GENETIC AND ENVIRONMENTAL INFLUENCES ON HUMAN BEHAVIORAL

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Annu. Rev. Neurosci. 1998. 21:124
Copyright c 1998 by Annual Reviews Inc. All rights reserved




GENETIC AND ENVIRONMENTAL
INFLUENCES ON HUMAN
BEHAVIORAL DIFFERENCES
Matt McGue and Thomas J. Bouchard, Jr
Department of Psychology and Institute of Human Genetics, 75 East River Road,
University of Minnesota, Minneapolis, Minnesota 55455;
e-mail: Mmcgue@tfs.psych.umn.edu

KEY WORDS:         heritability, gene-environment interaction and correlation, nonshared environ-
                   ment, psychiatric genetics


                                             ABSTRACT
    Human behavioral genetic research aimed at characterizing the existence and
    nature of genetic and environmental influences on individual differences in cog-
    nitive ability, personality and interests, and psychopathology is reviewed. Twin
    and adoption studies indicate that most behavioral characteristics are heritable.
    Nonetheless, efforts to identify the genes influencing behavior have produced
    a limited number of confirmed linkages or associations. Behavioral genetic re-
    search also documents the importance of environmental factors, but contrary to
    the expectations of many behavioral scientists, the relevant environmental factors
    appear to be those that are not shared by reared together relatives. The observation
    of genotype-environment correlational processes and the hypothesized existence
    of genotype-environment interaction effects serve to distinguish behavioral traits
    from the medical and physiological phenotypes studied by human geneticists. Be-
    havioral genetic research supports the heritability, not the genetic determination,
    of behavior.



INTRODUCTION
One of the longest, and at times most contentious, debates in Western intellectual
history concerns the relative influence of genetic and environmental factors
on human behavioral differences, the so-called nature-nurture debate (Degler
1991). Remarkably, the past generation of behavioral genetic research has led

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many to conclude that it may now be time to retire this debate in favor of a
perspective that more strongly emphasizes the joint influence of genes and the
environment. Nonetheless, the controversy surrounding the recent publication
of The Bell Curve (Herrnstein & Murray 1994) shows that the proposition that
genetic factors influence fundamental aspects of our human nature continues
to inflame passions.
   Human behavioral genetics seeks to identify and characterize both the genetic
and the environmental sources of individual differences (phenotypic variance)
in human behavior. As this topic has not been previously reviewed in this se-
ries, we have taken a broader perspective than might be customary, electing to
consider the past 25 years of behavioral genetic research, albeit with a decided
emphasis on research published in the past 5 years. The reader may also want to
consult the recent general review of this area by Rose (1995), as well as specific
reviews of behavioral genetic research on crime and violence (Bock & Goode
1996), behavioral medicine (Turner et al 1995), psychiatric genetics (Blum &
Noble 1997, McGuffin et al 1994), intelligence (Sternberg & Grigorenko 1997),
and personality (Loehlin 1992). Our review is organized around three broad as-
pects of behavioral genetic research--(a) the nature of genetic influence, (b)
the nature of environmental influence, and (c) models for the joint influence
of genes and the environment--and is focused on three broad domains of psy-
chological functioning--(a) cognitive ability, (b) personality and interests, and
(c) psychopathology. We do not review research on mental retardation and
neurogenetic disorders such as Alzheimer's disease and epilepsy.

METHODOLOGICAL CONSIDERATIONS
In standard biometrical formulations, the phenotypic variance is decomposed
into genetic and environmental components. The genetic component is further
decomposed into additive and nonadditive components, the latter reflecting
interactive effects within (dominance) and among (epistasis) loci. The envi-
ronmental component is decomposed into a shared environmental component,
representing the effects of characteristics such as family income, parental strate-
gies on child-rearing, and level of intellectual stimulation within the home that
are shared by reared together relatives and are thus a potential source of their
behavioral similarity; and a nonshared environmental component, representing
the effects of characteristics such as accidents, peer affiliations, and differential
parental treatment that are not shared by reared together relatives and are thus a
source of their behavioral dissimilarity. Three general strategies have been used
to resolve the separate influence of genetic and shared environmental factors
on the familial resemblance that characterizes the vast majority of behavioral
traits: twin studies, adoption studies, and gene identification methods.
                                       HUMAN BEHAVIORAL GENETICS                 3

   The classical twin study involves the comparison of monozygotic and dizy-
gotic twins reared together (MZTs and DZTs). If genetic factors influence the
trait in question, MZTs, who share 100% of their genetic material, should be
more similar than DZTs, who, like ordinary siblings, share on average only 50%
of their genetic material. In a classical twin study, the proportion of phenotypic
variance associated with additive genetic factors (i.e. the narrow heritability)
is estimated by doubling the difference in correlation between the MZTs and
DZTs, the contribution of shared environmental factors is estimated by subtract-
ing the heritability estimate from the MZT correlation, and the contribution of
nonshared environmental factors and measurement error is estimated by sub-
tracting the MZT correlation from 1.0. These estimates, like any statistics, can
change over time and vary across culture; nonetheless, they have proven to
be useful indices for characterizing the sources of individual differences in
psychological traits (e.g. Neisser et al 1996). Powerful methods for analyzing
twin data and estimating environmental and genetic components of variance
are now available (Neale & Cardon 1992). Owing to the availability of several
large population-based twin registries in Western Europe, the United States,
and Australia, the classical twin study is a popular behavioral genetic design.
The assumptions that underlie the classical twin study have drawn substantial
empirical attention that has generally supported the basic validity of this method
(Plomin et al 1990b).
   An adoption study involves determining the degree to which adopted individ-
uals resemble both their biological relatives, an indication of genetic influences,
as well as their adoptive relatives, an indication of shared environmental influ-
ences. Although there are some notable US adoption studies, most adoption
research has been undertaken in Scandinavian countries, where the availability
of national registries has allowed researchers to ascertain relatively large and
representative cohorts of adopted individuals as well as both their adoptive and
biological relatives. As is the case with twin studies, the assumptions that under-
lie the adoption study have drawn much empirical investigation, most of which
is generally supportive of the utility of this method (Cadoret 1986, Plomin
et al 1990b). Nonetheless, one limitation bears noting. As adoptive homes are
likely to underrepresent those who are living at the extremes of poverty and de-
privation, the importance of environmental influences may be underestimated
in adoption studies. Environmental inferences may apply only to the broadly
constituted middle class.
   Increasingly, behavioral geneticists are using molecular genetic techniques
in an attempt to identify the genes implied to exist by twin and adoption stud-
ies, an effort that has been greatly aided by the development of a comprehen-
sive human linkage map. In contrast to classical human genetic phenotypes
such as Huntington's disease, phenylketonuria, or cystic fibrosis--which are
4     McGUE & BOUCHARD

fully penetrant, homogeneous, single-gene disorders--behavioral phenotypes
are influenced by both environmental and genetic factors and are most likely
heterogeneous. Moreover, for psychiatric disorders, risk to MZT cotwins typi-
cally exceeds by more than a factor of two the corresponding risk to first-degree
relatives, implying that the underlying genetic diathesis is the result of several
(oligogenic) or many (polygenic) genes (Risch 1990), adding further complex-
ity to attempts at gene identification. Success in identifying the multiple genes
influencing risk for disorders like Type I diabetes (Todd 1995) may provide a
useful model for those investigating complex psychiatric phenotypes.
   Most systematic efforts at gene identification for behavioral traits have taken
one of two approaches. In a linkage study, within-family associations between
disease status and genetic marker status serve to identify chromosomal regions
likely to contain a disease susceptibility locus. A genome-wide search with
approximately 400 to 600 markers distributed throughout the human genome
provides an average marker density of less than 10 cM, and a reasonable likeli-
hood of finding linkage if the risk-increasing allele is common (frequency > .01)
and has a large effect on disease risk (risk ratio  4.0) (Risch & Merikangas
1996). In an association study, a population association between disease status
and genetic marker status indicates that the marker either directly influences
disease risk (i.e. is a candidate gene) or is physically proximal and in linkage
disequilibrium with a disease susceptibility locus. Currently, there is debate as
to which approach is preferable with complex behavioral phenotypes. On the
one hand, there is concern that linkage studies may not be sufficiently powerful
to identify the genes of modest effect that may constitute the genetic basis for
many behavioral phenotypes (Risch & Merikangas 1996). On the other hand,
association studies are especially susceptible to false positive findings, owing
to imperfect matching of cases with controls, and there are at present a limited
number of candidate genes for behavioral characteristics, given the relatively
small proportion of genes expressed in human brain that have thus far been
identified (Gelernter 1997).


THE NATURE OF GENETIC INFLUENCE
Twin and Adoption Studies Document the Heritable Nature
of Most Psychological Traits
COGNITIVE ABILITIES General cognitive ability, or IQ, has been more exten-
sively studied from a behavioral genetic perspective than any other psycho-
logical trait. Model fitting analyses of the combined IQ kinship correlations
(Bouchard & McGue 1981) result in heritability estimates of approximately
.50, shared environmental influences of .20 and .30, and the balance of variance
                                        HUMAN BEHAVIORAL GENETICS                  5

being accounted for by nonshared environmental effects and measurement
error (Chipuer et al 1990, Loehlin 1989). These analyses, however, do not take
age into account, and recent evidence suggests that the heritability of general
cognitive ability varies with age. In a landmark longitudinal twin study, Wilson
(1983) observed little difference in MZT and DZT correlation for mental ability
in the first 36 months of life (correlations of about .68) but did observe diver-
gence in correlation thereafter until age 15 years, when the MZT correlation for
IQ equaled .86 and the DZT correlation equaled .54. IQ studies of adult twins,
although limited in number and size, extend this pattern by finding an average
MZT correlation of .83 and an average DZT correlation of .39 (McGue et al
1993). Finkel et al (1995) analyzed general cognitive ability data from adult
MZTs and DZTs participating in the Minnesota Twin Study of Adult Develop-
ment and Aging (MTSADA) and the Swedish Adoption/Twin Study of Aging
(SATSA). The heritability of IQ did not vary significantly across the younger
(age 27 to 50 years), middle-aged (50 to 65), and older (65 to 88) MTSADA
samples (common estimate was .81) but did decline significantly in the older
SATSA sample (estimate of .58 in this group). The heritability of IQ thus ap-
pears to be substantial throughout much of adulthood, but declines perhaps very
late in life.
   The five studies of monozygotic twins reared apart (MZAs), almost all
of whom were assessed as adults (Bouchard et al 1990a, Juel-Nielsen 1965,
Newman et al 1937, Pedersen et al 1992, Shields 1962), have reported IQ
correlations ranging from .64 to .78, with a weighted average of .75 (a direct
estimate of the total contribution of genetic factors or the broad heritability). The
substantial MZA IQ correlation cannot be accounted for by contact between
the twins, either prior to or after their separation, or by the placement of the
twins in homes similar in their trait-relevant environments (Bouchard 1997a,
Pedersen et al 1992). It is moreover inconceivable that MZA twins share rearing
environmental factors to a greater degree than two nonbiologically related but
reared together siblings (adoptive siblings). The IQ correlations for the latter
(a direct estimate of the shared environmental contribution to variance) aver-
age only .04 in the four studies of adult samples (Loehlin et al 1997, Scarr &
Weinberg 1978, Scarr et al 1993, Teasdale & Owen 1984).
   The substantial estimate of IQ heritability from twin studies is consistent
with adoption research. Teasdale & Owen (1984) systematically identified four
types of siblings from young males who had completed an IQ assessment as
conscripts in the Danish military. All males in Denmark (fit for service or not)
complete this test, so this is the most representative sample ever used for as-
sessing genetic influences on IQ. They reported correlations of .47 for full
siblings reared apart as compared with .52 for full siblings reared together,
.22 for half-siblings reared apart, and .02 for adoptive siblings reared together.
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