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Resolving the Paradox of Common, Harmful, Heritable Mental Disorders: Which Evolutionary Genetic Models Work Best?

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Resolving the Paradox of Common, Harmful, Heritable Mental Disorders: Which Evolutionary Genetic Models Work Best? BEHAVIORAL AND BRAIN SCIENCES (2006) 29, 385–452 Printed in the United States of America Resolving the paradox of common, harmful, heritable mental disorders: Which evolutionary genetic models work best? Matthew C. Keller Virginia Institute for Psychiatric and Behavioral Genetics, Virginia Commonwealth University, Richmond, VA 23219. [email protected] www.matthewckeller.com Geoffrey Miller Department of Psychology, University of New Mexico, Albuquerque, NM 87131-1161. [email protected] www.unm.edu/psych/faculty/gmiller.html Abstract: Given that natural selection is so powerful at optimizing complex adaptations, why does it seem unable to eliminate genes (susceptibility alleles) that predispose to common, harmful, heritable mental disorders, such as schizophrenia or bipolar disorder? We assess three leading explanations for this apparent paradox from evolutionary genetic theory: (1) ancestral neutrality (susceptibility alleles were not harmful among ancestors), (2) balancing selection (susceptibility alleles sometimes increased fitness), and (3) polygenic mutation-selection balance (mental disorders reflect the inevitable mutational load on the thousands of genes underlying human behavior). The first two explanations are commonly assumed in psychiatric genetics and Darwinian psychiatry, while mutation-selection has often been discounted. All three models can explain persistent genetic variance in some traits under some conditions, but the first two have serious problems in explaining human mental disorders. Ancestral neutrality fails to explain low mental disorder frequencies and requires implausibly small selection coefficients against mental disorders given the data on the reproductive costs and impairment of mental disorders. Balancing selection (including spatio-temporal variation in selection, heterozygote advantage, antagonistic pleiotropy, and frequency-dependent selection) tends to favor environmentally contingent adaptations (which would show no heritability) or high-frequency alleles (which psychiatric genetics would have already found). Only polygenic mutation-selection balance seems consistent with the data on mental disorder prevalence rates, fitness costs, the likely rarity of susceptibility alleles, and the increased risks of mental disorders with brain trauma, inbreeding, and paternal age. This evolutionary genetic framework for mental disorders has wide-ranging implications for psychology, psychiatry, behavior genetics, molecular genetics, and evolutionary approaches to studying human behavior. Keywords: adaptation; behavior genetics; Darwinian psychiatry; evolution; evolutionary genetics; evolutionary psychology; mental disorders; mutation-selection balance; psychiatric genetics; quantitative trait loci (QTL) 1. Introduction schizophrenia often imagine hostile, confusing voices; they have trouble thinking clearly, feeling normal Mental disorders such as schizophrenia, depression, emotions, or communicating effectively; and they tend to phobias, obsessive-compulsive disorder, and mental lose jobs, friendships, and sexual partners. In response, retardation are surprisingly prevalent and disabling. In many people with schizophrenia kill themselves, and a industrialized countries such as the United States, an esti- much larger proportion dies childless. mated 4% of people have a severe mental disorder This is an evolutionary puzzle, because differences in (National Institute of Mental Health 1998), and almost the risk of developing schizophrenia and other common, half of people will meet the criteria for some type of less debilitating mental disorders are due, in large part, to severe mental disorder at some point in their lives differences in people’s genes. Given that natural selection (Kessler et al. 2005). The annual economic costs in treat- has built the most exquisitely complex machinery known to ment and lost productivity are in the hundreds of billions humankind – millions of species of organic life-forms – of dollars (Rice et al. 1992). The less quantifiable personal why do so many people suffer from such debilitating and costs of mental disorders to sufferers, families, and friends heritable mental disorders? If these mental disorders are are even more distressing. For example, schizophrenia as disabling as they appear, natural selection should have affects about 1% of people worldwide (Jablensky et al. eliminated the genetic variants (susceptibility alleles) 1992), typically beginning in early adulthood and often that predispose to them long ago. Does the prevalence following a chronic lifelong course. People with of heritable mental disorders therefore imply that mental # 2006 Cambridge University Press 0140-525X/06 $12.50 385 Keller & Miller: Resolving the paradox of heritable mental disorders disorder susceptibility alleles were selectively neutral or they have proven less important than expected in explain- perhaps even advantageous in the ancestral past, or has ing persistent genetic variation in traits related to fitness. natural selection been unable to remove susceptibility Conversely, the third model – polygenic mutation- alleles for some hidden reason? selection balance – has enjoyed a theoretical and empirical renaissance in evolutionary genetics, but remains obscure and misunderstood in psychiatric genetics and Darwinian psychiatry. 1.1. The goal of this article and who should read it Cross-fertilization between these fields promises not This article tries to develop an understanding of the evol- only to shed light on deep quandaries regarding the utionary persistence of susceptibility alleles underlying origins of mental disorders; it also may help resolve common, heritable, harmful mental disorders. We some ongoing frustrations within each field by guiding compare and contrast the three broadest classes of evol- research and theory more effectively. Evolutionarily utionary genetic models that explain persistent genetic oriented mental health researchers, such as Darwinian variation: ancestral neutrality, balancing selection, and psychiatrists and evolutionary psychologists, often go to polygenic mutation-selection balance. Such models have torturous lengths to find hidden adaptive benefits that been tested mostly by evolutionary geneticists on traits could explain the evolutionary persistence of profoundly such as bristle numbers in fruit flies, survival in nematode harmful mental disorders such as schizophrenia or anor- worms, and growth rates in baker’s yeast. Yet these models exia, but these accounts are often frustratingly implausible make strong, discriminating predictions about the gen- or hard to test. New ideas from evolutionary genetics and etics, phenotypic patterns, and fitness payoffs of any trait data from psychiatric genetics can help this audience in any species, and so should be equally relevant to better understand which evolutionary genetic models are explaining mental disorder susceptibility alleles. theoretically credible and empirically relevant to mental However, these three main models of persistent genetic disorders. variation have never before been directly compared with Many psychiatric and behavioral geneticists try to find regard to their theoretical and empirical adequacy for the specific susceptibility alleles that underlie common, explaining human mental disorders. That is our first harmful, heritable mental disorders. They are often fru- main goal. strated that even the most promising loci explain little Our second main goal is to promote more consilience overall population risk and rarely replicate across studies among evolutionary genetics, human behavioral/psychia- or populations. Traditional methods for gene hunting tric genetics, and Darwinian psychiatry/evolutionary implicitly assume that mental disorder susceptibility psychology. Trying to integrate these disparate fields is alleles will be at relatively high frequencies and common hard, not just because each field has different goals, across populations. Such a convenient scenario, we will terms, assumptions, methods, and journals, but also argue, could arise from ancestral neutrality or balancing because each field has various outdated misunderstand- selection, but is much less likely to arise from a ings of one another. For example, we will argue that mutation-selection balance. Evolutionary genetics could Darwinian psychiatry often relies too heavily on balancing help guide more fruitful gene hunting based on more selection, whereas psychiatric genetics often assumes realistic assumptions. fitness neutrality or ignores evolutionary forces altogether. Evolutionary geneticists try to understand the origins Although balancing selection and neutral evolution were and implications of natural genetic variation across traits historically seen as primary causes of genetic variation, and species. The beautiful empirical and theoretical work in evolutionary genetics is under-funded and too MATTHEW C. KELLER is a postdoctoral fellow at the often thought irrelevant to human welfare. Greater famili- Virginia Institute for Psychiatric and Behavioral arity with evolutionary genetics might help funding Genetics. He received a B.A. from the University of agencies appreciate the potential relevance of this work Texas, Austin in 1995 and a Ph.D. from the University to understanding some of the leading causes of human of Michigan, Ann Arbor in 2004. He has done postdoc- suffering, and may introduce evolutionary geneticists to toral work in genetic epidemiology at the Queensland rich genetic data sets on complex human traits
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