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A Complete Theory of Psychosis and Autism As Diametric Disorders Of BEHAVIORAL AND BRAIN SCIENCES (2008) 31, 241–320 Printed in the United States of America doi:10.1017/S0140525X08004214 Psychosis and autism as diametrical disorders of the social brain Bernard Crespi Killam Research Professor, Department of Biosciences, Simon Fraser University, Burnaby, BC V5A 1S6, Canada [email protected] http://www.sfu.ca/biology/faculty/crespi/ Christopher Badcock Department of Sociology, London School of Economics, London WC2A 2AE, United Kingdom [email protected] http://www.lse.ac.uk/collections/sociology/whoswho/badcock.htm Abstract: Autistic-spectrum conditions and psychotic-spectrum conditions (mainly schizophrenia, bipolar disorder, and major depression) represent two major suites of disorders of human cognition, affect, and behavior that involve altered development and function of the social brain. We describe evidence that a large set of phenotypic traits exhibit diametrically opposite phenotypes in autistic-spectrum versus psychotic-spectrum conditions, with a focus on schizophrenia. This suite of traits is inter-correlated, in that autism involves a general pattern of constrained overgrowth, whereas schizophrenia involves undergrowth. These disorders also exhibit diametric patterns for traits related to social brain development, including aspects of gaze, agency, social cognition, local versus global processing, language, and behavior. Social cognition is thus underdeveloped in autistic-spectrum conditions and hyper-developed on the psychotic spectrum. We propose and evaluate a novel hypothesis that may help to explain these diametric phenotypes: that the development of these two sets of conditions is mediated in part by alterations of genomic imprinting. Evidence regarding the genetic, physiological, neurological, and psychological underpinnings of psychotic-spectrum conditions supports the hypothesis that the etiologies of these conditions involve biases towards increased relative effects from imprinted genes with maternal expression, which engender a general pattern of undergrowth. By contrast, autistic-spectrum conditions appear to involve increased relative bias towards effects of paternally expressed genes, which mediate overgrowth. This hypothesis provides a simple yet comprehensive theory, grounded in evolutionary biology and genetics, for understanding the causes and phenotypes of autistic-spectrum and psychotic-spectrum conditions. Keywords: autism, cognition, genomic conflict, genomic imprinting, hyper-mentalism, psychosis, schizophrenia People divide roughly, it seems to me, into two kinds, or rather a continuum is stretched between two extremes. There are BERNARD CRESPI, Professor of Evolutionary Biology at people people and things people. Simon Fraser University, has authored more than 100 —W. D. Hamilton (2005, p. 205) publications and 4 books in the areas of social behavior, life-history evolution, and evolutionary genetics. He conducted his doctoral work with William Hamilton and Richard Alexander at the University of Michigan, 1. Introduction followed by postdoctoral studies at Oxford and Cornell. Dr. Crespi has received the Theodosius Dobz- We describe a new hypothesis that seeks to conceptually hansky Prize and the E. O. Wilson Award from the unify the analyses of psychosis and autism, two disorders Society for the Study of Evolution; and a Killam Fel- of the human social brain (Burns 2004; 2006a; McAlonan lowship from the Canada Council has allowed him to apply his expertise to the evolution of human cognition et al. 2005). The core of this hypothesis is that psychosis and psychiatric disorders. and autism represent two extremes on a cognitive spec- trum with normality at its center. Social cognition is thus CHRISTOPHER BADCOCK was born in 1946 and studied underdeveloped in autism, but hyper-developed to dys- for his first degree and Ph.D. at the London School of function in psychosis. We also suggest that these forms Economics, where he is now a Reader in the Depart- of deviation from normal social brain development in ment of Sociology. Following a private didactic analysis either direction are mediated in part by alterations in with Anna Freud, he published a number of books and developmental and metabolic systems affected by genomic papers on Freud, evolutionary psychology, and gen- imprinting, notably via effects of genes that are imprinted etics, and is now completing a book on the wider impli- in the brain and in the placenta (Davies et al. 2005; Tycko cations of the theory outlined in this paper. He is author of Evolutionary Psychology: A Critical Intro- & Morison 2002). Genomic imprinting involves a develop- duction (Polity Press, 2000), and currently teaches mental and physiological tug-of-war, in the growing fetus graduate and undergraduate courses on evolution and and child, between the effects of paternally expressed genetics. (maternally “imprinted,” that is, maternally silenced) # 2008 Cambridge University Press 0140-525X/08 $40.00 241 Crespi & Badcock: Psychosis and autism as diametrical disorders of the social brain genes, which favor enhanced growth as well as selfishness development may be social rather than ecological in interactions with the mother, and the effects of mater- (Emery 2000). This idea can be traced to Chance and nally expressed (paternally silenced) genes, which favor Mead (1953), Jolly (1966), Humphrey (1976; 1983), Alex- relatively constrained growth and other traits that tend ander (1989), and Brothers (1990), who have suggested to benefit mothers (Haig 2000b; 2004b). Relatively small that living in large, complex groups, under strong within- genetic or epigenetic disruptions of this tug-of-war may group and between-group social competition for resources increase the fitness of the child or mother, respectively, and mates, has selected for a “social brain,” functionally as in some disorders of placentation mediated by dysregu- designed by evolution mainly for solving social problems. lated imprinting (Haig 1999b; Oudejans et al. 2004); but Recent studies have described how early development larger alterations are pathological, and we hypothesize of components of the social brain is impaired in autism, that they contribute to the development of either autis- which may lead to a cascade of social deficits, and how tic-spectrum disorders (due to a paternal-gene bias) or many of the core features of schizophrenia can also be psychotic-spectrum disorders (due to a maternal-gene understood in terms of dysregulation in multiple aspects bias) via their effects on growth, neurodevelopment, cog- of uniquely human social cognition (Arbib & Mundhenk nition, and behavior. 2005; Baron-Cohen & Belmonte 2005; Benes & Berretta We unpack our hypothesis by first providing a brief back- 2001; Burns 2004; 2006a). These advances have suggested ground on the social brain, and how its development is that autism and schizophrenia are related to one another altered in autism and psychosis. Second, we provide an in some conceptual and etiological ways, because they overview of genomic imprinting and explain Haig’s both involve alterations in recently evolved human social (2000b; 2004b) “conflict theory” for how imprinting has behavior as central features (Burns 2006a). Although evolved. Third, we describe our nosological framework for both disorders can be conceived as dimensional, grading conceptualizing autistic-spectrum conditions and what we more or less finely into normality (e.g., Frith & Happe´ call psychotic-spectrum conditions, and we explain how 2005; see also, Hill & Frith 2003; Linney et al. 2003; the conflict theory of imprinting provides an evolutionary Schu¨ rhoff et al. 2005), the relationship of autistic- basis for elucidating their genetic, epigenetic, and neurode- spectrum conditions with schizophrenia, and other con- velopmental causes. Fourth, we describe how Prader-Willi ditions on the psychotic spectrum, has yet to be explicitly syndrome and Angelman syndrome, which are caused investigated in any detail. We do so here, in the context of by alterations of a region of chromosome 15 harboring evolutionary theory and genetics, with a focus on effects of imprinted genes, provide useful tests of the role of genomic imprinting. imprinted genes in autism and psychosis. Fifth, we contrast autistic-spectrum and psychotic-spectrum conditions for a wide range of anatomical, neurological, developmental, 3. Genomic imprinting cognitive, behavioral, and epidemiological data. Our hypothesis predicts that to the degree that they represent Analysis of the social brain in contemporary neuroscience opposite, generalized disorders, autistic- and psychotic- and psychology is yielding stunning insights into human spectrum conditions should exhibit diametric phenotypes cognition and psychiatric disorders. However, the concep- for traits related to growth, development, and the social tual social brain is not yet an evolutionary brain, because it brain. Finally, we develop a conceptual model for how sex has yet to fully incorporate central features of evolutionary differences interact with genomic-imprinting effects, biology, such as inclusive fitness theory (Foster et al. 2006; which can help to explain some key features of autistic- Hamilton 1964), intragenomic conflict (Burt & Trivers and psychotic-spectrum epidemiology and symptoms. 2006), social-behavioral ecology (e.g., Krebs & Davies We appreciate that autistic-spectrum and psychotic- 1991), sex differences attributable to sex-differential selec- spectrum conditions are each highly heterogeneous, with tive pressures
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