0 Birkhiiuser Verlag, Basel, 1997

J. evol. biol. 10 (1997) I-16

lOlO-061X,97~010001-16 $1.50+0.20/O 1journal of Evolutionary Biology

Target review

A meta-analysis of the heritability of developmental

stability

A. P. Moller’.* and R. Thornhill’

‘Laborutoire d’Ecologie, CNRS URA 258, UniversitP Pierre et Murie Curie,

Bdt. A, 7the huge, 7 quui St. Bernard, Cuse 237, F-75252 Paris Cedex 5,
Frunce, e-mail: umoller@hull.snvjussieu.fr
‘Depurtment of’ Biology,, University of New Mexico, Albuquerque, NM 87131,
USA

Key words: Developmental stability; directional selection; fluctuating asymmetry;

fluctuating selection; heritability; meta-analysis.

Abstract

The existence of additive genetic variance in developmental stability has impor-

tant implications for our understanding of morphological variation. The heritability
of individual fluctuating asymmetry and other measures of developmental stability
have frequently been estimated from parent-offspring regressions, sib analyses, or
from selection experiments. Here we review by meta-analysis published estimates of
the heritability of developmental stability, mainly the degree of individual fluctuat-
ing asymmetry in morphological characters. The overall mean effect size of
heritabilities of individual fluctuating asymmetry was 0.19 from 34 studies of 17
species differing highly significantly from zero (P < 0.0001). The mean heritability
for 14 species was 0.27. This indicates that there is a significant additive genetic
component to developmental stability. Effect size was larger for selection experi-
ments than for studies based on parent-offspring regression or sib analyses,
implying that genetic estimates were unbiased by maternal or common environment
effects. Additive genetic coefficients of variation for individual fluctuating asymme-
try were considerably higher than those for character size per se. Developmental
stability may be significantly heritable either because of strong directional selection,
or fluctuating selection regimes which prevent populations from achieving a high
degree of developmental stability to current environmental and genetic conditions.

* Author for correspondence

2 Merller and Thornhill

Introduction

Morphological characters within species demonstrate a range of variation from

highly stable as in skeletal characters of homeothermic vertebrates to extremely
variable as in secondary sexual characters (e.g., Alatalo et al., 1987; Grant and Price,
1981). A high degree of phenotypic variance appears to be associated with a high
degree of developmental instability; characters that are highly variable also tend to
demonstrate elevated levels of developmental instability as measured by their degree
of fluctuating asymmetry (Soul& 1982; Soult: and Cuzin-Roudy, 1982). Fluctuating
asymmetry occurs when bilateral symmetry is the rule, but small directionally
random errors during development cause deviations from perfect symmetry (Lud-
wig, 1932; Van Valen, 1962; Palmer and Strobeck, 1986; Parsons, 1990; MDller and
Swaddle, 1997). These patterns of morphological variation can be the result of a
recent history of directional selection which tends to decrease genomic co-adaptation
as a result of allelic substitutions and hence decrease the level of developmental
control. Under directional selection, both genetic and environmental perturbations
increase developmental instability (Merller and Pomiankowski, 1993a).
A number of studies have addressed the question of whether developmental
stability has a heritable basis. Heritability of developmental stability has usually
been estimated from comparing measurements of individual fluctuating asymmetry
in sibs or parents and their offspring, or from selection experiments. The conclu-
sions from such studies differ considerably. Some studies claim that one measure of
developmental stability, the degree of individual fluctuating asymmetry in morpho-
logical characters, is heritable (e.g., Hagen, 1973; Thornhill and Sauer, 1992;
Mailer, 1994), while others have been unable to demonstrate a statistically signifi-
cant heritability (e.g., Thoday, 1958; Tuinstra et al., 1990). Individual fluctuating
asymmetry is likely to have a low heritability if performance of individuals is closely
associated with bilateral symmetry and the resulting well-functioning morphology.
Furthermore, estimates of heritability often suffer from limited sample sizes and
thus low statistical power (Cohen, 1984). The frequency of type II errors when
standard errors are large and sample sizes small is therefore likely to be high in
single studies (Cohen, 1984). This is an ideal situation for meta-analysis which has
a unique ability to deal with type II errors in multiple studies (e.g., Glass, 1976;
Hedges and Olkin, 1985; Arnqvist and Wooster, 1995).
In this paper we review heritability estimates of one measure of developmental
stability, the level of individual fluctuating asymmetry in morphological characters,
using a meta-analysis of published information. We also discuss the evolutionary
causes and consequences of a statistically significant additive genetic component of
developmental stability.

Materials and methods

Data set

We searched the literature for all available estimates of the heritability of

Heritability of developmental stability 3

measures of developmental stability, mainly the level of individual fluctuating

asymmetry. We were also able to obtain some unpublished heritability estimates
from correspondence with scientists involved in studies of fluctuating asymmetry.
Our data set of heritability estimates for developmental stability is not likely to be
biased due to the inclusion of these unpublished data. Some references tested for
heritability of developemental stability, but without providing quantitative informa-
tion on heritabilities (Sumner and Huestis, 1921; Paxman, 1956; Maynard Smith
and Sondhi, 1960; Kindred, 1967; Lundstrom, 1967; Coyne, 1987; Markow and
Gottesman, 1989; Chakraborty et al., 1991). These studies therefore had to be
excluded from the analyses. Some of the selection experiments on fluctuating
asymmetry may have resulted in an evolutionary alteration of the kind of asymme-
try from fluctuating asymmetry to directional asymmetry or antisymmetry (Palmer
and Strobeck, 1986, 1992). If this is the case, the alterations in asymmetry still may
mark developmental stability. It is still an unresolved question whether only
fluctuating asymmetry or also other kinds of asymmetry should be considered to
reflect developmental stability (Graham et al., 1993). We have therefore included
studies like that of Mather (1953) in the present review even though the selection
experiment may have resulted in a change of the kind of asymmetry displayed by
the morphological character. The meta-analysis also allows a test of whether the
inclusion of studies based on characters that were not specifically tested for
demonstrating fluctuating asymmetry resulted in any bias in the conclusions.

Statistical procedures

We specifically checked whether studies had tested for anti-symmetry or direc-

tional asymmetry, which may not reflect developmental stability. This can be done
by testing whether signed left-minus-right character values deviate from a normal
distribution with a mean value of zero. Studies that have reported such tests and
found no statistically significant deviations are marked in Table 1 with 1, while
studies without a test are marked with 0. The absence of statistical tests for the
presence of fluctuating asymmetry does of course not imply that the character did
not show fluctuating asymmetry. Most of these studies were based on large sample
sizes, and the power of these statistical tests was therefore high.
Estimates of heritability or correlations between relatives of individual fluctuating
asymmetry were treated in a meta-analysis (Glass, 1976; Hedges and Olkin, 1985;
Rosenthal, 1991; Arnqvist and Wooster, 1995). We used heritabilities or correlation
coefficients as estimates of the additive genetic component of individual asymmetry.
Estimates from different samples of the same study were combined as the un-
weighted mean value because sample sizes never differed markedly among esti-
mates. Effect size was calculated as the Pearson product-moment correlation
coefficient based on reported test statistics in the various publications, using
procedures reported in Kirby (1993). The effect size of heritability estimates or
regression coefficients was calculated from the t-statistic with Y = J(t2/(t2 + df)).
The effect size of each study was calculated as the mean effect size of the different
 4 Mnller and Thornhill

estimatesof heritabilities or regression coefficients of that study in order not to bias

the results in favour of rejection of the null hypothesis of no relationship. A mean
effect size was subsequently calculated for each species. For the comparison of
effect sizes in relation to study method (selection experiments vs. others) two effect
sizes were calculated for species if estimates were available for both selection
experiments and other methods. A weighted effect size was estimated as Z, =
(X(n - 3)Z,)/(X(ni - 3)) where nj is the number of subjects in study j, and Z, is the
z-transformed effect size of studyj (Kirby 1993). Mean effect size was tested against
the null hypothesis of no effect after z-transformation of correlation coefficients
(Rosenthal, 1991). Heterogeneity in effect size among studies was tested using a
chi-square test statistic calculated as x2 = C[(n, - Z, - Z,)‘] with k - 1 degrees of
freedom, where nj is the sample size of the number of subjects in study j, Z, is the
z-transformed effect size of study j, Z, is the mean z-transformed effect size, and k
is the number of studies (Hedges and Olkin, 1985; Rosenthal, 1991).
We attempted to determine additional variables that may have affected the
magnitude of the heritability estimates, and in that way avoid problems of
inconsistency in methodology and study organism when combining the results from
different studies(Glass et al., 1981;Wolf, 1986). These included (i) test for fluctuating
asymmetry, (ii) type of study (parent-offspring regression and sib analysis versus
selection experiment), and (iii) internal validity. Selection experiments were generally
not experiments attempting to select for higher or lower levels of fluctuating
asymmetry. The correlated responseof asymmetry to selection on another character
could be due to additive or dominance effects. Fluctuating asymmetry is thought to
be strongly influenced by dominance effects. The results of the experiments (with the
exception of Beardmore (1965)) should therefore be considered in this light.
Meta-analysis may cause problems if studies with high and low validity are merged
becausethe level of validity clearly affects the reliability of the heritability estimates.
Internal validity concerns aspectsof the study that may render results suspect, while
external validity concerns the ability to generalize results beyond the study (e.g.,
Cochran and Cox, 1957; Cox, 1958). Both types of validity were scored as either low
or high. Internal validity was scored as high if(i) maternal and common environment
effects were minimized by standardization of rearing conditions, or (ii) if samplesizes
were large (above 50). External validity was scored as high if(i) the study population
was stable, and (ii) the study population had not experienced some kind of selection
of particular individuals due to the design of the experiment. Only internal validity
was included as a factor potentially affecting effect size because most studies were
classified as having high external validity. The effects of three variables that migh
influence effect size ((i) test for fluctuating asymmetry, (ii) internal validity, and (iii)
type of study) were tested statistically by means of unpaired t-tests based on
z-transformed Pearson product-moment correlation coefficients.
The studies included may represent a biased sample of all studies, if publication
is influenced by a specific result (Hunter and Schmidt, 1990). This problem seems
unlikely because the entire literature on developmental stability is a mixture of
studies demonstrating and not demonstrating an additive genetic component.
Publishing bias is therefore not assumedto increase the probability of a type-1 error
Heritability of developmental stability 5

in the meta-analysis. The file-safe number of studies was calculated. It estimates the
number of studies that would be needed to eliminate the effect’s significance when
those studies showed no heritability (Rosenthal, 1991).
We calculated additive genetic coefficients of variation (CV, = (lOOJV, )/x,
where V, is the additive genetic variance and 2 is mean character value; Houle,
1992) for fluctuating asymmetry and character size per se for as many studies as
possible. Coefficients of variation for the two kinds of characters were compared in
paired t-tests after log,,,-transformation.
All statistical tests reported are two-tailed. Values reported are means (SE).

Results

Heritability of developmental stability

Heritabilities or other estimates of resemblance among relatives exist for 34

studies of which 31 are positive and 3 negative. Nine out of 34 estimates were
statistically significant which is five times the number of studies predicted to reach
statistical significance by chance. Test statistics from all studieswere transformed to
Pearson product-moment correlation coefficients and thus to effect sizes using the
methods described in Rosenthal (1991) and Kirby (1993). The average weighted
effect size was 0.188, which is highly significantly different from the null hypothesis
of no effect when using the Stouffer method to convert one-tailed P-values into
standard normal deviates (z = 5.76, P < 0.0001). The heritability and effect size
estimates of developmental stability are presented in Table 1. The overall un-
weighted mean heritability estimate is 0.27 (SE = 0.08, N= 14 species) which is
significantly different from zero (one-sample t-test, t = 3.39, df = 13, P = 0.0049). A
total of 13 mean heritability estimates from the same number of studies were
positive while only one was negative. The cumulative frequency distribution of
mean heritability estimates for the 14 speciesis shown in Fig. 1. It is clear from the
graph that most estimates are small with a median value of 0.21. In conclusion,
there appears to be a statistically significant additive genetic component of develop-
mental stability in morphological characters.
The file-safe number of studies was calculated as the number of studies that
would be needed to eliminate the effect’s significance when those studies showed no
effect (Rosenthal, 1991). This number exceeds hundred with z = 5.76 and P <
0.0001.
We then tested whether there was a statistically significant heterogeneity of effect
sizesamong the studies using the methods described in Rosenthal (1991). There was
indeed a statistically significant heterogeneity among studies (chi-square = 110.23,
df = 33, P < 0.001). One possibility is that studies based on characters that demon-
strate fluctuating asymmetry differed in effect size from studies where the require-
ments for fluctuating asymmetry were not tested statistically. This was not the case
when comparing z-transformed correlation coefficients (mean z-value (SE): test for
fluctuating asymmetry: 0.203(0.042), N = 21; no test: 0.300(0.086), N = 13; t = 1.13,
Table 1. Heritabilities of developmental stability and additional information on genetic studies

Species Character Heritability Effect Study N FA Internal External Reference

(SE) size method test validity validity

Brassica campestris IO traits 0.192(0.063)” 0.1089 Sib 78 fam. I I 0 Evans et al. (MS)
Arabidopsis thaliana Days to first flowering and plant height
0.4514 s 16, 21 1 1 I Bagchi and Iyama
(1983)
Epilobium angustijolium Petal length 0.18*(0.07)” 0.3275 P 56 1 I I Moller (I 996)
Euphydryas editha 11 traits wing spot - o.14594’ P 20 1 0 I Mason et al. (1967)
Gryllodes sigillatus Wing - 0.022(0.206)” PO.0237 P 21 I 0 I Eggert and Sakaluk
(I 995)
Eyprepocnemis plorans 4 exoskeletal traits 0.02016’ P 12, 14 I I I Castro et al. (MS)
Drosophila melanogaster Chaetae 0.5374” s 29 gen. 0 I 1 Mather (1953)
Drosophila melanogaster Chaetae - 0.5574Q s 40 0 1 1 Thoday (1958)
Drosophila melanogaster Chaetae 0.023(0.018)9’ 0.2563 P 30-31 0 0 1 Reeve (I 960)
Drosophila melanogaster Chaetae 0.019(0.006)“” 0.5519 s 5, IO gen. 0 I I Reeve (1960)
Drosophila melanogaster Chaetae - 0.7337”’ s 41 gen. 0 1 1 Beardmore (I 965)
Drosophila melanogaster Chaetae 0.0472’“’ S IO gen. I I I Tuinstra et al.
(1990)
Drosophila melanogasrer Chaetae 0.0325 P I4 lines I 1 I Scheiner et al.
(1991)
Drosophila falleni Chaetae 0.26“” 0.2920 P 49 I 0 I Polak and Jaenike,
unpubl.
Panorpa oulgaris Fore-wing length I .072*(0.436)‘s’ 0.4814 P 21 sires I 0 I Thornhill and
Sauer (1992)
Gasterosteus aculeatus Gill rakers 0.63*(0.16)‘@ 0.3763 P 95 fam. 0 1 I Hagen (1973)
Salmo gairdneri Meristic 0.02”’ 0.2699 P I4 fam. 0 I I Leary et al. (1985) s
Oncorhynchus mykiss Meristic 0.017(0.015)‘~’ 0.0522 P 14, 8 fam. 0 I I Leary et al. (1992) s
Lacerta vivipara Scales 0.0706’9’ P 94 1 0 I Chenuil (1991) F
Hirundo rustica 8 traits 0.3070 P 57 I 0 I Moller (1994, g
a
unpubl.)
Homo sapiens Dermatoglyphics -o.04752” P 125 0 0 I Holt (1954) 2
Homo sapiens Dental traits o.035*2’ P II3 0 0 I Bailit et al. (1970) 3
Homo sapiens Dermatoglyphics 0.312*(0.040)” 0.1540 P 150 fam. I 0 I Singh (I 970) E
Homo sapiens Dermatoglyphics 0.1 6*(0.04)24’ 0.0797 P, Sib 711 0 0 1 Mi and Rashad
(1977)
Homo sapiens Dermatoglyphics 0.0698’5) P, Sib 445 I 0 1 Bener (1979)
Homo sapiens Dermatoglyphics 0.0917”” P, Sib 423 1 0 I Bener and Erk
(1979)
Homo sapiens Dental traits 0.0025”’ Sib 32 1 0 I Townsend and
Brown (1980)
Homo sapiens Dental traits 0.03(0.03)=’ 0.0150’ Sib 75 1 0 1 Corruccini and
Potter (1981)
Homo sapiens Dermatoglyphics 0.28(0.07)29’ 0.2250 Sib 301 1 0 1 Loesch and
Martin (1982)
Homo sapiens Dermatoglyphics 0.320*(0.200)‘“’ 0.3008 P 221 1 0 1 Martin et al. (I 982)
Homo sapiens Morphology - 0.2240”’ P 276 1 0 1 Livshits and
Kobyliansky (1989)
Macaca mulatta Skeleton 0.350(0.143)~2’ 0.0647’ P 133 0 0 1 McGrath et al.
(1984)
Mus musculus Dental traits 0.6006’ s 11 gen. I I 1 Leamy (1986)
Mus musculus Skeletal traits 0.1008 P 200 1 0 0 Parker and
Leamy (1991)

Study method: P - estimate based on parent-offspring regression, S estimate based on selection experiment, Sib estimate based on sib analysis.
FA test: test for fluctuating asymmetry (whether left-minus-right character values were random with respect to side, and/or whether frequency
distributions of left-minus-right character values were normal with a mean value of zero) is marked with 1, while an absence of a test is marked
with 0.
Internal validity: I -high, O&low.
External validity: 1 -high, OGlow.
*: estimate significantly (P < 0.05) different from zero.
Notes:
‘r Mean (SE) of ten heritability estimates from Table 2.
‘) Mean (SE) of two heritability estimates from p. 89.
‘) A heritability estimate for father-offspring.
4, Mean of two correlation coefficients of the range reported p. 90.
” A heritability estimate reported p. 712.
6, Mean of seven correlation coefficients reported in Table 5.
‘) Mean effect size of eight regression coefficients calculated for low and high lines in Figs, 4 and 10.
‘) Mean effect size of seven regression coefficients calculated for high and low lines and F, lines in Table 3.
Table 1. (continued).

‘)) Mean (SE) of two heritability estimates reported pp. 1533154.

“‘1 Mean (SE) of two heritability estimates reported in Table 2.
‘I) Effect size calculated from the regression coefficient of the high line in Fig. 4.
I71 Mean of four regression coefficients in Table 4.
r2) Mean of four heritability estimates for two characters at two temperatures in Table 2.
I.+1 A heritability estimate.
Is) A heritability estimate reported p, 261. /r2 of absolute asymmetry of forewing length was 0.964(0.351).
16) A heritability estimate reported p. 310.
“) A heritability estimate reported p. 31 I. The effect size was recalculated from data in Fig. 2a.
Is) Mean (SE) of three heritability estimates reported in Table 8.
“) Mean correlation coefficient between parent and offspring asymmetry for two years.
X” Mean (SE) of eight heritability estimates.
?‘) Mean of four correlation coefficients reported pp. 225, 227 and 228.
X’ Mean of the two extremes of four correlation coefficients reported on p. 635.
“’ Mean (SE) of six heritability estimates reported in Table 4.
X’ Mean (SE) of two heritability estimates reported p. 279.
‘s) Mean of 120 correlation coefficients among relatives for ten different traits reported in Tables I3 and 14.
X) Mean of 60 correlation coefficients among relatives for five different traits reported in Table 6.
?‘) Mean of I2 correlation coefficients for two different traits reported in Table 3.
“) Mean (SE) of seven heritability estimates reported in Table 4.
?” Heritability estimate reported p. 93.
“‘r Mean (SE) of two heritability estimates reported in Table 6.
z” Midparent-child correlation coefficient for mean asymmetry reported in Table 2.
Q) Mean (SE) of 12 heritability estimates reported in Table 5.
U’ Mean (SE) regression coefficients for pooled lines in Table 3.
U) Mean heritability estimate for nine characters reported p. 148.
 Heritability of developmental stability 9
df = 32, P = 0.27). Although the power of this test probably is low (formal power
analyses do not exist for meta-analyses), There is no indication of a major effect.
A second possibility is that studies with high internal validity had higher effect
sizes than studies with low validity. This appeared to be so when comparing
z-transformed correlation coefficients (mean z-value (SE): high internal validity:
0.348(0.078), N = 15; low internal validity: 0.155(0.033), N = 19; t = 2.45, df = 32,
P = 0.02). This result is consistent with expectations that effect sizes should increase
when for example rearing conditions are standardized, and sources of confounding
variance are removed.
Finally, heritability estimates obtained from selection experiments should be less
affected by maternal and common environment effects than estimates based on
parent-offspring regression and sib analyses (Falconer, 1989). Effect size did in fact
differ among these two types of studies when comparing z-transformed correlation
coefficients (mean z-value (SE): selection experiments: 0.524(0.102), N = 7; parent-
offspring regression and sib analysis: 0.154(0.028), N = 27; t = 5.63, df = 32, P <
0.0001). Therefore, effect size increased when selection experiments rather than
parent-offspring regression was used as a method of study, suggesting that esti-
mates from parent-offspring regressions and sib analyses were not biased by
maternal and common environment effects (i.e., maternal and common environ-
ment effects alone die not create the resemblance between relatives).
Both types of studies revealed effect sizes significantly different from the null
expectation of no effect when using the Stouffer method to convert one-tailed
probabilities into standard normal deviates (selection experiments: z = 5.58, P <
0.0001; parent-offspring regressions and sib analyses: z = 7.38, P < 0.0001). Hence,
the additive genetic variance in developmental stability was statistically significant
independent of the type of study.

Fig. 1. Cumulative distribution of mean heritabilities for 14 different species.

 10 Moller and Thornhill

Table 2. Additive genetic coefficients of variation (CV, ) for fluctuating asymmetry and character size.

Species Character cv.4 CVA Reference

(Fluctuating (Character
asymmetry) size)
(‘Ih) (‘X,)

Drosophila mrlanogaster Sternopleural chaetae 38.53 2.08 Scheiner et al. (1991)

Drosophila fhllrni Sternopleural chaetae 25.70 10.15 Polak and Jaenike,
unpubl.
Panorpa ix&ark Wing length 16.41 4.44 Thornhill and Sauer
(1992) and unpubl.
Gastrrosteus aculeatus Gill rakers 157.59 23.07 Hagen (1973)
Hirundo rustica Tail length 170.43 4.09 Moller (1994)
and unpubl.
Homo sapiens Dental traits 39.85 4.52 Corruccini and
Potter (1981)
Homo sapiens Dermatoglyphics 186.08 32.80 Martin et al. (1982)

Additive genetic coejjkient of variution

A more appropriate measure of the evolvability of a character can be obtained by

calculating additive genetic coefficients of variation because they correct for scale
effects such as the relationship between phenotypic variation and trait size (Home,
1992). Unfortunately, there was no information on means and variances in most
studies, and the sample is therefore reduced considerably. Seven studies revealed
high additive genetic coefficients of variation for fluctuating asymmetry (Table 2).
These values were on average almost nine times as large as the corresponding
figures for character size per se, and this difference is statistically significant (paired
t-test based on log,,,-transformed data: t = 6.68, df = 6, P = 0.0005).

Discussion

The overall conclusion from the meta-analysis of the heritability of developmen-

tal stability is that there is a small, but statistically significant, additive genetic
component. Additive genetic variance in developmental stability as measured by
phenodeviants has also been reported in the literature (Rosenthal and Rosenthal,
1950; Gordon, 1954). Estimates of heritability based on parent-offspring regressions
and sib analyses may not represent true additive genetic variance because they may
include maternal and common environment effects (Falconer, 1989). However,
similar conclusions were reached from studies using parent-offspring regression or
sib analysis and from selection experiments, and it is thus unlikely that maternal or
common environment effects have biased the results considerably (Falconer, 1989).
On the other hand, selection experiments under controlled laboratory conditions
will always reduce the phenotypic variance because of access to ad libitum food and
absence or reduced levels of predators, parasites, and conspecific competitors. A
Heritability of developmental stability 11

reduced phenotypic variance will invariably result in a smaller response to selection

and thus give rise to inflated estimates of heritability. Finally, one estimate of the
heritability of individual fluctuating asymmetry was based on asymmetries corrected
for character size by using residuals of asymmetry regressed on character size
(Moller, 1994). Although such correction may provide better estimates of the
heritability, as suggested by Moller (1994) and Palmer (1994) corrections for
phenotypic correlations among characters are not commonly adopted in the
literature (Falconer, 1989).
Heritability estimates based on parent-offspring regression of individual fluctuat-
ing asymmetry may not be directly comparable to those of other morphological
characters because of the peculiar distributions of estimates of absolute asymmetry.
Fluctuating asymmetry is usually defined as the unsigned left-minus-right character
value, and the frequency distribution thus represents a truncated normal distribution.
The assumption of normally distributed y-values for each x-value of model I linear
regression is therefore violated, and that may result in biased heritability estimates
(Moller, 1994; Palmer, 1994). However, it is unlikely that this will result in any bias
of the null hypotheses tested in the present review.
Even though the heritability of developmental stability on average was small, an
additive genetic component of this magnitude will have important micro-evolution-
ary implications. Why is the heritability of developmental stability so low? A recent
review of heritabilities suggested that their magnitude depended on the character.
Morphological characters had the highest heritabilities, behavioural traits intermedi-
ate values, and life-history traits small values (Mousseau and Roff, 1987). These
observations are consistent with a corollary of Fisher’s fundamental theorem of
natural selection which suggests that characters closely associated with fitness will
have low heritabilities (Fisher, 1930). In contrast, more recent reviews of the genetic
variability of characters has demonstrated that the highest genetic variability exists
for traits closely associated with fitness such as life-history traits and secondary
sexual characters (Houle, 1992; Pomiankowski and Moller, 1995). This is probably
so because of the large number of genetic and environmental events affecting these
traits and the intense directional selection which tends to increase their phenotypic
variance (Houle, 1992). This is exactly the case for fluctuating asymmetry, which is
known to be affected by a host of genetic and environmental factors, and which is
strongly selected against (reviews in Palmer and Strobeck, 1986; Parson, 1990; Moller
and Swaddle, 1997). The small, average heritability of developmental stability
suggests that this trait is closely associated with fitness. The additive genetic
coefficients of variation for fluctuating asymmetry were many times larger than the
corresponding values for character size per se (Table 2). Even small levels of
developmental stability have important implications for the overall performance of
individuals (review in Moller and Swaddle, 1997), and deviant morphology in terms
of fluctuating asymmetry or phenodeviants will result in poor reproductive perfor-
mance if, for example, resource acquisition and ability to avoid predators are
associated with a well-balanced, symmetrical morphology (Moller and Swaddle,
1997). There is a high potential for evolutionary change because of the very high
additive genetic coefficients of variation.
12 Msller and Thornhill

Given that symmetrically and developmentally stable phenotypes perform best,

why should the heritable variance in developmental stability not have become
completely depleted due to selection? There are at least five reasons why that should
not be the case. First, continuous directional selection may have displaced the
phenotype of individuals from the developmentally controlled optimum and thus
have resulted in an increase in the genetic variance in developmental stability. One
example is sexual selection which tends to be directional and therefore displace the
male phenotype (and sometimes also the female phenotype if there is a strong
genetic correlation between the sexes) from the optimum under natural selection.
Intense directional selection will result in a reduction in the degree of developmental
stability and an increased level of fluctuating asymmetry (Thoday, 1958; Reeve,
1960, Leamy and Atchley, 1985; Leamy, 1986; Moller and Pomiankowski, 1993b;
review in Moller and Swaddle, 1997). A second example of a continuous directional
selection regime is host-parasite interactions or interactions between other kinds of
biotic players (Hamilton, 1982, 1986). Again, the hypothesized result is a reduction
in the degree of developmental stability (Moller and Pomiankowski, 1993b).
Second, the entry of new mutants into a developmentally stable genome may
result in genetic perturbations and these may increase the level of fluctuating
asymmetry as in the case of the Australian blowfly Lucilia cuprina (Clarke and
McKenzie, 1987). Similar phenomena may occur in cycling parasite-host coevolu-
tionary systems. New mutants that disrupt development may subsequently become
incorporated into the genome, and the level of fluctuating asymmetry will evolve
towards the background level prior to genetic perturbation (Clarke and McKenzie,
1987).
Third, characters that are subject to intense directional selection will tend to
demonstrate biased mutation (Mukai, 1964; Pomiankowski et al., 1991). If develop-
mentally well controlled phenotypes are at a selective advantage, developmental
stability as a trait must have been subject to intense directional selection. Most
mutations will result in phenotypes with higher degrees of developmental instabil-
ity, and such individuals will therefore perform less well than those without the
mutations.
Fourth, fluctuating selection pressures will always prevent many individuals from
developing the optimum phenotype given the current environmental and genetic
conditions. For example, genotypically large individuals may develop less well
under poor environmental conditions such as those prevailing in marginal habitats,
but not under favourable conditions in prime habitats. Such genotype-by-environ-
ment interactions will continuously produce asymmetrical phenotypes that are at a
selective disadvantage. Spatially or temporally fluctuating selection regimes thus
will tend to maintain additive genetic variance in the degree of developmental
stability.
Fifth, a heterozygote advantage may maintain genetic variance in fluctuating
asymmetry when fluctuating asymmetry is lowest in heterozygotes as is often the
case (see Mitton, 1993; review in Moller and Swaddle, 1997).
Fluctuating asymmetry has traditionally been used as an indicator of the ability
of individuals to cope with genetic and environmental stress (Zakharov, 1989;
Heritability of developmental stability 13

Parsons, 1990; review in Moller and Swaddle, 1997). An inherent assumption in the
use of the level of fluctuating asymmetry in assessment of environmental conditions
is that developmental stability per se does not have a heritable basis. The generally
small magnitude of the additive genetic variance component of developmental
stability suggests that fluctuating asymmetry may remain a reliable indicator of the
level of environmental stress. Since directional selection increases the level of
fluctuating asymmetry, characters subject to a regime of intense directional selec-
tion may be more suitable for assessment of environmental stress.
In conclusion, developmental stability of morphological characters demonstrate a
statistically significant additive genetic component, and this has important evolu-
tionary implications. Many traits may not be developmentally stable because of
prevailing directional or fluctuating selection regimes.

Acknowledgements

This paper arose from discussions at a workshop on developmental stability arranged by T. A.

Markow in Tempe, Arizona, June 1993. The participants in the workshop are acknowledged for their
contributions. J. P. M. Camacho, A. Evans, J. Jaenike, and M. Polak kindly provided unpublished
information. A.P.M. was supported by grants from the Swedish and Danish Natural Science Research
Councils. G. Amqvist, A. R. Palmer and M. Whitlock provided useful criticisms for improving the
manuscript.

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