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HUMAN DEVELOPMENT: Biological and Genetic Processes 23 Dec 2004 19:46 AR AR231-PS56-10.tex AR231-PS56-10.sgm LaTeX2e(2002/01/18) P1: IKH 10.1146/annurev.psych.56.091103.070208 Annu. Rev. Psychol. 2005. 56:263–86 doi: 10.1146/annurev.psych.56.091103.070208 Copyright c 2005 by Annual Reviews. All rights reserved First published online as a Review in Advance on July 21, 2004 HUMAN DEVELOPMENT: Biological and Genetic Processes Irving I. Gottesman Department of Psychiatry and Department of Psychology, University of Minnesota, Minneapolis, Minnesota 55454; email: [email protected] Daniel R. Hanson Departments of Psychiatry and Psychology, University of Minnesota, Minneapolis, and Veterans Administration Hospital, Minneapolis, Minnesota 55417; email: [email protected] KeyWords adaptive systems, endophenotypes, CNS plasticity, schizophrenia, autism ■ Abstract Adaptation is a central organizing principle throughout biology, whether we are studying species, populations, or individuals. Adaptation in biological systems occurs in response to molar and molecular environments. Thus, we would predict that genetic systems and nervous systems would be dynamic (cybernetic) in contrast to pre- vious conceptualizations with genes and brains fixed in form and function. Questions of nature versus nurture are meaningless, and we must turn to epigenetics—the way in which biology and experience work together to enhance adaptation throughout thick and thin. Defining endophenotypes—road markers that bring us closer to the biolog- ical origins of the developmental journey—facilitates our understanding of adaptive or maladaptive processes. For human behavioral disorders such as schizophrenia and autism, the inherent plasticity of the nervous system requires a systems approach to incorporate all of the myriad epigenetic factors that can influence such outcomes. by OCCIDENTAL COLLEGE LIBRARY on 07/20/05. For personal use only. CONTENTS Annu. Rev. Psychol. 2005.56:263-286. Downloaded from arjournals.annualreviews.org INTRODUCTION .....................................................264 COMPLEX ADAPTIVE SYSTEMS IN HUMAN DEVELOPMENT ............265 The Meaning of “Gene-Environment Interaction” ..........................265 Epigenesis .........................................................266 Endophenotypes .....................................................268 Generation and Degeneration as a Continuum of Development ................270 BUILDING THE BRAIN FROM THE GENES UP ...........................271 Cellular Differentiation and Migration ...................................271 Angiogenesis .......................................................271 PLASTICITY ........................................................272 EXAMPLE: AUTISM ..................................................274 Epidemiology .......................................................274 0066-4308/05/0203-0263$14.00 263 23 Dec 2004 19:46 AR AR231-PS56-10.tex AR231-PS56-10.sgm LaTeX2e(2002/01/18) P1: IKH 264 GOTTESMAN HANSON Twin Data Paradoxes .................................................275 Phenotypes and Endophenotypes .......................................276 EXAMPLE: OFFSPRING OF SCHIZOPHRENIC PARENTS, CHILDHOOD ONSET CASES, AND COTWINS AS “MEDIA” FOR GROWING ENDOPHENOTYPES .......................................276 Systems Biology ....................................................276 Prospective High-Risk Studies .........................................277 Candidate Genes ....................................................278 Clues from Childhood Schizophrenia ....................................279 CONCLUSIONS AND A GLIMPSE AT THE FUTURE ......................279 CONFLICT OF INTEREST STATEMENT .................................280 INTRODUCTION Newton’s laws of physics and Einstein’s theories of relativity anchor the physical sciences. Biological sciences have a parallel organizing principle in the concept of adaptation (Holland 1975). Adaptation can be viewed from many perspectives, including adaptation of species, of populations, or of individuals. The time scale for evolutionary adaptation of species occurs over a very long period, measured in multiple generations. During this process, genotypes (DNA) are altered through mutation followed by natural selection to reconfigure the architectures of species. Populations adapt on an intermediate time scale that is often within one, or a few, life spans. Genetic diversity reflected in population individual differences allows for deployment of different partially heritable skill sets for different challenges. Forexample, human populations have both created and then adapted to the changes from a largely agrarian existence to a complex industrial world within one or two life spans. Individuals adapt over short time frames measured in fractions of a life span. This ability to adapt quickly is an evolutionarily derived trait. We humans, with opposable thumbs, hands freed by upright locomotion, expanded forebrains, and skills with symbolic language, are the most adaptable of all creatures. This chapter is about adaptation and how, in large part, our genetic and biological systems foster adaptation in health and detract from it in illness. by OCCIDENTAL COLLEGE LIBRARY on 07/20/05. For personal use only. By understanding the ramifications of the concept of adaptation in biological systems, most of the details of biological development and behavioral function Annu. Rev. Psychol. 2005.56:263-286. Downloaded from arjournals.annualreviews.org can be derived (Turkheimer 1998, 2004). In so doing, we quickly confront two old dogmas and hope to teach them new tricks. First, if we accept the idea that our genomes have been “designed” by evolution to maximize adaptability, we could not conclude that genetically mediated traits are fixed and immutable. On the contrary, if our genomes are tuned to maximize adaptability, we would expect genetic factors to play an important role in change even within the individual and over short time frames. The idea that genetic factors influencing behavior are fixed stems mostly from the study of human genetic diseases such as the inborn er- rors of metabolism and chromosomal anomalies. However, these are examples of broken genes, which cannot be generalized to genes functioning via “rheostatic” control. For example, phenylketonuria (PKU), a recessive disorder producing one kind of mental retardation, is due to a dysfunctional genotype for phenylalanine 23 Dec 2004 19:46 AR AR231-PS56-10.tex AR231-PS56-10.sgm LaTeX2e(2002/01/18) P1: IKH HUMAN DEVELOPMENT 265 hydroxylase. In the absence of normal function, people cannot metabolize ubiqui- tous dietary phenylalanine, leading to high concentrations that damage the brain. However, the normal or even half-normal genotype allows the individual to adapt to widely varying amounts of phenylalanine, thus preventing toxic levels even with massive ingestion. The expression of any one gene is embedded within a biological system influenced by a multitude of other genetic and environmental influences; concepts of gene regulation (expression) and epigenesis are now es- sential for understanding development (Carey 2003, Petronis 2004). The classic Mendelian disorders involve genes that are so broken as to overshadow ancillary modifiers. Such dramatic errors of nature divert us from appreciating the subtle, complex, and dynamic nature of biological systems (Dipple & McCabe 2000) that allows them to be adaptive and self-regulating. Second, it has been a long-held belief that the central nervous system is hard- wired and cannot be changed easily by the time we reach adulthood. From the perspective of adaptability, this would make no sense because we continue to learn, change, and adapt throughout the life span. The brain does change with experience and the underlying physiology is guided by genetic factors (Grossman et al. 2003, Insel & Fernald 2004, Kennedy et al. 2003, Weaver et al. 2002). Just as observations of broken genes lead to the erroneous conclusion that genetic effects are unmodifiable, the observations that broken brains (e.g., stroke, trauma) do not heal has led to the belief that the central nervous system (CNS) is a fixed structure. However, in the intact brain, synaptic connections and neuronal circuits are shaped continuously to enhance adaptation. Everything that is genetic is biological, but not all things biological are genetic. Having stated that our genomes and CNS are designed to promote adaptation, we must then consider to what are the adaptations responding. The obvious answer is the environment. However, a global concept such as environment is not helpful. In the PKU example, environmental factors could mean the difference between normal IQ and mental retardation. But, by “environment,” we are not referring to air quality, climate, economic class, amount of parental affection, or hours spent watching Sesame Street. All of these factors may have an impact on a child with PKU, but the trait-relevant environment is the amount of phenylalanine in the diet by OCCIDENTAL COLLEGE LIBRARY on 07/20/05. For personal use only. (Meehl 1977). Thus, the outcomes for a person with the PKU mutation (genotype) Annu. Rev. Psychol. 2005.56:263-286. Downloaded from arjournals.annualreviews.org are determined to a large degree by diet (trait-relevant environment), mediated through the biology of phenylalanine blood levels (endophenotype) that affect the eventual IQ (phenotype). COMPLEX ADAPTIVE SYSTEMS IN HUMAN DEVELOPMENT The Meaning of “Gene-Environment Interaction” The phrase “gene-environment interaction” is used in a variety
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