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J. evol. biol. 10 (1997) lOlO-061X,97~010001-16 I-16 $1.50+0.20/O

1journal

of Evolutionary

Biology

Target review

**A meta-analysis stability
**

A. P. Moller’.*

of the heritability

of developmental

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 fluctuating selection; heritability; meta-analysis. selection; fluctuating asymmetry;

Abstract The existence of additive genetic variance in developmental stability has important 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 fluctuating 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 experiments 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 asymmetry 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 Introduction

Merller

and Thornhill

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 (Ludwig, 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 conclusions from such studies differ considerably. Some studies claim that one measure of developmental stability, the degree of individual fluctuating asymmetry in morphological characters, is heritable (e.g., Hagen, 1973; Thornhill and Sauer, 1992; Mailer, 1994), while others have been unable to demonstrate a statistically significant 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 Data set We searched the literature for all available estimates of the heritability of and methods

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 information 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 asymmetry 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 directional 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 unweighted mean value because sample sizes never differed markedly among estimates. 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 unweighted 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 developmental 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 demonstrate fluctuating asymmetry differed in effect size from studies where the requirements 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 Heritability (SE) 0.192(0.063)” and plant height 78 fam. 0 Evans et al. (MS) I 16, 21 1 1 I I 0.4514 0.18*(0.07)” - 0.022(0.206)” 0.3275 o.14594’ PO.0237 P P P 56 20 21 I I I 1 1 I I 0 0 s 0.1089 Sib Effect size Study method N FA test Internal validity External validity Reference

1. Heritabilities

of developmental

stability

and additional

information

on genetic

studies

Species

Character

Brassica campestris Arabidopsis thaliana

IO traits Days to first flowering

Epilobium angustijolium Euphydryas editha Gryllodes sigillatus traits

Petal length 11 traits wing spot Wing

0.023(0.018)9’ 0.019(0.006)“”

Eyprepocnemis plorans Drosophila melanogaster Drosophila melanogaster Drosophila melanogaster Drosophila melanogaster Drosophila melanogaster Drosophila melanogaster

4 exoskeletal Chaetae Chaetae Chaetae Chaetae Chaetae Chaetae

I4 lines 49 21 sires 95 fam. I4 fam. 14, 8 fam. 94 57 I I I 0 0 0 1 I 1 0 0 1 I I 0 0

0.02016’ 0.5374” 0.5574Q 0.2563 0.5519 0.7337”’ 0.0472’“’ 12, 14 29 gen. 40 30-31 5, IO gen. 41 gen. IO gen. I 1 1 1 I 1 I I I I I I I I I I 0 0 0 0 0 I I I 1 0 I 1 I 0.0325 P P P P P P P P

P s s P s s S

Drosophila 0.26“” length 0.4814 0.3763 0.2699 0.0522 0.0706’9’ 0.3070 0.63*(0.16)‘@ 0.02”’ 0.017(0.015)‘~’ I .072*(0.436)‘s’ 0.2920

melanogasrer

Chaetae

Drosophila

falleni

Chaetae

Panorpa

oulgaris

Fore-wing

Gasterosteus aculeatus Salmo gairdneri Oncorhynchus mykiss Lacerta vivipara Hirundo rustica Dermatoglyphics Dental traits Dermatoglyphics 0.312*(0.040)” -o.04752” o.035*2’ 0.1540 P P P

Gill rakers Meristic Meristic Scales 8 traits

s s F g a 125 II3 150 fam. 0 0 I 0 0 0 I I I 2 3 E

Homo Homo Homo

sapiens sapiens sapiens

Bagchi and Iyama (1983) Moller (I 996) Mason et al. (1967) Eggert and Sakaluk (I 995) Castro et al. (MS) Mather (1953) Thoday (1958) Reeve (I 960) Reeve (1960) Beardmore (I 965) Tuinstra et al. (1990) Scheiner et al. (1991) Polak and Jaenike, unpubl. Thornhill and Sauer (1992) Hagen (1973) Leary et al. (1985) Leary et al. (1992) Chenuil (1991) Moller (1994, unpubl.) Holt (1954) Bailit et al. (1970) Singh (I 970)

Homo 0.0698’5) 0.0917”” 0.0025”’ 0.03(0.03)=’ 0.28(0.07)29’ 0.320*(0.200)‘“’ 0.350(0.143)~2’ 0.6006’ 0.1008 s P 11 gen. 200 I 1 I 0 1 0 0.0647’ P 133 0 0 1 0.3008 0.2240”’ P P 221 276 1 1 0 0 1 1 0.2250 Sib 301 1 0 1 0.0150’ Sib 75 1 0 1 Sib 32 1 0 I P, Sib P, Sib 445 423 I 1 0 0 1 I

sapiens

Dermatoglyphics

0.1 6*(0.04)24’

0.0797

P, Sib

711

0

0

1

Homo Homo traits traits

sapiens sapiens

Dermatoglyphics Dermatoglyphics

Homo

sapiens

Dental

Homo

sapiens

Dental

Homo

sapiens

Dermatoglyphics

Homo Homo

sapiens sapiens

Dermatoglyphics Morphology

Macaca

mulatta

Skeleton

Mus musculus Mus musculus

Dental traits Skeletal traits

Mi and Rashad (1977) Bener (1979) Bener and Erk (1979) Townsend and Brown (1980) Corruccini and Potter (1981) Loesch and Martin (1982) Martin et al. (I 982) Livshits and Kobyliansky (1989) McGrath et al. (1984) Leamy (1986) 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).

‘)) “‘1 ‘I) I71 r2) I.+1 Is) 16) “) Is) “) X” ?‘) X’ “’ X’ ‘s) X) ?‘) “) ?” “‘r z” Q) U’ U)

Mean (SE) of two heritability estimates reported pp. 1533154. Mean (SE) of two heritability estimates reported in Table 2. Effect size calculated from the regression coefficient of the high line in Fig. 4. Mean of four regression coefficients in Table 4. Mean of four heritability estimates for two characters at two temperatures in Table 2. A heritability estimate. A heritability estimate reported p, 261. /r2 of absolute asymmetry of forewing length was 0.964(0.351). A heritability estimate reported p. 310. A heritability estimate reported p. 31 I. The effect size was recalculated from data in Fig. 2a. Mean (SE) of three heritability estimates reported in Table 8. Mean correlation coefficient between parent and offspring asymmetry for two years. Mean (SE) of eight heritability estimates. Mean of four correlation coefficients reported pp. 225, 227 and 228. Mean of the two extremes of four correlation coefficients reported on p. 635. Mean (SE) of six heritability estimates reported in Table 4. Mean (SE) of two heritability estimates reported p. 279. Mean of 120 correlation coefficients among relatives for ten different traits reported in Tables I3 and 14. 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. Mean (SE) of two heritability estimates reported in Table 6. Midparent-child correlation coefficient for mean asymmetry reported in Table 2. Mean (SE) of 12 heritability estimates reported in Table 5. Mean (SE) regression coefficients for pooled lines in Table 3. 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; parentoffspring 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 estimates from parent-offspring regressions and sib analyses were not biased by maternal and common environment effects (i.e., maternal and common environment 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

Table Species 2. Additive genetic coefficients Character of variation (CV, ) for fluctuating asymmetry

Moller

and Thornhill size.

and character

**cv.4 (Fluctuating asymmetry) (‘Ih) chaetae chaetae 38.53
**

25.70 16.41 157.59 170.43 39.85

**CVA (Character size) (‘X,)
**

2.08

Reference

Drosophila Drosophila Panorpa

mrlanogaster fhllrni ix&ark

Sternopleural Sternopleural Wing length

10.15

4.44 23.07 4.09 4.52 32.80

Gastrrosteus aculeatus Hirundo rustica Homo Homo sapiens sapiens

Gill rakers Tail length Dental traits

Dermatoglyphics

186.08

Scheiner et al. (1991) Polak and Jaenike, unpubl. Thornhill and Sauer (1992) and unpubl. Hagen (1973) Moller (1994) and unpubl. Corruccini and Potter (1981) 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 developmental 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 fluctuating 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-evolutionary 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 intermediate 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 performance 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 coevolutionary 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 developmentally 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 instability, 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-environment 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 selection 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 evolutionary 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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