): 1659; T. Oberlander et al., “Prenatal Exposure to Maternal Depression, Neonatal Methylation of Human Glucocorticoid Receptor Gene (NR3C1) and Infant Cortisol Stress Responses,” Epigenetics 3 (2008): 97; F. A. Champagne, “Epigenetic Mechanisms and the Transgenerational Effects of Maternal Care,” Front Neuroendocrinology 29 (2008): 386; J. P. Curley et al., “Transgenerational Effects of Impaired Maternal Care on Behaviour of Offspring and Grandoffspring,” Animal Behav 75 (2008): 1551; J. P. Curley et al., “Social Enrichment During Postnatal Development Induces Transgenerational Effects on Emotional and Reproductive Behavior in Mice,” Front Behav Nsci 3 (2009): 1; F. A. Champagne, “Maternal Imprints and the Origins of Variation,” Horm Behav 60 (2011): 4; F. A. Champagne and J. P. Curley, “Epigenetic Mechanisms Mediating the Long-Term Effects of Maternal Care on Development,” Nsci Biobehav Rev 33 (2009): 593; F. A. Champagne et al., “Maternal Care Associated with Methylation of the Estrogen Receptor-alpha1b Promoter and Estrogen Receptor-Alpha Expression in the Medial Preoptic Area of Female Offspring,” Endo 147 (2006): 2909; F. A. Champagne and J. P. Curley, “How Social Experiences Influence the Brain,” Curr Opinion in Neurobiol 15 (2005): 704.

  Chapter 8: Back to When You Were Just a Fertilized Egg

  1.Footnote: E. Suhay and T. Jayaratne, “Does Biology Justify Ideology? The Politics of Genetic Attribution,” Public Opinion Quarterly (2012): doi:10.1093/poq/nfs049. See also M. Katz, “The Biological Inferiority of the Undeserving Poor,” Social Work and Soc 11 (2013): 1.

  2.E. Uhlmann et al., “Blood Is Thicker: Moral Spillover Effects Based on Kinship,” Cog 124 (2012): 239.

  3.E. Pennisi, “ENCODE Project Writes Eulogy for Junk DNA,” Sci 337 (2012): 1159.

  4.M. Bastepe, “The GNAS Locus: Quintessential Complex Gene Encoding Gsa, XLas, and Other Imprinted Transcripts,” Curr Genomics 8 (2007): 398.

  5.Y. Gilad et al., “Expression Profiling in Primates Reveals a Rapid Evolution of Human Transcription Factors,” Nat 440 (2006): 242.

  6.D. Moore, The Developing Genome: An Introduction to Behavioral Genetics (Oxford: Oxford University Press, 2015); H. Wang et al., “Histone Deacetylase Inhibitors Facilitate Partner Preference Formation in Female Prairie Voles,” Nat Nsci 16 (2013): 919.

  7.I. Weaver et al., “Epigenetic Programming by Maternal Behavior,” Nat Nsci 7 (2004): 847.

  8.Y. Wei et al., “Paternally Induced Transgenerational Inheritance of Susceptibility to Diabetes in Mammals,” PNAS 111 (2014): 1873; M. Anway et al., “Epigenetic Transgenerational Actions of Endocrine Disruptors and Male Fertility,” Sci 308 (2005): 1466; K. Siklenka et al., “Disruption of Histone Methylation in Developing Sperm Impairs Offspring Health Transgenerationally,” Sci 350 (2016): 651. For the controversy, see J. Kaiser, “The Epigenetics Heretic,” Sci 343 (2014): 361.

  9.E. Jablonka and M. Lamb, Epigenetic Inheritance and Evolution: The Lamarckian Dimension (Oxford: Oxford University Press, 1995).

  10.E. T. Wang et al., “Alternative Isoform Regulation in Human Tissue Transcriptomes,” Nat 456 (2008): 470; Q. Pan et al., “Deep Surveying of Alternative Splicing Complexity in the Human Transcriptome by High-Throughput Sequencing,” Nat Gen, 40 (2008): 1413.

  11.A. Muotri et al., “Somatic Mosaicism in Neuronal Precursor Cells Mediated by L1 Retrotransposition,” Nat 435 (2005): 903; P. Perrat et al., “Transposition-Driven Genomic Heterogeneity in the Drosophila Brain,” Sci 340 (2013): 91; G. Vogel, “Do Jumping Genes Spawn Diversity?” Sci 332 (2011): 300; J. Baillie et al., “Somatic Retrotransposition Alters the Genetic Landscape of the Human Brain,” Nat 479 (2011): 534.

  12.A. Eldar and M. Elowitz, “Functional Roles for Noise in Genetic Circuits,” Nat 467 (2010): 167; C. Finch and T. Kirkwood, Chance, Development, and Aging (Oxford: Oxford University Press, 2000).

  13.Some of the early, classic adoption studies: L. L. Heston, “Psychiatric Disorders in Foster Home Reared Children of Schizophrenic Mothers,” Brit J Psychiatry 112 (1
966): 819; S. Kety et al., “Mental Illness in the Biological and Adoptive Families of Adopted Schizophrenics,” Am J Psychiatry 128 (1971): 302; D. Rosenthal et al., “The Adopted-Away Offspring of Schizophrenics,” Am J Psychiatry 128 (1971): 307.

  14.For an extraordinary example of a mix-up of babies shortly after birth, and the implications, see S. Dominus, “The Mixed-Up Brothers of Bogotá,” New York Times Magazine, July 9, 2015, www.nytimes.com/2015/07/12/magazine/the-mixed-up-brothers-of-bogota.html.

  15.R. Ebstein et al., “Genetics of Human Social Behavior,” Neuron 65 (2008): 831; S. Eisen et al., “Familial Influence on Gambling Behavior: An Analysis of 3359 Twin Pairs,” Addiction 93 (1988): 1375. Footnote: W. Hopkins et al., “Chimpanzee Intelligence Is Heritable,” Curr Biol 24 (2014): 1649.

  16.T. Bouchard and M. McGue, “Genetic and Environmental Influences on Human Psychological Differences,” J Neurobiol 54 (2003): 4; D. Cesarini et al., “Heritability of Cooperative Behavior in the Trust Game,” PNAS 105 (2008): 3721; S. Zhong et al., “The Heritability of Attitude Toward Economic Risk,” Twin Res and Hum Genetics 12 (2009): 103; D. Cesarini et al., “Genetic Variation in Financial Decision-Making,” J the Eur Economic Association 7 (2010): 617.

  17.K. Verweij et al., “Shared Aetiology of Risky Sexual Behaviour and Adolescent Misconduct: Genetic and Environmental Influences,” Genes, Brain and Behav 8 (2009): 107; K. Verweij et al., “Genetic and Environmental Influences on Individual Differences in Attitudes Toward Homosexuality: An Australian Twin Study,” Behav Genetics 38 (2008): 257.

  18.K. Verweij et al., “Evidence for Genetic Variation in Human Mate Preferences for Sexually Dimorphic Physical Traits. PLoS ONE 7 (2012): e49294; K. Smith et al., “Biology, Ideology and Epistemology: How Do We Know Political Attitudes Are Inherited and Why Should We Care?” Am J Political Sci 56 (2012): 17; K. Arceneaux et al., “The Genetic Basis of Political Sophistication,” Twin Res and Hum Genetics 15 (2012): 34; J. Fowler and D. Schreiber, “Biology, Politics, and the Emerging Science of Human Nature,” Sci 322 (2008): 912.

  19.J. Ray et al., “Heritability of Dental Fear,” J Dental Res 89 (2010): 297; G. Miller et al., “The Heritability and Genetic Correlates of Mobile Phone Use: Twin Study of Consumer Behavior,” Twin Res and Hum Genetics 15 (2012): 97.

  20.L. Littvay et al., “Sense of Control and Voting: A Genetically-Driven Relationship,” Soc Sci Quarterly 92 (2011): 1236; J. Harris, The Nurture Assumption: Why Children Turn Out the Way They Do (NY: Free Press, 2009); A. Seroczynski et al., “Etiology of the Impulsivity/Aggression Relationship: Genes or Environment?” Psychiatry Res 86 (1999): 41; E. Coccaro et al., “Heritability of Aggression and Irritability: A Twin Study of the Buss-Durkee Aggression Scales in Adult Male Subjects,” BP 41 (1997): 273.

  21.E. Hayden, “Taboo Genetics,” Nat 502 (2013): 26.

  22.Some strong criticisms of twin and adoption approaches: R. Rose, “Genes and Human Behavior,” Ann Rev Psych 467 (1995): 625; J. Joseph, “Twin Studies in Psychiatry and Psychology: Science or Pseudoscience?” Psychiatric Quarterly 73 (2002): 71; K. Richardson and S. Norgate, “The Equal Environments Assumption of Classical Twin Studies May Not Hold,” Brit J Educational Psych 75 (2005): 339; R. Fosse et al., “A Critical Assessment of the Equal-Environment Assumption of the Twin Method for Schizophrenia,” Front Psychiatry 6 (2015): 62; A. V. Horwitz et al., “Rethinking Twins and Environments: Possible Social Sources for Assumed Genetic Influences in Twin Research,” J Health and Soc Behav 44 (2003): 111.

  23.Work of some of the most prominent defenders of the approaches:

  Kenneth Kendler: K. S. Kendler, “Twin Studies of Psychiatric Illness: An Update,” AGP 58 (2001): 1005; K. S. Kendler et al., “A Test of the Equal-Environment Assumption in Twin Studies of Psychiatric Illness,” Behav Genetics 23 (1993): 21; K. S. Kendler and C. O. Gardner Jr., “Twin Studies of Adult Psychiatric and Substance Dependence Disorders: Are They Biased by Differences in the Environmental Experiences of Monozygotic and Dizygotic Twins in Childhood and Adolescence?” Psych Med 8 (1998): 625; K. S. Kendler et al., “A Novel Sibling-Based Design to Quantify Genetic and Shared Environmental Effects: Application to Drug Abuse, Alcohol Use Disorder and Criminal Behavior,” Psych Med 46 (2016): 1639; K. S. Kendler et al., “Genetic and Familial Environmental Influences on the Risk for Drug Abuse: A National Swedish Adoption Study,” AGP 69 (2012): 690; K. S. Kendler et al., “Tobacco Consumption in Swedish Twins Reared Apart and Reared Together,” AGP 57 (2000): 886.

  Thomas Bouchard: Y. Hur and T. Bouchard, “Genetic Influences on Perceptions of Childhood Family Environment: A Reared Apart Twin Study,” Child Development 66 (1995): 330; M. McGue and T. J. Bouchard, “Genetic and Environmental Determinants of Information Processing and Special Mental Abilities: A Twin Analysis,” in Advances in the Psychology of Hum Intelligence, ed. R. J. Sternberg, vol. 5 (Hillsdale, NJ: Erlbaum, 1989), pp. 7–45; T. J. Bouchard et al., “Sources of Human Psychological Differences: The Minnesota Study of Twins Reared Apart,” Sci 250 (1990): 223.

  Robert Plomin: R. Plomin et al., Behavioral Genetics, 5th ed. (New York: Worth, 2008); K. Hardy-Brown et al., “Selective Placement of Adopted Children: Prevalence and Effects,” J Child Psych and Psychiatry 21 (1980) 143; N. L. Pedersen et al., “Genetic and Environmental Influences for Type A–Like Measures and Related Traits: A Study of Twins Reared Apart and Twins Reared Together,” Psychosomatic Med 51 (1989): 428; N. L. Pedersen et al., “Neuroticism, Extraversion, and Related Traits in Adult Twins Reared Apart and Reared Together,” JPSP 55 (1988): 950.

  Also: E. Coccaro et al., “Heritability of Aggression and Irritability: A Twin Study of the Buss-Durkee Aggression Scales in Adult Male Subjects,” BP 41 (1997): 273; A. Bjorklund et al., “The Origins of Intergenerational Associations: Lessons from Swedish Adoption Data,” Quarterly J Economics 121 (2006): 999; E. P. Gunderson et al., “Twins of Mistaken Zygosity (TOMZ): Evidence for Genetic Contributions to Dietary Patterns and Physiologic Traits,” Twin Res and Hum Genetics 9 (2006): 540; B. N. Sánchez et al., “A Latent Variable Approach to Study Gene-Environment Interactions in the Presence of Multiple Correlated Exposures,” Biometrics 68 (2012): 466.

  24.Evidence that chorionic status is a meaningful variable: M. Melnick et al., “The Effects of Chorion Type on Variation in IQ in the NCPP Twin Population,” Am J Hum Genetics 30 (1978): 425; N. Jacobs et al., “Heritability Estimates of Intelligence in Twins: Effect of Chorion Type,” Behav Genetics 31 (2001): 209; M. Melnick et al., “The Effects of Chorion Type on Variation in IQ in the NCPP Twin Population,” Am J Hum Genetics 30 (1978): 425; R. J. Rose et al., “Placentation Effects on Cognitive Resemblance of Adult Monozygotes,” in Twin Research 3: Epidemiological and Clinical Studies, ed. L. Gedda et al. (New York: Alan R. Liss, 1981), p. 35; K. Beekmans et al., “Relating Type of Placentation to Later Intellectual Development in Monozygotic (MZ) Twins (Abstract),” Behav Genetics 23 (1993): 547; M. Carlier et al., “Manual Performance and Laterality in Twins of Known Chorion Type,” Behav Genetics 26 (1996): 409.

  Mixed findings: L. Gutknecht et al. “Long-Term Effect of Placental Type on Anthropometrical and Psychological Traits Among Monozygotic Twins: A Follow Up Study,” Twin Res 2 (1999): 212; D. K. Sokol et al., “Intrapair Differences in Personality and Cognitive Ability Among Young Monozygotic Twins Distinguished by Chorion Type,” Behav Genetics 25 (1996): 457; A. C. Bogle et al., “Replication of Asymmetry of a-b Ridge Count and Behavioral Discordance in Monozygotic Twins,” Behav Genetics 24 (1994): 65; J. O. Davis et al., “Prenatal Development of Monozygotic Twins and Concordance for Schizophrenia,” Schizophrenia Bull 21 (1995): 357.

  Evidence against: Y. M. Hur, “Effects of the Chorion Type on Prosocial Behavior in Young South Korean Twins,” Twin Res and Hum Genetics 10 (2007): 773; M. C. Wichers et al., “Chorion Type and Twin Similarity for Child Psychiatric Symptoms,” AGP 59 (2002): 562; P. Welch et al., “Placental Type and Bayley Mental Development Scores in 18 Mont
h Old Twins,” in Twin Research: Psychology and Methodology, ed. L. Gedda et al. (New York: Alan R Liss, 1978), pp. 34–41.

  Quote from: C. A. Prescott et al., “Chorion Type as a Possible Influence on the Results and Interpretation of Twin Study Data,” Twin Res 2 (1999): 244.

  25.R. Simon and H. Alstein, Adoption, Race and Identity: From Infancy to Young Adulthood (New Brunswick, NJ: Transaction Publishers, 2002); Child Welfare League of America, Standards of Excellence: Standards of Excellence for Adoption Services, rev. ed. (Washington, DC: Child Welfare League of America, 2000); M. Bohman, Adopted Children and Their Families: A Follow-up Study of Adopted Children, Their Background, Environment and Adjustment (Stockholm: Proprius, 1970).

  26.L. J. Kamin and A. S. Goldberger, “Twin Studies in Behavioral Research: A Skeptical View,” Theoretical Population Biol 61 (2002): 83.

  27.M. Stoolmiller, “Correcting Estimates of Shared Environmental Variance for Range Restriction in Adoption Studies Using a Truncated Multivariate Normal Model,” Behav Gen 28 (1998) 429; M. Stoolmiller, “Implications of Restricted Range of Family Environments for Estimates of Heritability and Nonshared Environment in Behavior-Genetic Adoption Studies,” Psych Bull 125 (1999): 392; M. McGue et al., “The Environments of Adopted and Non-adopted Youth: Evidence on Range Restriction from the Sibling Interaction and Behavior Study (SIBS),” Behav Gen 37 (2007): 449.

  28.R. Ebstein et al., “Genetics of Human Social Behavior,” Neuron 65 (2008): 831.

  29.This example comes from N. Block, “How Heritability Misleads About Race,” Cog 56 (1995): 99–128.

  30.D. Moore, The Dependent Gene: The Fallacy of “Nature Versus Nurture” (NY: Holt, 2001); M. Ridley, Nature via Nurture (New York: HarperCollins, 2003); A. Tenesa and C. Haley, “The Heritability of Human Disease: Estimation, Uses and Abuses,” Nat Rev Genetics 14 (2013): 139; P. Schonemann, “On Models and Muddles of Heritability,” Genetica 99 (1997): 97.