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Intelligence 33 (2005) 643 – 661

Environmental moderators of genetic influence on verbal


and nonverbal abilities in early childhood
Kathryn Asburya,*, Theodore D. Wachsb, Robert Plomina
a
Box P080, Social, Genetic, and Developmental Psychiatry Centre, Institute of Psychiatry,
King’s College London, De Crespigny Park, London, SE5 8AF, U.K.
b
Department of Psychological Sciences, Purdue University, W. Lafayette, IN 47907-1364, USA
Received 3 January 2004; received in revised form 3 February 2005; accepted 2 March 2005
Available online 13 October 2005

Abstract

The study of genotype–environment interaction (G  E) has been dominated by two competing hypotheses, one
that heritability is greater in high-risk environments (diathesis-stress) and the other that heritability is greater in
permissive environments. The current study examined relationships between verbal and nonverbal abilities and 10
measured environments, using a sample of 4-year-old same-sex twins (N = 4446 children). Significant G  E
emerged for verbal ability with three of the environmental indices, all in the direction of the diathesis-stress model
(family chaos, instructive parent–child communication and informal parent–child communication). No significant
G  E emerged for nonverbal ability. We conclude that G  E exists for verbal ability in early childhood and tends
to be in the direction of greater heritability in high-risk environments.
D 2005 Published by Elsevier Inc.

Genotype–environment interactions (G  E) occur when genes prove sensitive to environmental


effects or, in other words, when an environment moderates a genetic effect (Kendler & Eaves, 1986;
Plomin, DeFries, & Loehlin, 1977; Rutter et al., 1997). It is an alluring concept for researchers
because pinpointing moderating relationships between measured environments and genes is a potent
way of opening up new possibilities for the identification or design of environmental interventions
which could enhance lives. The best known example of an environmental intervention which

T Corresponding author. Tel.: +44 20 7848 5401; fax: +44 20 7848 0092.
E-mail address: spjgkaa@iop.kcl.ac.uk (K. Asbury).

0160-2896/$ - see front matter D 2005 Published by Elsevier Inc.


doi:10.1016/j.intell.2005.03.008
644 K. Asbury et al. / Intelligence 33 (2005) 643–661

capitalizes on a G  E is the low phenylalanine diet recommended to PKU sufferers (Guthrie, 1996).
Other such interventions, not just for single-gene disorders like PKU, are the ultimate aim of G  E
research.
The study of G  E has so far been dominated by two competing hypotheses. The first, that
heritability is greater in high risk environments, is seen most often in the psychiatric literature
(diathesis-stress model: Gottesman, 1991; Paris, 1999). Underlying this hypothesis is the assumption
that individuals at genetic risk for a disorder are more sensitive to environmental risk factors than
those not at genetic risk (Plomin & Rutter, 1998). As a result, the genetic predisposition for a
disorder is more likely to be expressed when environmental risk conditions are high. The second
dpermissive environmentsT hypothesis, seen most often in the animal literature, shares much in
common with Bronfenbrenner and Ceci’s (1994) bioecological framework and leads to more
complex predictions. A major aspect of the bioecological framework involves the concept of
bproximal processesQ, which are defined as bprogressively more complex reciprocal interactions
between an active evolving biopsychological human organism and the persons, objects and symbols
in its immediate environment. . .Proximal processes raise levels of effective developmental
functioning and thereby increase the proportion of individual differences attributable to actualized
genetic potential.Q (Bronfenbrenner & Ceci, 1994, p 572). Within the bioecological framework, when
proximal processes are high then heritability will also be high (Bronfenbrenner & Ceci, 1994,
hypothesis 1). In addition, given that proximal processes (e.g., parent–child communication) are
nested in a larger environmental system, then heritability will be lower when components of the
environment (e.g. high levels of disorganization in the home) interfere with them: bThe power of
proximal processes to actualize genetic potentials for developmental competence. . .will be greater in
advantaged and stable environments than in those that are disadvantaged and disorganizedQ
(Bronfenbrenner & Ceci, 1994 hypothesis 2–1, p 578). These diathesis-stress and bioecological
hypotheses lead to different predictions about the conditions in which G  E interactions should
appear.
Exploration of G  E for cognitive traits has been at its most successful in animal research where both
genotypes and environments can be manipulated, yet even in these conditions positive results have been
somewhat rare (e.g., De Kloet, Grootendorst, Karssen, & Oitzl, 2002). Almost half a century ago, in a
classic G  E study, maze-bright and maze-dull selected lines of rats were found to respond differently to
benrichedQ and brestrictedQ rearing environments (Cooper & Zubeck, 1958). The enriched condition—
larger, more stimulating cages—had no effect on the maze-bright selected line, but improved the maze-
running performance of maze-dull rats significantly, in fact almost to the level of the genetically bright
animals. The restricted environment was detrimental to the performance of maze-bright rats but had little
effect on the maze-dull rats. In both instances, and for better or worse, environmental influence altered
genetic effects.
This finding corresponds to neither of the two G  E hypotheses in that heritability, as estimated by
the difference between the two selected lines of rats, is not higher in the high risk environment (diathesis-
stress hypothesis) or in the enriched environment (bioecological hypothesis). Instead, heritability is
highest in the dnormalT laboratory condition.
Attempts to find G  E results in human research have shown some successes in relation to
psychopathology (e.g., Cadoret, Cain, & Crowe, 1983; Heath, Eaves, & Martin, 1998; Kendler,
Kessler, Walters, MacLean, & Neale, 1995; Riggins-Caspers, Cadoret, Knutson, & Langbehn, 2003;
Silberg, Rutter, Neale, & Eaves, 2001), including striking successes in recent studies assessing
K. Asbury et al. / Intelligence 33 (2005) 643–661 645

interactions with specific genes (Caspi et al., 2002; Caspi et al., 2003). In addition, replicated
organism  environment interactions have been reported involving individual differences in
temperament which has a known genetic basis (Bates, 2001). However, in the domain of cognitive
development, reported examples of G  E have yet to be replicated convincingly (Plomin, DeFries,
McLearn, & McGuffin, 2001). For example, in one study of 176 monozygotic (MZ) twin pairs, 347
dizygotic (DZ) twin pairs, 795 full sibling pairs, 269 half sibling pairs, 118 cousin pairs and 204
unrelated sibling pairs (mean age = 16 years), the heritability of verbal IQ was found to be significantly
greater in families with more highly educated parents (74%) than in families with less well educated
parents (26%) (Rowe, Jacobsen, & Van den Oord, 1999). Although this G  E result was not found in
an earlier study of cognitive abilities in 9-year-olds conducted by the same authors (Van den Oord &
Rowe, 1998), a recent study of 319 7-year-old twin pairs also reported lower heritability for IQ in
poorer families (Turkheimer, Haley, Waldron, D’Onofrio & Gottesman, 2003). However, two adoption
studies showed no G  E for IQ when they used parental education as an index of the environment
(Duyme, Dumaret, & Tomkiewicz, 1999; Plomin et al., 1977). Nonetheless, the two reports of lower
heritability for IQ in lower socio-economic status families warrant additional study.
A second exception to the generally negative G  E results in human cognitive research is a
study that found significantly lower heritability for infant verbal and nonverbal cognitive
development in very premature twins, as compared to twins of more normal gestational age
(Koeppen-Schomerus, Eley, Wolke, Gringras, & Plomin, 2000). To the extent that biomedical risk
conditions act to reduce the impact of proximal processes these results could be considered as
evidence in support of the predictions derived from Bronfenbrenner and Ceci (1994). This analysis
used data from the Twins Early Development Study (TEDS: Trouton, Spinath, & Plomin, 2002), as
does the current research.
Although other reports of G  E in the cognitive domain could be used to support the predictions
derived from the bioecological hypothesis, these reports which involved twin studies have major
methodological shortcomings. For example, one twin study investigating G  E between IQ and SES
compared same-sex and opposite-sex twins but did not measure zygosity, relying instead on estimated
proportions of MZ and DZ pairs (Scarr-Salapatek, 1971). Another twin study (Fischbein, 1980) had
much too small a sample size to draw reliable conclusions about G  E involving SES and IQ (14 MZ
and 24 DZ pairs in the low social class group).
Almost all of the G  E research on cognitive ability carried out so far invokes the distal index of
SES as a potential environmental moderator of genetic effects on cognition. Reviews of
methodological issues involved in the detection of G  E have emphasized the importance of
adequate statistical power. For example, it is well known that demands for power are daunting when
comparing heritabilities (Wahlsten, 1991). Statistical power can be enhanced by increasing sample
size and through use of more precise assessment of predictors (Wachs & Plomin, 1991). Application
of the latter criterion would suggest that more proximal measures of the family environment may be
more sensitive to G  E effects than distal SES measures. The main aim of the current study was
therefore to assess whether the heritability of cognitive abilities differs as a function of the
environment in early childhood, by systematically examining a wide range of both distal and
proximal environmental factors. Statistical power to detect G  E is maximized by use of a large
sample and by also including more precise proximal assessments. A secondary aim was to establish
whether such G  E, if found, would be better described by the diathesis-stress model or the
bioecological framework.
646 K. Asbury et al. / Intelligence 33 (2005) 643–661

1. Method

1.1. Participants

A total of 4446 twin children were assessed close to their fourth birthdays. This sample of same-sex
twin pairs was drawn from the Twins Early Development Study (TEDS). TEDS is an ongoing
longitudinal study in which all twins born in England and Wales between 1994 and 1996 were invited to
take part (Trouton et al., 2002). Twin pairs were excluded from the current analyses if at least one child
in the pair had a specific medical syndrome such as Downs or was an extreme outlier for birthweight,
time spent in hospital (including special care at birth) or gestational age. The sample is reasonably
representative of UK families with young children (Trouton et al., 2002). For example, UK census data
suggests that 92% of UK mothers are white, and 92% of mothers in the total TEDS sample are white. In
addition, 32% of mothers in the UK population have A-level qualifications (advanced-level
examinations, usually taken at age 18), where 34% of TEDS mothers have A-levels. A parent-rated
instrument was used to assign zygosity and has an accuracy of 95% as evaluated against DNA markers
(Price et al., 2000).

1.2. Measures

We investigated two cognitive variables (verbal ability and nonverbal ability) and ten environmental
variables. The environmental variables were chosen to test the competing hypotheses defined above. In
order to test the diathesis-stress hypothesis, both distal (e.g., SES, maternal and child medical problems)
and proximal (e.g., harsh parental discipline, negative parental feelings) risk factors were included. To
test the bioecological hypothesis, measures of proximal processes (e.g., parent–child communication,
educational toys in the home) were used, along with environmental factors that might interfere with the
operation of those proximal processes (e.g., family chaos, maternal depression). Because of our large
sample size, direct observational assessment of proximal processes and certain environmental risk
factors was impractical. Therefore we chose to utilize previously validated measures assessing parental
perceptions of the family environment. Parental perceptions of family characteristics have been
repeatedly used in research on environmental influences and have been shown to predict a variety of
offspring developmental outcomes (Bradley, 1999).
The cognitive measures were coded so that a higher score represented higher ability. Environmental
measures were coded in the directions indicated by their labels. The cognitive and environmental
measures are described briefly below. Further information about construction and factor structure are
available for both cognitive measures (Spinath, Price, Dale, & Plomin, 2004; Spinath, Ronald,
Harlaar, Price, & Plomin, 2003) and environmental measures (Pike, Iervolino, Eley, Price, & Plomin,
in press).

1.3. Cognitive variables

1.3.1. Verbal ability


Verbal ability was assessed at age 4 using the Expressive Vocabulary and Grammatical Complexity
subscales of the MacArthur Communicative Development Inventory (MCDI: Fenson et al., 1994). These
measures were parent-administered. The MCDI is widely used and demonstrates excellent internal
K. Asbury et al. / Intelligence 33 (2005) 643–661 647

consistency, test–retest reliability, and concurrent validity with tester-administered measures (Fenson et
al., 1994). Expressive Vocabulary is assessed with a 100-item checklist on which parents were asked to
report on their children’s production of root words. A composite score was calculated by summing the
number of words checked. The Grammatical Complexity subscale examines whether and how children
combine words. A total verbal ability score was calculated by summing standardized scores on these two
measures (Spinath et al., 2004).

1.3.2. Nonverbal ability


Nonverbal ability was measured using the Parent Report of Children’s Abilities (PARCA: Oliver et
al., 2002; Saudino et al., 1998). The PARCA is a two-part measure in which parents complete a
questionnaire about their children’s cognitive abilities and administer an hour-long battery of cognitive
tests. The battery is based on age-appropriate developments of a match-to-sample task, a design-drawing
task, and an Odd-Man-Out task. Some of these items were adapted from standard tests (e.g. McCarthy
Scales of Children’s Abilities, McCarthy, 1972; Bayley Scales of Infant Development (BSID), Bayley,
1993) while other items were developed specifically for use in TEDS. A total nonverbal ability score
was calculated by standardizing and summing the three test scores. Validation studies of the PARCA at
ages 2 and 3 have demonstrated good internal consistencies for the parent report section (.74 and .67,
respectively). The reported results are consistent with a meta-analysis supporting the validity of parent-
based measures (Dinnebeil & Rule, 1994).
It should be noted that verbal and nonverbal scores show a moderate correlation (r = .46) indicating
that we might expect moderate similarity in G  E results for verbal and nonverbal abilities. This
correlation is comparable to that found for tester-administered standardized measures. For example, the
correlation is .53 between verbal and nonverbal (perceptual performance) ability scales at 4 years in the
McCarthy Scales of Children’s Abilities (McCarthy, 1972).

1.4. Environmental variables

Most environmental variables were assessed by questionnaire when the twins were 4 years old,
although three measured environments (SES, maternal medical problems in pregnancy and twin medical
risk) were assessed at the point of first contact, when the twins were on average 18 months old. Two of
these measures, SES and family chaos, have recently been reported as mediators of shared
environmental influence on verbal and non-verbal abilities (Petrill, Pike, Price, & Plomin, 2004). They
have not, however, been investigated as potential moderators.

1.4.1. Socio-economic status (SES)


An index of SES was derived from a factor analysis of five variables: mothers’ occupational status,
fathers’ occupational status, mothers’ highest educational qualification, fathers’ highest educational
qualification and mothers’ age at the birth of her eldest child. A single-factor solution yielded an eigenvalue
of 2.51 and accounted for 50% of the variance. A single SES composite was created by standardizing these
five variables and summing them using unit weights (Pike et al., in press).

1.4.2. Family chaos


The degree of chaos in the home was assessed using a short version of the Confusion, Hubbub, and
Order Scale (CHAOS) (Matheny, Wachs, Ludwig, & Phillips, 1995). The scale consists of 6 items
648 K. Asbury et al. / Intelligence 33 (2005) 643–661

rated on a five-point scale (where 1 = definitely untrue and 5 = definitely true) and includes items such
as bYou can’t hear yourself think in our homeQ and bWe are usually able to stay on top of thingsQ. A
total chaos score was generated by summing the items (alpha = .63). Parent CHAOS scores have been
validated through comparison with direct observations in the home environment (Matheny et al.,
1995).

1.4.3. Maternal depression


Maternal depression was assessed using the Edinburgh Postnatal Depression Scale (EPDS), a brief
measure of depressed mood that was originally used in a large-scale epidemiological study of women’s
psychological health following childbirth (Cox, Holden, & Sagovsky, 1987). The scale consists of 10
items (e.g., bI have felt sad and miserableQ) assessed using a Likert scale ranging from 0 (bnot at allQ) to 3
(byes, most of the timeQ). The scale has been validated against diagnostic criteria in the postpartum
period (Murray & Corothers, 1990) and later (Thorpe, 1993) and demonstrated reasonable internal
reliability in the TEDS study (alpha = .67).

1.4.4. Harsh parental discipline


Parents’ perceptions of the harshness of their discipline strategies were measured using 4
questionnaire items derived from a previously validated semi-structured interview (Deater-Deckard,
Dodge, Bates, & Pettit, 1998). Parents (usually mothers) gave information on their use of harsh
discipline strategies such as hitting and shouting, and more developmentally facilitative strategies such
as being firm and calm and explaining and reasoning with the child. These items were rated on a 6-point
scale from dI rarely or never do thisT, to dI usually do thisT. After answering for the first-born twin,
parents were asked bDo you do this more or less with your second-born twin?Q and their answers were
rated on a 5-point scale from da lot moreT to da lot lessT. Thus scores for second-born twins were derived
from comparisons with their co-twins, rather than from their own raw scores. A feasibility study
conducted when the TEDS booklets were first designed indicated that presenting the items for first- and
second-born twins side by side, as opposed to in separate booklets, did not significantly alter the amount
that parents differentiated between their twins.
First-born twins’ scores were based on the sum of the parental discipline items that had been
standardized to zero mean and unit variance for the whole population. Each second-born twin’s score
was derived from that of the first-born co-twin whose standardized sum was added to the standardized
sum of the differential items in order to indicate whether the second-born twin received more, less or the
same amount of parental discipline. Individual twin scores were then averaged across the pair to create
an index of family-level risk (alpha = .51).

1.4.5. Negative parental feelings


Parental perceptions of the positivity or negativity of their feelings for their children were assessed
using a shortened version of the previously validated Parental Feelings Questionnaire (Deater-Deckard,
2000). The measure has 7 items which were rated on a 5-point scale from ddefinitely trueT to ddefinitely
untrueT for first-born twins and included statements such as bI usually feel close to him/herQ and
bSometimes I feel very impatient with him/herQ. As with parental discipline, parents were then asked bDo
you feel this way more or less with your second-born twin?Q and answers were rated on a 5 point scale
from da lot moreT to da lot lessT. Scores were derived in the same way as for harsh parental discipline
(alpha = .70).
K. Asbury et al. / Intelligence 33 (2005) 643–661 649

1.4.6. Maternal medical problems in pregnancy


A maternal medical problems variable was derived from a factor analysis of data collected at the point
of first contact. These were subjected to a principal component analysis. Based on an inspection of the
scree plot, the cumulative percentage of variance explained (46.7%), and a relatively bcleanQ factor
structure when Varimax rotation with Kaiser normalization was utilized, a four-factor (all eigenvalues
greater than 1.0) solution was deemed most appropriate. The first factor was high blood pressure and
toxemia during pregnancy; the second was birth complications and gestation in weeks (negatively
loaded); the third factor was vaginal bleeding, prescribed bed rest and medicine during pregnancy; and
the fourth was cigarettes smoked and units of alcohol consumed during pregnancy, stress, slow baby
growth and fertility treatment (negatively loaded). In order to create the total maternal medical
composite, all items were first reverse coded where necessary, and standardized. Four scales were then
created summing constituent items using unit weights. Finally, these scale scores were standardized, and
the four scales summed to form the composite.

1.4.7. Twin medical risk


All medical information about the twins was obtained via the first contact booklet. A factor analysis
including birthweight (reverse coded), time spent in special care, medical problems at birth and time in
hospital yielded a single factor solution, accounting for 66% of the variance. The twin medical risk
composite was created by standardizing these four variables and summing them using unit weights.
Separate composites were created for each of the twins in the pair and then averaged to create an index of
family-level risk.

1.4.8. Instructive parent–child communication


Factor analysis of a series of questions answered by parents about how they talk to their twins yielded
2 factors. Instructive parent–child communication was based on 3 items related to correcting
pronunciation, sentence structure and vocabulary. First-born twin scores for each item were summed
and each second-born twin’s score was statistically derived from that of their co-twin. Individual twin
scores were averaged across the pair, as with the parenting variables (alpha = .86).

1.4.9. Informal parent–child communication


This factor was based on 4 items asking about how parents interact with their children in terms of
singing songs, talking about directions when out and about, looking at books and generally chatting.
Second-born twin scores were derived from those of first-borns and then averaged across the pair, as
described above (alpha = .50).

1.4.10. Educational toys


Factor analysis yielded an educational toys factor based on 3 items relating to the number of puzzles,
tapes and books owned by each child. Individual twin scores were averaged across the pair, as with the
other twin specific variables (alpha = .69).
Correlations between these environmental variables are presented in Table 1.
They range from .00 to .45 and are not, in general, highly correlated (mean r = .13). However, as will be
subsequently described in the Results Section, the correlations between assessed distal and proximal aspects
of the environment, between risk and proximal process variables, and between proximal process predictors
are almost all in the direction that would be predicted from previous research and theory (Wachs, 2000).
650
Table 1

K. Asbury et al. / Intelligence 33 (2005) 643–661


Correlations between environmental measures
SES Parental Negative Family Maternal Maternal Twin Instructive Informal Educational
discipline parental chaos depression medical medical parent–child parent–child toys
feelings problems risk communication communication
SES 1 .18** .04**  .27**  .08** .07** .01 .03** .13** .23**
Harsh parental discipline 1 .34** .31** .23** .06* .00 .02  .18** .19**
Parental feelings 1 .32** .34** .07** .06** .01  .15** .14**
Family chaos 1 .41** .09**  .02* .01  .21** .23**
Maternal depression 1 .11** .03* .00  .12** .15**
Maternal medical problems 1 .40** .04** .00 .03**
Twin medical risk 1 .04** .02* .00
Instructive parent–child 1 .10** .06**
communication
Informal parent–child 1 .45**
communication
Educational toys 1
K. Asbury et al. / Intelligence 33 (2005) 643–661 651

1.4.11. Analysis
Based on the diathesis-stress and bioecological hypotheses the following predictions were made:

(1) If the diathesis-stress hypothesis is correct, higher levels of heritability will be seen when
environmental risk is higher. That is, higher levels of heritability should be shown when family
chaos, maternal depression, maternal medical factors in pregnancy, twin medical risk, harsh
parental discipline and negative feelings scores are higher, as well as when SES, instructive parent–
child communication, informal parent–child communication and educational toys in the home
scores are lower.
(2) If the bioecological hypothesis is correct, higher levels of heritability will be shown when proximal
processes are higher. Specifically, we would expect to see higher levels of heritability with higher
levels of instructive parent–child communication, informal parent–child communication and
availability of educational toys, as well as lower levels of harsh parental discipline and negative
parental feelings. We would also predict lower levels of heritability for those environmental context
variables that inhibit proximal processes and, in fact, Table 1 shows that family chaos, SES and
maternal depression were negatively related to indices of proximal processes such as informal
parent–child communication and educational toys in the home.

Several cut-offs were established to compare the group heritability of the cognitive scores of children
experiencing different environmental characteristics. For each measured environment the sample was
divided at the median to compare the more risky 50% (high risk or low proximal processes) against the
less risky 50%. We also compared the top and bottom 33%, 25% and 15%. We did not include more
extreme cut-offs as this would have resulted in samples too small to provide adequate statistical power.
We compared these groups using DF regression analysis (DeFries & Fulker, 1985) to estimate individual
differences heritability for each group on each measure—a least-squares model-fitting approach that
gives the same parameter estimates as does maximum-likelihood model-fitting. We used DF regression
because it is easily extended to consider G  E, as explained later. In the individual differences DF
regression equation the phenotypic score of twin 1 ( P 1) is predicted from the phenotypic score of twin 2
( P 2), the coefficient of genetic relatedness (R which = 1.0 for MZ twins and 0.5 for DZ twins), and the
interaction between them (R  P 2).
P1 ¼ b0 þ b1 P2 þ b2 R þ b3 Rd P2
The b 3 regression coefficient tests the extent to which twin resemblance differs as a function of
zygosity and provides an estimate of heritability essentially by doubling the difference in MZ and DZ
correlations; b 2 tests and controls for mean differences between MZ and DZ twins; b 1 assesses twin
resemblance not explained by heritability; and b 0 is the regression constant. We used the Extended DF
model (LaBuda & DeFries, 1990) to test G  E quantitatively, that is, using the entire distribution of the
measured environment rather than a cut-off for environmental risk, and to assess the significance of
G  E across the distribution. The full extended DF equation is:
P1 ¼ b0 þ b1 P2 þ b2 R þ b3 E þ ðb4 Rd P2 Þ þ ð b5 Rd E Þ þ ð b6 P2 d EÞ þ ð b7 P2 dRd E Þ
which adds a measure of the environment (E) to the above equation. The three-way interaction denoted
by b 7 tests whether heritability (i.e. P 2 d R) differs as a function of the environmental variable (i.e.,
P 2 d R d E). This analysis was used to assess whether group heritability differed significantly as a
652 K. Asbury et al. / Intelligence 33 (2005) 643–661

function of environmental risk considered continuously, and by using the whole sample it provides us
with adequate power to detect significant interactions.

2. Results

Table 2 shows means and standard deviations for MZ and same-sex DZ pairs on both the cognitive
and environmental measures. Although significant mean differences were found between MZ and DZ
twins for nonverbal ability and several of the environmental variables, the effect sizes (d) were .1 or less.
Table 3 shows correlations for each of the environmental measures with verbal and nonverbal ability,
presented separately for MZ and DZ twins.
It can be seen in Table 3 that associations between environments and cognitive outcomes, while mainly
significant, were similarly modest for MZ and DZ twins peaking between r = .25 and r = .32 for informal
parent–child communication and educational toys in the home. Associations with other environmental
variables were smaller and generally, predictably, negative. It should be noted that main effects of
measured environments on verbal and nonverbal abilities are independent of any effects of G  E.
In addition to assessing the association between the environmental variables and verbal and nonverbal
abilities for the entire sample using correlations, we also investigated the association at all cut-offs (15%,
25%, 33% 50%) by testing the mean difference between the low and high groups for each cut-off. These
results indicated that the patterns of association seen in the correlational results in Table 3 are also seen at
all cut-offs. (Results available from first author.)
In order to assess whether group heritability differs as a function of environmental risk, DeFries and
Fulker (DF) regression analyses were conducted for each of the 160 cut-off groups (based on 8 cut-offs
within 10 environmental variables for two cognitive measures).

Table 2
Descriptive statistics for cognitive and environmental measures, separately for MZ and DZ twin pairs
MZ DZ Significance
M SD N M SD N
Cognitive variables
Verbal ability .02 .88 2040 .03 .83 1944 NS
Nonverbal ability .03 .71 2174 .06 .68 2041 **

Environmental variables
SES .05 .97 1826  .05 1.01 1740 **
Harsh parental discipline .09 .88 1916 .10 1.10 1828 **
Negative parental feelings .00 .95 1911 .10 1.04 1828 **
Family chaos .02 .98 1928  .02 .99 1843 NS
Maternal depression .03 .98 1926  .09 .98 1848 NS
Maternal medical problems in pregnancy .07 .95 1862  .13 1.02 1796 **
Twin medical risk .09 1.09 1936  .12 .86 1854 **
Instructive parent–child communication .11 1.00 1914  .06 1.00 1838 **
Informal parent–child communication .00 .96 1911 .03 .98 1830 NS
Educational toys in the home .04 .96 1914 .13 1.00 1826 **
*p b .05; **p b .01. The significance of the mean differences between MZ and DZ twin pairs was assessed using t-tests.
K. Asbury et al. / Intelligence 33 (2005) 643–661 653

Table 3
Correlations between verbal and nonverbal abilities and environmental measures, separately for MZ and DZ twins
Environmental variables Verbal Nonverbal
MZ DZ All MZ DZ All
SES  .14** .22**  .18**  .10**  .16** .13**
Harsh parental discipline  .07** .10**  .09**  .13**  .12** .13**
Negative parental feelings  .07** .06**  .07**  .13**  .13**  .13**
Family chaos  .16** .17**  .17**  .22**  .20**  .21**
Maternal depression  .07** .07**  .07**  .10**  .06** .08**
Maternal medical problems .00 .05*  .03  .05* .00 .03
in pregnancy
Twin medical risk  .03 .01  .01  .04  .03 .04
Instructive parent–child  .07** .04  .06**  .01  .03 .02
communication
Informal parent–child .25** .32** .29** .29** .31** .30**
communication
Educational toys in the home .27** .28** .28** .31** .28** .30**
N (individual children) 1917–2036 1821–1938 3738–3974 2026–2170 1908–2035 3934–4205
*p b .05, **p b .01.

Table 4 summarizes heritability estimates for verbal ability for the 10 environmental variables. In the
full sample, the group heritability of verbal ability was 44%. Comparing group heritability estimates for
the various low and high cut-offs indicated several consistent patterns of results suggestive of
differential heritability across environments. The six characteristics of the home showing consistent
heritability differences across cut-offs were harsh parental discipline, family chaos, maternal
depression, twin medical risk, instructive and informal parent–child communication. The overlapping
confidence intervals for these comparisons indicated that although the trends were noteworthy (which
the extended DF analysis presented later takes into account) none of the individual comparisons were
significantly different, even for the 50% cut-off where the high and low risk samples are the largest.
However, simple binomial probability tests (z = 2.00, p b .05, two-tailed) suggest that although
individual comparisons were not statistically significant, in a number of cases the overall consistency
of the pattern of results was. In Table 4, six variables were found to have 100% directional consistency
(harsh parental discipline, family chaos, maternal depression, instructive and informal parent–child
communication and twin medical risk). Four of these consistent G  E effects (harsh parental discipline,
family chaos, maternal depression and informal parent–child communication in which low
communication is the direction of risk) supported the diathesis-stress hypothesis in that group
heritability was greater with greater environmental risk. The pattern for instructive parent–child
communication was also noteworthy and again supported the diathesis-stress hypothesis if we remain
with the assumption that low communication is the direction of risk. This will be considered in more
detail in the Discussion. The results for twin medical risk show the opposite pattern in that group
heritability was lower with increased risk, especially at the extremes, a result supporting that found by
Koeppen-Schomerus et al. (2000). Educational toys in the home and SES did not yield a systematic
pattern of results. Educational toys in the home showed no substantial heritability differences between
groups at any cut-off. For SES, group heritability was greater for the lowest 15% SES group (81%) as
654
Table 4

K. Asbury et al. / Intelligence 33 (2005) 643–661


DF heritability estimates of verbal ability based on environmental cut-offs (95% confidence intervals are shown in parentheses, which were constrained to lie
between 0 and 1)
Whole sample: h 2 = 44%
Cut-off Low 15% High 15% Low 25% High 25% Low 33% High 33% Low 50% High 50%
SES .81 (.45–1) .49 (.16–.82) .62 (.37–.87) .43 (.32–.54) .58 (.36–.80) .58 (.36–.80) .46 (.29–.63) .57 (.35–.79)
Harsh parental discipline .26 (0–.57) .36 (.03–.69) .20 (0–.42) .45 (.20–.70) .34 (.17–.51) .56 (.28–.84) .39 (0–1) .54 (.26–.80)
Negative parental feelings .44 (0–.88) .44 (0–.88) .38 (.13–.63) .48 (.15–.81) .44 (.22–.66) .41 (0–.85) .58 (.19–.97) .37 (.06–.68)
Family chaos .21 (0–.52) .72 (.25–1) .28 (.03–.53) .56 (.20–.92) .33 (.14–.52) .56 (.25–.87) .29 (.12–.46) .59 (.37–.81)
Maternal depression .31 (0–.67) .59 (.26–.92) .38 (.16–.60) .60 (.18 –1) .32 (.07–.57) .60 (.18–1) .36 (.11–.61) .55 (.27–.83)
Maternal medical factors .43 (.11–.75) .56 (.21–.91) .50 (0–1) .50 (.25–.75) .51 (0–1) .58 (.37–.79) .42 (0–.85) .55 (.18–.92)
Twin medical risk .70 (.39–.1) .11 (0–.53) .57 (0–1) .38 (.10–.66) .56 (.37–.75) .54 (.32–.76) .48 (.01–.95) .42 (.03–.81)
Instructive parent–child .69 (.30 –1) .08 (0–.47) .61 (.28–.94) .14 (0–1) .49 (.32–.66) .24 (0–1) .50 (.33–.67) .42 (.17–.67)
communication
Informal parent–child .83 (.50 –1) .30 (.06–.53) .63 (.38–.88) .22 (0–.47) .68 (.46–.90) .21 (.02–.40) .65 (.48–.82) .28 (.11–.45)
communication
Educational toys .63 (.30–.66) .66 (.30–1) .50 (.25–.75) .52 (.27–.77) .51 (.29–.73) .50 (.28–.72) .48 (.31–.65) .57 (.40–.74)
N (individual children) 448–634 442–744 900–1044 752–1094 1190–1354 1030–1464 1470–2002 1642–2444
Table 5

K. Asbury et al. / Intelligence 33 (2005) 643–661


DF heritability estimates of nonverbal ability based on environmental cut-offs
Whole sample: h 2 = 28%
Cut-off Low 15% High 15% Low 25% High 25% Low 33% High 33% Low 50% High 50%
SES .21 (0–.54) .42 (.06–.78) .32 (.07–.57) .34 (.01–.67) .30 (.05–.55) .32 (.01–.63) .28 (0–1) .30 (0–.74)
Harsh parental discipline .20 (0–.51) .27 (0–.96) .22 (0–.44) .29 (0–.93) .23 (0–.45) .37 (0–1) .26 (0–1) .34 (0–1)
Negative parental feelings .24 (0–.66) .22 (0–.78) .17 (0–.48) .29 (0–.68) .22 (0–.55) .24 (0–.77) .25 (0–.64) .30 (0–1)
Family chaos .24 (0–.55) .34 (0–.78) .23 (0–.51) .35 (.02–.68) .27 (.05–.49) .35 (.04–.66) .26 (.09–.43) .32 (0–.65)
Maternal depression .22 (0–1) .46 (0–1) .28 (0–.86) .39 (0–1) .31 (.06–.56) .39 (0–1) .26 (0–.54) .33 (0–1)
Maternal medical factors .21 (0–.53) .51 (.19–.83) .15 (0–.79) .32 (.08–.55) .18 (0–.68) .37 (.16–.57) .21 (0–1) .35 (.18–.51)
Twin medical risk .37 (0–1) .37 (0–.93) .31 (06–.56) .38 (.13–.63) .27 (0–.74) .38 (0–1) .23 (.01–.45) .33 (.16–.50)
Instructive parent–child .24 (0–.74) .13 (0–.55) .20 (0–.62) .33 (0–1) .19 (0–1) .24 (.02–.46) .20 (0–.87) .37 (0–.95)
communication
Informal parent–child .39 (.08–.70) .40 (0–.93) .36 (.13–.59) .29 (.07–.51) .31 (.09–.53) .30 (.08–.52) .27 (.10–.44) .35 (.16–.54)
communication
Educational toys .20 (0–.53) .26 (0–.57) .17 (0–.42) .37 (.12–.62) .23 (.01–.45) .37 (.15–.59) .25 (.06–.44) .34 (.17–.51)
N (individual children) 474–662 470–784 952–1098 794–1140 1270–1434 1092–1530 1550–2114 1734–2582

655
656 K. Asbury et al. / Intelligence 33 (2005) 643–661

compared to the highest 15% group (49%)—a result in the opposite direction from Rowe et al. (1999)
and Turkheimer et al. (2003). However, although a difference in the same direction was also seen at the
25% cut-off, the other cut-offs yielded no real differences in heritability, suggesting that any effect is
only seen at the extremes.
Table 5 shows similar G  E patterns for nonverbal as verbal ability but to a lesser extent. In the full
sample, the group heritability of nonverbal ability was 28%. Again all confidence intervals overlapped.
Assessing consistency of directionality using the binomial probability test, six variables shown in Table 5
achieved perfect consistency across all comparisons. Four of the six measured environments (harsh
parental discipline, family chaos, maternal depression and maternal medical problems in pregnancy)
showed greater heritability with higher risk, suggesting diathesis-stress. In contrast, the higher levels of
heritability shown for higher levels of educational toys in the home is consistent with predictions from the
bioecological framework. The lower levels of heritability found for lower SES groups, although slight,
would also fit the bioecological framework to the extent that lower SES can interfere with proximal
processes (Table 1). The results for negative parental feelings and twin medical risk were inconsistent,
showing no real difference at the 15% extremes but a very slight trend in the direction of diathesis-stress at
the less extreme cut-offs. Results for instructive and informal parent–child communication were also
inconsistent.
In order to address this issue more formally, we applied the Extended DF model described earlier.
This is a powerful tool for assessing G  E as it makes use of the entire distribution rather than cut-off
based groups (for more details, see LaBuda & DeFries, 1990).
Results for the Extended DF analyses of G  E are shown in Table 6 and confirm several of the
implications drawn from Tables 4 and 5. Three significant interaction effects were found for verbal
ability (family chaos, instructive parent–child communication and informal parent–child communication,
p b .01), and none for nonverbal ability.
The significant positive regression estimate in Table 6 for family chaos suggests higher heritability
with higher chaos (diathesis-stress). The negative regression estimate for informal parent–child
communication indicates greater heritability with lower communication (diathesis-stress) as does the
negative estimate for instructive parent–child communication (diathesis-stress).

Table 6
Extended DF analysis of G  E
Environment Verbal Ability Non-verbal Ability
B SE B SE
Low SES .07 .16 .01 .06
Parental discipline .00 .05 .01 .04
Negative parental feelings .01 .05 .01 .04
Family chaos .17** .05 .05 .05
Maternal depression .09 .05 .04 .05
Maternal medical factors in pregnancy .01 .02 .04 .02
Twin medical risk  .07 .05 .09 .05
Instructive parent–child communication  .17** .05 .02 .04
Informal parent–child communication  .13** .05 .01 .04
Educational toys .00 .05 .03 .05
*p b .05; **p b .01.
K. Asbury et al. / Intelligence 33 (2005) 643–661 657

3. Discussion

This study was designed to answer two main questions: firstly, is the heritability of cognitive abilities
affected by measured environments in early childhood, and secondly, is G  E better described by the
diathesis-stress model or the bioecological approach? To answer these questions we utilized a large
sample with measures of both proximal and distal aspects of the environment. We found significant
interaction effects for verbal ability with family chaos, instructive parent–child communication and
informal parent–child communication ( p b .01). All three significant interactions appeared to support the
diathesis-stress model of G  E, although there are some lingering doubts about interpreting the
instructive parent–child communication results in this way. We conclude that G  E exists for verbal
ability in early childhood and tends to be in the direction of greater group heritability in high risk
environments.
Although the results for nonverbal ability were considerably weaker than those for verbal ability and
did not achieve statistical significance, they generally followed the same pattern of results. Verbal and
nonverbal abilities correlate moderately (r = .46) in the current sample, so similar patterns are to be
expected. So, while current results only allow us to conclude that we have found G  E for verbal ability,
we suggest that the same measured environmental forces also exert some influence, albeit to a lesser
extent, on the expression of genes for nonverbal ability. However, the possibility of increased
measurement bias on the verbal over the nonverbal measure should also be borne in mind as a potential
influence on the results.
Some of the non-significant G  E results also suggested an interaction effect at the extremes that did
not apply across the continuum. For example, for verbal ability, noteworthy G  E effects appeared at
the 15% and 25% extreme for SES and twin medical risk. Because these G  E effects did not emerge
for the other cut-offs, they were not found to be significant in the Extended DF analysis. Nonetheless,
such G  E interactions warrant further research because it is quite possible that some G  E
interactions will only be found for more extreme environments. Levels of underprivilege which affect
feeding a family or buying shoes for the children may very plausibly affect the heritability of cognitive
abilities in a way that relatively mild underprivilege, such as struggling to afford holidays and other
treats, may not.
Previous G  E research in the field of cognitive development has focused almost exclusively on SES.
In the case of the current research it could be argued that interactions between SES and cognitive
abilities do not exist. However, what our data actually suggest is that only very low SES has an effect
that, in the case of verbal ability, is to raise group heritability (diathesis-stress). We do not find a
significant interaction using Extended DF regression analysis because it is not an interaction that takes
place across the distribution. This suggests an opposite effect to that reported by Turkheimer et al. (2003)
and Rowe et al. (1999). The discrepancy between these findings may reflect unmeasured differences
between US and UK populations, or perhaps differences in the types of measure or methods of data
collection used. They are unlikely to reflect different degrees of poverty because, although the sample
used in one of the studies (Turkheimer et al., 2003) included a high proportion of families selected on the
basis of their low SES, the TEDS sample is a representative UK population sample. It is more likely that
we are witnessing differences between UK and US societies and, perhaps, their early childrearing and
education practices.
Our findings in general support the view that proximal environments have a more potent effect than
distal environments on the genes for verbal ability. Distal environments may, we suggest, only operate to
658 K. Asbury et al. / Intelligence 33 (2005) 643–661

moderate childhood cognition at the extremes of risk. It is therefore important that we move away from
an almost exclusive focus on SES and consider more measures of the proximal environment in G  E
research, as we have in the current study.
The trends in heritability estimates shown in Table 4 and confirmed in the analyses reported in Table 6
provide evidence for the presence of genotype-environment interaction for verbal ability with three
proximal measures of family environment: family chaos, instructive parent–child communication and
informal parent-child communication. For family chaos, the interpretation of higher chaos as a risk
variable is supported by correlations of about .17 between chaos and verbal ability. Similarly, the
correlations of about .29 between informal parent–child communication and verbal ability support the
interpretation that less informal communication is a risk factor. However, the interpretation of less
instructive parent–child communication as a risk factor for verbal development is on weaker ground
because this measure is uncorrelated with verbal ability (about  .06). In relation to the parent–child
communication measures it should also be borne in mind that they may operate as genetic rather than
environmental markers rendering the relationship between measured environment and child outcome
more difficult to interpret.
Interestingly, the pattern of correlations suggests that greater heritability with increased risk is due to
DZ correlations decreasing rather than MZ correlations increasing with increased risk. This suggests that
shared environment is more influential in lower risk families. This pattern applies more strongly to
verbal than nonverbal ability which is not surprising as our verbal measure shows more shared
environmental influence than our nonverbal measure.
The results as they stand are best described by the diathesis-stress model. What does it mean to say
that group heritability increases in higher risk environments? In their presentation of the bioecological
framework, Bronfenbrenner and Ceci (1994) argued that heritability estimates equate to the expression
of genetic potential. This suggests that people have a genetic ceiling to their abilities and that high levels
of proximal processes will support the expression of natural tendencies whereas natural abilities will not
be supported if proximal processes are low or other aspects of the environment inhibit the mechanism of
proximal process. Our findings suggest, in fact, that a risk environment acts in combination with genetic
potential so that children may show lower levels of ability or achievement than their genetic make-up
would predict.
We commented in the Introduction to this paper that G  E is an alluring concept for researchers
because it opens up possibilities for life-enhancing environmental interventions. The current research
does not, in itself, suggest anything so bold. These findings do suggest however that it may be especially
important to reduce the presence of environmental risk factors for children who are at known genetic risk
in order to reduce negative developmental outcomes associated with synergistic interaction effects. More
importantly, the findings provide suggestions as to the types of specific environmental risk factors that
interact with the individuals’ genotypes. In particular, our results point towards the desirability of further
exploring the relationship between verbal ability and family chaos, instructive parent–child
communication and informal parent–child communication. More research in this direction might
ultimately yield useful, genetically sensitive, messages for parents and preschool workers about how best
to nurture children’s verbal abilities, implying a potentially important role for shared environmental
influence. We know that shared environmental influence on IQ in childhood disappears by adulthood
(Plomin, 1986) but making the difference in childhood, and concurrently cultivating the relationship
between cognition and achievement, is likely to positively enhance adult life and to help some children
to outperform their genetic propensities.
K. Asbury et al. / Intelligence 33 (2005) 643–661 659

Acknowledgements

The authors are indebted to the twins and their parents in the Twins Early Development Study (TEDS)
for making the study possible. TEDS is supported by a program grant from the UK Medical Research
Council (G9424799). During the initial drafting of this paper Theodore Wachs was supported by a
Fulbright Fellowship.

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