Copyright 2003 by the Genetics Society of America
The Effect of Neutral Nonadditive Gene Action on the Quantitative Index of
Carlos Lo ´pez-Fanjul,*,1Almudena Ferna ´ndez†and Miguel A. Toro†
*Departamento de Gene ´tica, Facultad de Ciencias Biolo ´gicas, Universidad Complutense, 28040 Madrid, Spain and
†Departamento de Mejora Gene ´tica Animal, SGIT-INIA, 28040 Madrid, Spain
Manuscript received July 17, 2002
Accepted for publication April 10, 2003
fixation index (FST). Thus, divergent or convergent selection is usually invoked, respectively, as a cause of
the observed increase (QST? FST) or decrease (QST? FST) of QSTfrom its neutral expectation (QST? FST).
However, neutral nonadditive gene action can mimic the additive expectations under selection. We have
studied theoretically the effect of consecutive population bottlenecks on the difference FST? QSTfor two
neutral biallelic epistatic loci, covering all types of marginal gene action. With simple dominance, QST?
FSTfor only low to moderate frequencies of the recessive alleles; otherwise, QST? FST. Additional epistasis
extends the condition QST? FSTto a broader range of frequencies. Irrespective of the type of nonadditive
action, QST? FSTgenerally implies an increase of both the within-line additive variance after bottlenecks
over its ancestral value (VA) and the between-line variance over its additive expectation (2FSTVA). Thus,
both the redistribution of the genetic variance after bottlenecks and the FST? QSTvalue are governed
largely by the marginal properties of single loci. The results indicate that the use of the FST? QSTcriterion
to pure additive traits.
tion for quantitative traits is an important issue, in both
evolutionary and conservation genetics (Wright 1978;
Endler 1986). In the absence of selection, inbreeding
affects all genes to the same average degree, and the
effect of the breeding structure on population diver-
gence can be described by Wright’s among-population
fixation index FST. In parallel, a dimensionless measure
of the quantitative genetic variance among populations
(termed QSTby Spitze 1993) can be defined as QST? Vb/
(Vb? 2Vw), where Vband Vware, respectively, the be-
tween- and the additive within-population components
of the genetic variance for the trait considered. For
neutral genes, with additive action between and within
loci, it is expected that Vb ? 2FSTVA and Vw ? (1 ?
titative analog of FST. This result holds quite generally,
regardless of the model of population structure (Whit-
lock 1999). The computation of the expected diver-
gence of population means due to drift requires the
estimation of generally unknown parameters, such as
the rate of mutation, the time since divergence, and
the effective population size (Lande 1977). However,
SSESSING the relative contributions of natural se-
lection and genetic drift to population differentia-
for a given set of populations, an FSTestimate can be
obtained from marker loci, assumed to be neutral, and
it can be used as the null expectation that can be com-
pared to the corresponding QSTestimate for a quantita-
tive trait, assumed to be additive. Thus, divergent or con-
of the observed increase (QST? FST) or decrease (QST?
FST) of QSTfrom its neutral expectation (QST? FST).
Experimentally, this approach has been used in many
studies (see Merila ¨ and Crnokrak 2001 and McKay
and Latta 2002 for reviews). In most instances, the
errors in the estimation of FSTand QSTwere large, re-
sulting in nonsignificant pairwise comparisons of these
estimates. Nevertheless, a meta-analysis carried out by
Merila ¨ and Crnokrak (2001) indicated that QSTwas
generally larger than FST, and this result was interpreted
in the sense that a considerable part of the observed
population divergence for quantitative traits should be
attributed to differential selection pressures imposed by
local environmental conditions.
Notwithstanding, the correspondence between QST
and FSTdepends crucially on the assumption of pure ad-
ditive gene action. This may not be an important restric-
tion to the study of morphological traits, typically show-
ing substantial additive genetic variation and little or no
inbreeding depression, but will markedly affect that of
life-history traits, usually exhibiting larger levels of non-
additive variance and, correspondingly, higher inbreed-
ing depression (Crnokrak and Roff 1995; DeRose and
Roff 1999). In the absence of selection, it has been
1Corresponding author: Departamento de Gene ´tica, Facultad de Cien-
cias Biolo ´gicas, Universidad Complutense, 28040 Madrid, Spain.
Genetics 164: 1627–1633 (August 2003)
1628 C. Lo ´pez-Fanjul, A. Ferna ´ndez and M. A. Toro
shown theoretically that inbreeding can change the
magnitude of the contribution of dominant and/or epi-
static loci to the values of Vband Vw, relative to their
additive expectations (Robertson 1952; Goodnight
1988; Willis and Orr 1993; Cheverud and Routman
1996; Lo ´pez-Fanjul et al. 1999, 2000, 2002). In parallel,
increases of the additive variance with inbreeding have
been reported for viability in Drosophila melanogaster
(Lo ´pez-Fanjul and Villaverde 1989; Garcı ´a et al.
1994) and Tribolium castaneum (Ferna ´ndez et al. 1995)
and for morphological and behavioral traits in the
housefly (reviewed by Meffert 2000). Thus, nonaddi-
tive gene action can potentially modify the expected
additive relationship between FSTand QST.
In this article, we have investigated theoretically the
ence FST? QSTfor two-locus neutral epistatic systems,
covering all possible types of marginal gene action at
the single-locus level (excluding overdominance). Our
approach follows that of Robertson (1952), where the
expected values of the derived within-line additive vari-
ance and the between-line variance, after consecutive
bottlenecks of size N, are obtained from the expressions
giving the corresponding ancestral values in an infinite
frequency distribution in populations of size N with
binomial sampling. Explicit equations in terms of the
genetic effects and allele frequencies derived by Lo ´pez-
Fanjul et al. (2002) have been used, allowing the speci-
fication of the necessary conditions to observe a depar-
ture of QSTfrom the pertinent FSTvalue.
Genotypic values for the neutral two-locus epistatic system
11 ? sh1
1 ? s(h1? h2)
1 ? s(1 ? h1)
1 ? s
1 ? s(1 ? h2)
1 ? ks
1 ? sh2
1 ? s
s/2 (s ? 0) and hi(0 ? hi? 1) are, respectively, the basic
homozygous effect at each locus and the basic coefficient of
dominance at the ith locus, and k (k ? 2) is the epistatic
?i? s[hi? (1 ? 2hi)qi? (k ? 2)qiq2
?i? s[(1 ? 2hi) ? (k ? 2)q2
?i? hi/[1 ? (k ? 2)q2
Thus, epistasis (k ? 2) modifies the basic properties of
single loci, as ?i, ?i, and ?ibecome dependent on the
allelic frequencies at the other locus (qj); i.e., they are
contingent on the genetic background. For a given k
value, the basic (hi) and the marginal (?i) degrees of
dominance become closer to each other as qjdecreases.
On the other hand, ?iapproaches zero (complete re-
cessivity) as k and qjincrease.
In an infinitely large panmictic population, expres-
sions for the mean (ancestral mean M) and the additive
component of the genetic variance (ancestral additive
variance VA) can be obtained from Table 1, as
M ? 1 ? 2s?hiqi? s?(1 ? 2hi)q2
i ? (k ? 2)q2
where Hiis the ancestral heterozygosity at the ith locus
equilibrium, after t consecutive bottlenecks of N ran-
domly sampled parents each (derived mean Mt* and
additivevariance VAt*),can readilybe deducedby substi-
exact mth moment of the allelic frequency distribution
with binomial sampling, given by Crow and Kimura
(1970, p. 335). In parallel, the between-line variance
V(Mt) after t consecutive bottlenecks can be derived by
taking variances in Equation 4, the resulting expression
being also a function of the first four moments of the
allelic frequency distribution at each locus. As these
moments can also be written in terms of the inbreeding
coefficient after t generations (Ft), expressions for Mt*,
VAt*, and V(Mt) also apply when bottleneck sizes are not
constant from generation to generation. Those expres-
unmanageable, but numerical solutions can be calcu-
lated for any combination of allele frequencies, as well
as the corresponding value of the quantitative index of
next section). In the following, the notations Ft, Qt,
i(i ? 1, 2; m ? 1–4) and their expected values at
We consider the model developed by Lo ´pez-Fanjul
et al. (2002), where the variation is due to segregation
at two neutral independent loci (i ? 1, 2) at Hardy-
Weinberg equilibrium. At each locus there are two al-
leles, with frequencies piand qi(?1 ? pi). Both loci have
equal homozygous effect (s/2), showing any degree of
dominance in the absence of epistasis(hi? 0,1⁄2, or 1 for
complete recessive, additive, or complete dominance
action, respectively). This basic gene action can be
viewed as that shown by single loci segregating against
a fixed genetic background. Epistasis has been imposed
on that basic system, and it is represented by a factor k
affecting the genotypic value of the double homozygote
for the negative allele at each locus (k ? 2, k ? 2,
or k ? 2 for diminishing, reinforcing, or no epistasis,
respectively). A full specification of the genotypic values
effect of gene substitution (?i), the marginal genotypic
value of the heterozygote (?i, expressed as deviation
from the midhomozygote value), and the marginal de-
gree of dominance (?i) are given by
iin Equations 4 and 5 by the corresponding
1629 Epistasis and Population Divergence
V(Mt), and VAt* are kept for the two-locus system and
the subdivided population studied, but FST, QST, Vb, and
Vware used, respectively, with reference to the whole
set of loci affecting a metric trait and the relevant popu-
It can be shown (Lo ´pez-Fanjul et al. 2002) that the
change in mean after t bottlenecks is always negative
0 ? hi?
epistasis (k ? 2). Nevertheless, diminishing epistasis
(k ? 2) and/or basic dominance (incomplete or com-
plete,1⁄2? hi? 1) result in an unrealistic enhancement
of the mean with inbreeding and, therefore, they are
not considered further.
For pure additive action it is expected that Qt? Ft,
as VAt* ? (1 ? Ft)VAand V(Mt) ? 2FtVA(Wright 1951).
For additive-by-additive epistasis, Qt ? Ft for Ft ? 1
(Whitlock 1999) as VAt* ? (1 ? Ft)VA? 4Ft(1 ? Ft)VAA
and V(Mt) ? 2FtVA? 4Ft2VAA, where VAAis the additive-
by-additive variance component (Goodnight 1988).
With dominance (with or without epistasis) equations
giving VAt* and V(Mt) cannot be written in terms of
summary statistics, as in the previous cases, but as com-
plex functions of the allele frequencies and effects at
each locus and the pertinent epistatic factor (Robert-
son 1952; Willis and Orr 1993; Lo ´pez-Fanjul et al.
1999, 2000, 2002). However, for nonepistatic complete
recessive action (hi? 0, k ? 2), some further insight
on the redistribution of the genetic variance induced
by bottlenecks and, consequently, on the relationship
between Qtand Ft, can be achieved as follows.
In general, from Equation 5, the expected additive
variance after bottlenecks can be given as
tion 2). Equation 7 shows that VAt* always exceeds its
additive expectation, i.e., VAt* ? (1 ? Ft)VA. Further-
more, as ? cov(?2
be given as VA? 2(1 ? Ft)VD, implying qi? (1 ? Ft)/
(2 ? Ft), i.e., qi?1⁄2. These results also apply for incom-
plete recessives (0 ? hi?1⁄2).
In parallel, the between-line variance can be written as
i, Hi) ? 0, the condition VAt* ? VAcan
V(Mt) ? ?4? FtVA? F2
1⁄2) and reinforcing epistasis (k ? 2) or no
where ?4? s2?[E(q4
its additive expectation (2FtVA) for ?4? 3FtVA? F2
Moreover, Qt will be larger than Ft if ?4 ? 3FtVA ?
slightly more restrictive than those for V(Mt) ? 2FtVA,
unless Ftis large [e.g., V(Mt) ? 2FtVAfor ?4? 3FtVA?
Summarizing, for neutral loci and nonadditive gene
action (dominant and/or epistatic), Qtwill generally
depart from Ft, except in the particular case of V(Mt) ?
2FtVAt*/(1 ? Ft).
i) ? q4
i] ? 0. Thus, V(Mt) equals only
tVD and smaller otherwise, these conditions being
Three representativecases were studied,with additive
(hi?1⁄2) or recessive (hi? 0) basic gene action at both
loci (s ? 0.1) and strong reinforcing epistasis (k ? 6)
or with recessive nonepistatic action (hi? 0, k ? 2). For
each case, surfaces were represented (Figure 1), giv-
ing the values of the following contrasts after one bottle-
neck (N ? 2, F1? 0.25) for all possible combinations
of allelefrequencies atboth loci: (1)the ratioof derived
to ancestral additive components of variance VA1*/VA,
(2) the ratio of the between-line variance to its expected
value for additive gene action V(M1)/2F1VA, and (3) the
difference F1? Q1between the inbreeding coefficient
and the quantitative index of population divergence.
sis, intermediate results were obtained (not shown).
For complete recessive nonepistatic action, Q1? F1
for only low to moderate frequencies of the recessive
allele at both loci (or for the recessive allele fixed in one
locus and segregating at low frequency in the other);
otherwise, Q1? F1. The absolute value of the difference
F1? Q1increased as the corresponding allele frequen-
cies became more extreme. With additional epistasis,
the condition Q1? F1holds for a much broader range
of allele frequencies, and Q1? F1for only high frequen-
cies of the recessive allele at both loci (or for the domi-
nant allele fixed in one locus and the recessive one
segregating at high frequency in the other). This situa-
tion is similar to that obtained with basic additive action
and epistasis but, for low frequencies of both negative
reduced. As shown by Equation 3, this can be ascribed
to the marginal degrees of dominance (?i) becoming
closer to the basic ones (hi?1⁄2) as the frequencies of
both negative alleles diminish. However, that excess was
VAt* ? ? cov(?2
i, Hi) ? ?E(Hi)E(?2
? ? cov(?2
i, Hi) ? (1 ? Ft)?Hi(V(?i) ? ?it*2) (6)
(Lo ´pez-Fanjul et al. 2002), where E(Hi) ? (1 ? Ft)Hi,
average effect of gene substitution at the ith locus after
t bottlenecks and its variance, which can be deduced by
taking expectations or variances, respectively, in Equa-
tion 1. Equation 6 shows that any excess of VAt* over its
ral changes in ?i(represented by V(?i) and ?it*, respec-
tively), which are both induced by drift, as well as to
the covariance term, which depends on the ancestral
properties of dominant loci [? cov(?2
additive or additive-by-additive gene action]. Of course,
dominance may be basic (0 ? hi?1⁄2) or marginal (hi?
1⁄2, k ? 2). For nonepistatic complete recessives (hi? 0,
k ? 2), ?it* ? ?i, V(?i) ? Fts2Hi/2, and ? cov(?2
i, Hi) ? 0 for pure
i, Hi) ?
VAt* ? ? cov(?2
i, Hi) ? (1 ? Ft)(VA? 2FtVD), (7)
where VDis the dominance component of the ancestral
genetic variance, VD? ??2
i ? ?s2H2
i/4 (from Equa-
1630C. Lo ´pez-Fanjul, A. Ferna ´ndez and M. A. Toro
Figure 1.—Ratio of derived to ancestral additive components of variance VA1*/VA(log scale), ratio of the between-line variance
to its additive expectation V(M1)/2F1VA(log scale), and difference F1? Q1between the inbreeding coefficient and the quantitative
index of population divergence, after one bottleneck (N ? 2, F1?1⁄4), for (1) nonepistatic complete recessive action at both
loci (hi? 0, k ? 2), (2) basic complete recessive action at both loci and reinforcing epistasis (hi? 0, k ? 6), and (3) basic
additive action at both loci and reinforcing epistasis (hi?1⁄2, k ? 6). Darker zones correspond to ratios smaller than one or to
negative F1? Q1values.
preserved when the negative allele is fixed in one locus
and segregates at low frequency in the other as, in this
case, the marginal degree of dominance of this second
locus approaches zero (i.e., the locus becomes increas-
ingly recessive). These results apply to populations sub-
jected to a single bottleneck of any size, albeit the abso-
lute value of F1 ? Q1 decreased as the size of the
bottleneck increased. With basic recessive action, in-
creasing values of the epistatic factor k did not affect
much the absolute value of the contrast (not shown)
as, in this case, the basic and marginal degrees of domi-
nance are the same. However, with epistasis and basic
additive action, that absolute value was positively corre-
lated with k, as the marginal degree of dominance tends
1631 Epistasis and Population Divergence
to zero for increasing k values. Of course, for basic
additive action without epistasis F1? Q1.
As shown in Figure 1, Q1? F1holds approximately
for the whole range of allele frequencies implying both
V(M1) ? 2F1VAand VA1* ? VA, irrespective of the type
conditions also hold after consecutive bottlenecks, but
the absolute value of Ft? Qtinitially increases with the
number of bottlenecks until a maximum is reached for
Ftclose to 0.5 and then subsequently decreases to zero
(not shown). These changes have also been described
by Robertson (1952) for nonepistatic recessives at low
frequency. Summarizing, with epistasis, Qt? Ftfor all
combinations of allele frequencies at both loci, excep-
ting for high frequencies of the negative (recessive)
alleles. Without epistasis, however, Qt? Ftfor only low
to moderate frequencies of those alleles.
only as a modulating factor (Lo ´pez-Fanjul et al. 1999,
the consequences of population bottlenecks on the Ft?
Qtdifference generated by two-locus nonadditive neu-
tral systems. An extension of these results to the whole
set of loci determining the additive variance of a quanti-
tative trait will, in principle, require a complete specifi-
cation of their genotypic effects and allele frequencies,
as the contribution of loci with the same type of gene
sign, depending on their respective allele frequencies.
Generalizations into multilocus systems can be made
only if individual loci show the same type of gene action
and segregate with similar frequencies. Only in this situ-
ation do our theoretical results provide a framework
within which some experimental data can be inter-
preted. The following discussion is restricted to D. mela-
nogaster and T. castaneum, where detailed genetic infor-
mation on relevant traits is available.
At one extreme of the spectrum, we have traits such
as abdominal bristle number or wing size and shape
characteristics of the wing. In natural populations of
Drosophila, very little or no inbreeding depression has
been detected for those characters and their between-
and within-line additive variances after bottlenecks very
closely approached the expectations under the pure
additive model (Lo ´pez-Fanjul et al. 1989; Whitlock
and Fowler 1999). In parallel, spontaneous mutations
affecting bristle number, wing length, and wing width
occur at a low rate and have a relatively large average
homozygous effect (Garcı ´a-Dorado et al. 1999). Fur-
thermore, those mutations with an effect smaller than
one-half phenotypic standard deviation of the pertinent
trait were predominantly additive and quasi-neutral
(Santiago et al. 1992; Lo ´pez and Lo ´pez-Fanjul 1993;
Merchante et al. 1995). Thus, a large fraction of the
corresponding genetic variance in natural populations
will be contributed by a small number of quasi-neutral
additive loci segregating at intermediate frequencies
(Robertson 1967; Gallego and Lo ´pez-Fanjul 1983).
At the other end of the spectrum, we consider viability
in natural populations of Drosophila and Tribolium.
After bottlenecks, viability showed strong inbreeding
depression and its within-line additive variance signifi-
cantly increased above the ancestral value (Lo ´pez-Fan-
jul and Villaverde 1989; Garcı ´a et al. 1994; Ferna ´n-
of the trait should be due to partially (or totally) reces-
sive deleterious alleles segregating at low frequencies.
In Drosophila, most newly arisen mutations affecting
viability had, on the average, a relatively large homozy-
gous disadvantage and their gene action was close to
recessive (Garcı ´a-Dorado et al. 1999; Garcı ´a-Dorado
and Caballero 2000; Chavarrı ´as et al. 2001). Using
mutational information, Wang et al. (1998) have been
We have shown that the Qtvalue generated by neutral
lation bottlenecks, will always be larger or smaller than
its additive expectation Ft, with the trivial exception de-
termined by those particular combinations of allele fre-
quencies fixing the boundary lines between the positive
and negative regions of the Ft? Qtsurface. Therefore,
the use of the Ft? Qtdifference as a criterion to investi-
gate the relative importance of genetic drift and natural
selection in population differentiation is restricted to
pure additive traits, as nonadditive action at neutral
loci can mimic the expectations for additive loci under
divergent (Qt? Ft) or convergent selection (Qt? Ft).
Moreover, for nonneutral nonadditive loci, selection
will also affect (positively or negatively) the Ft ? Qt
value and this additional effect could even change the
expected sign of that difference under neutrality.
For nonadditive gene action, previous theoretical
work concerned with the divergence between Ftand Qt
was restricted to the neutral additive-by-additive model,
where Qt? Ftfor Ft? 1 (Whitlock 1999). However,
the effect of dominance (with or without epistasis) can
qualitatively alter that result, as Qtmay be smaller or
larger than Ft, depending on the relevant allele frequen-
cies. With simple dominance, Qt? Ftfor only low to
moderate frequencies of the recessive alleles, but addi-
tional epistasis extends that condition to higher values
of the frequencies of the negative (recessive) alleles at
one of the loci involved (but not at both). Irrespective
of the type of gene action considered, we have also
shown that Qt? Ftgenerally implies an increase of the
within-line additive variance after bottlenecks (VAt* ?
VA), as well as an excess of the between-line variance
over its additive expectation (V(Mt) ? 2FtVA). Thus,
both the redistribution of the genetic variance after
bottlenecksand thevalue ofFt? Qtare governedlargely
by the marginal properties of single loci, epistasis acting
1632C. Lo ´pez-Fanjul, A. Ferna ´ndez and M. A. Toro
known bout of random drift in sets of loci differing in
their predominant type of gene action. In other words,
the results in Table 2 can be taken as an experimental
check of the validity of our theoretical predictions.
Incomplete information on the genetic properties of
the traits studied makes the interpretation of the FST?
QSTdifference more problematic. Estimates of FST(from
molecular markers) and QST(for different quantitative
traits) have been reported for sets of populations in a
variety of plant and animal species (reviewed by Merila ¨
and Crnokrak 2001 and McKay and Latta 2002). For
most traits QSTwas larger than FST, this result being in-
terpreted as a consequence of differential population
adaptation to local conditions. The most common ex-
perimental design included populations from different
geographic origins, each of them subdivided into fami-
als assayed per family, all of them maintained under
the same environmental conditions. Here we are not
concerned with the validity of inferring the population
structure from the marker’s information, but we con-
ment of quantitative data (detailed by Merila ¨ and
Crnokrak 2001). Following standard ANOVA proce-
dures, the total variance for each trait was partitioned
between families, within populations, and within fami-
lies. In general, the genetic architecture of the traits
assayed was unknown and, therefore, the estimates of
the additive within-line variance obtained from full-sib
analysis could be biased upward, as they may include
fractions of the dominance and epistatic components
of variance, as well as twice the environmental compo-
maternaleffects). Biasesduetononadditive geneaction
will be more likely for life-history traits, which generally
logical traits show. Furthermore, estimates of the be-
tween-population variance could also be inflated to an
unknown amount, due to common environmental ef-
fects (maternal and nonmaternal) that have not been
situation, with biased estimates of the between- and
Vb? 2FST(1 ? a)VA, Vw? (1 ? FST)(1 ? b)VA, and QST?
(1 ? a)FST/[(1 ? a)FST? (1 ? b)(1 ? FST)]. Therefore,
the neutral expectation QST? FSTwill hold only when
the magnitude of both biases is the same (a ? b), and
a ? b or a ? b will, respectively, mimic the expectation
under divergent (QST ? FST) or convergent selection
(QST ? FST). In parallel, as shown by our theoretical
analysis, nonadditive action of neutral quantitative loci
could also distort the expected additive relationship
between FSTand QST, even if the estimates of QSTare
free from environmental biases.
Summarizing, the sign of the difference FST? QSTwill
be indicative of selection for only those traits whose
FSTand QSTestimates after experimental bottlenecks
Species and traitsV
Estimates of the between- (Vb) and the additive within- (Vw)
line components of variance after one or three consecutive
bottlenecks (N ? 2) and the corresponding FSTand QSTvalues
for morphological traits and viability in Drosophila melanogaster
and Tribolium castaneum.
aWhitlock and Fowler (1999) and unpublished data.
bLo ´pez-Fanjul et al. (1989).
cLo ´pez-Fanjul and Villaverde (1989).
dGarcı ´a et al. (1994).
eFerna ´ndez et al. (1995).
fAll estimates were corrected for common environmental
effects by subtracting the corresponding Vbat generation 0.
ence in a) or realized heritability after one generation of
artificial selection (references in b–e).
able to show that the inbreeding depression and the
increase in the additive variance of viability following
bottlenecks can be ascribed mainly to a rise in the fre-
quency of lethals and partially recessive mutations of
large deleterious effects.
Table 2 shows the between- and the additive within-
line components of the genetic variance after one or
three consecutive bottlenecks (N ? 2) and the corre-
sponding FSTand QSTvalues, for seven morphological
are defined by the intersections of the veins of the wing,
and abdominal bristle number) and viability in Dro-
sophila and Tribolium. As expected, FSTand QSTwere
very close for all morphological traits (average FST?
QST? ?0.018, range ?0.03–0) and, for viability, FSTwas
considerably larger than QSTin all cases (average FST?
QST? 0.14, range 0.08–0.30). It must be stressed that,
in the experiments reviewed, all lines have been main-
tained under the same environmental conditions and
have been subjected to a small number of bottlenecks
(typically one). Thus, the effect of selection can be as-
sumed to be small and the contrasting behavior of the
FST? QSTvalue for morphological traits and viability can
be ascribed essentially to the changes induced by a
1633 Epistasis and Population Divergence
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C03-01 from the Ministerio de Educacio ´n y Cultura and RZ01-028-
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An Introduction to Population Genet-
A comparison of inbreeding
The number of loci affect-
On the average coef-
The changes in genetic and
Increased heritable variation
Communicating editor: Z-B. Zeng