8/14/2019 A Meta-Analysis of the Her It Ability of Developmental Stability

1/16

0 Birkhiiuser Verlag, Basel, 1997J. evol. biol. 10 (1997) I-16lOlO-061X,97~010001-16 $1.50+0.20/O 1 ournal of Evolutionary Biology

Target review

A meta-analysis of the heritability of developmentalstabilityA. P. Moller.* and R. ThornhillLaborutoire dEcologie, 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.frDepurtment of Biology,, University of New Mexico, Albuquerque, NM 87131,USAKey words: Developmental stability; d irectional selection; fluctuating asymmetry;fluctuating selection; heritability; meta-analysis.

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

tant implications for our understanding of morphological variation. The heritabilityof individual fluctuating asymmetry and other measures of developmental stabilityhave frequently been estimated from parent-offspring regressions, sib analyses, orfrom selection experiments. Here we review by meta-analysis published estimates ofthe heritability of developmental stability, mainly the degree of individual fluctuat-ing asymmetry in morphological characters. The overall mean effect size ofheritabilities of individual fluctuating asymmetry was 0.19 from 34 studies of 17species differing highly significantly from zero (P < 0.0001). The mean heritabilityfor 14 species was 0.27. This indicates that there is a significant additive genet iccomponent 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 environmenteffects. Additive genetic coefficients of variation for individual fluctuating asymme-try were considerably higher than those for character size per se. Developmentalstability may be significantly heritable either because of strong directional selection,or fluctuating selection regimes which prevent populations from achieving a highdegree of developmental stability to current environmental and genetic conditions.

* Author for correspondence

8/14/2019 A Meta-Analysis of the Her It Ability of Developmental Stability

2/16

2Introduction

Merller and Thornhill

Morphological characters within species demonstrate a range of variation fromhigh ly stable as in skeletal characters of homeothermic vertebrates to extremelyvariable 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 highdegree of developmental instability; characters that are highly variable also tend todemonstrate elevated levels of developmental instab ility as measured by their degreeof fluctuating asymmetry (Soul& 1982; Soult : and Cuzin-Roudy, 1982). Fluctuatingasymmetry occurs when bilateral symmetry is the rule, but small directionallyrandom errors during development cause deviations from perfect symmetry (Lud-wig, 1932; Van Valen, 1962; Palmer and Strobeck, 1986; Parsons, 1990; MDller andSwaddle, 1997). These patterns of morphological variation can be the result of arecent history of directional selection which tends to decrease genomic co-adaptationas a result of allelic substitutions and hence decrease the leve l of developmentalcontrol. Under directional selection, both genetic and environmental perturbationsincrease developmental instability (Merller and Pomiankowski, 1993a).

A number of studies have addressed the question of whether developmentalstability has a heritable basis. Heritability of developmental stability has usuallybeen estimated from comparing measurements of ind ividual fluctuating asymmetryin sibs or parents and their offspring, or from selection experiments. The conclu-sions from such studies differ considerably. Some studies claim that one measure ofdevelopmental stability, the degree of individual fluctuating asymmetry in morpho-log ical 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 fluctuatingasymmetry is likely to have a low heritabili ty if performance of indiv iduals is closelyassociated with bila teral symmetry and the resulting well-functioning morphology.Furthermore, estimates of heri tabil ity often suffer from limited sample sizes andthus low statistical power (Cohen, 1984). The frequency of type II errors whenstandard errors are large and sample sizes small is therefore likely to be high insingle studies (Cohen, 1984). This is an ideal situation for meta-analysis which hasa unique abil ity to deal with type II errors in mul tiple studies (e.g., Glass, 1976;Hedges and Olkin, 1985; Arnqvist and Wooster, 1995).

In this paper we review heri tabi lity estimates of one measure of developmentalstability, the level of individual fluctuating asymmetry in morphological characters,using a meta-analysis of published information. We also discuss the evolutionarycauses and consequences of a statistically significant additive genetic component ofdevelopmental stability.

Materials and methodsData set

We searched the literature for all availab le estimates of the heritability of

8/14/2019 A Meta-Analysis of the Her It Ability of Developmental Stability

3/16

Heritability of developmental stability 3measures of developmental stability, mainly the level of individual fluctuatingasymmetry. We were also able to obtain some unpublished heri tabi lity estimatesfrom correspondence with scientists involved in studies of fluctuating asymmetry.Our data set of heri tabi lity estimates for developmental stability is not likely to bebiased due to the inclusion of these unpubl ished data. Some references tested forheritability of developemental stability, but without providing quantitative informa-tion on heritabilities (Sumner and Huestis, 1921; Paxman, 1956; Maynard Smithand Sondhi, 1960; Kindred, 1967; Lundstrom, 1967; Coyne, 1987; Markow andGottesman, 1989; Chakraborty et al., 1991). These studies therefore had to beexcluded from the analyses. Some of the selection experiments on fluctuatingasymmetry may have resulted in an evolutionary alteration of the kind of asymme-try from fluctuating asymmetry to direc tional asymmetry or antisymmetry (Palmerand Strobeck, 1986, 1992). If this is the case, the alterations in asymmetry still maymark developmental stability . It is still an unresolved question whether onlyfluctuating asymmetry or also other kinds of asymmetry should be considered toreflect developmental stability (Graham et al., 1993). We have therefore includedstudies like that of Mather (1953) in the present review even though the selectionexperiment may have resulted in a change of the kind of asymmetry displayed bythe morphological character. The meta-analysis also allows a test of whether theinclusion of studies based on characters that were not specifically tested fordemonstrating fluctuating asymmetry resulted in any bias in the conclusions.

Statistical proceduresWe 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 normaldistribution with a mean value of zero. Studies that have reported such tests andfound no statistically significant deviations are marked in Table 1 with 1, whilestudies without a test are marked with 0. The absence of statistical tests for thepresence of fluctuating asymmetry does of course not imply that the character didnot show f luctuating asymmetry. Most of these studies were based on large samplesizes, and the power of these statist ical tests was therefore high.

Estimates of heri tabil ity or correlations between relatives of ind ividual fluctuatingasymmetry were treated in a meta-analysis (Glass, 1976; Hedges and Olkin, 1985;Rosenthal, 1991; Arnqvist and Wooster, 1995). We used heritabili ties or correlationcoefficients 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 correlationcoefficient based on reported test statistics in the various publications, usingprocedures reported in Kirby (1993). The effect size of heri tabi lity estimates orregression coefficients was calcu lated 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

8/14/2019 A Meta-Analysis of the Her It Ability of Developmental Stability

4/16

4 Mnller and Thornhillestimatesof heritabilities or regression coefficients of that study in order not to biasthe results in favour of rejection of the null hypothesis of no relationship. A meaneffect size was subsequently calculated for each species. For the comparison ofeffect sizes n relation to study method (selection experiments vs. others) two effectsizes were calculated for species if estimates were available for both selectionexperiments 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 thez-transformed effect size of studyj (Kirby 1993). Mean effect size was tested againstthe null hypothesis of no effect after z-transformation of correlation coefficients(Rosenthal, 1991). Heterogeneity in effect size among studies was tested using achi-square test statistic calculated as x2 = C[(n, - Z, - Z,)] with k - 1 degrees offreedom, where nj is the sample size of the number of subjects n study j, Z, is thez-transformed effect size of study j, Z, is the mean z-transformed effect size, and kis the number of studies (Hedges and Olkin, 1985; Rosenthal, 1991).We attempted to determine additional variables that may have affected themagnitude of the heritability estimates, and in that way avoid problems ofinconsistency in methodology and study organism when combining the results fromdifferent studies Glass et al., 1981;Wolf, 1986). These ncluded (i) test for fluctuatingasymmetry, (ii) type of study (parent-offspring regression and sib analysis versusselection experiment), and (iii) internal validity. Selection experiments were generallynot experiments attempting to select for higher or lower levels of fluctuatingasymmetry. The correlated responseof asymmetry to selection on another charactercould be due to additive or dominance effects. Fluctuating asymmetry is thought tobe strongly influenced by dominance effects. The results of the experiments (with theexception of Beardmore (1965)) should therefore be considered in this light.Meta-analysis may cause problems if studies with high and low validity are mergedbecause he level of validity clearly affects the reliability of the heritability estimates.Internal validity concerns aspectsof the study that may render results suspect, whileexternal 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 lowor high. Internal validity was scored as high if(i) maternal and common environmenteffects were minimized by standardization of rearing conditions, or (ii) if samplesizeswere large (above 50). External validity was scored as high if(i) the study populationwas stable, and (ii) the study population had not experienced some kind of selectionof particular individuals due to the design of the experiment. Only internal validitywas included as a factor potentially affecting effect size because most studies wereclassified as having high external validity. The effects of three variables that mighinfluence 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 onz-transformed Pearson product-moment correlation coefficients.The studies included may represent a biased sample of all studies, if publicationis influenced by a specific result (Hunter and Schmidt, 1990). This problem seemsunlikely because the entire literature on developmental stability is a mixture ofstudies demonstrating and not demonstrating an additive genetic component.Publishing bias is therefore not assumed o increase the probability of a type-1 error

8/14/2019 A Meta-Analysis of the Her It Ability of Developmental Stability

5/16

Heritability of developmental stabil ity 5in the meta-analysis. The file-safe number of studies was calculated. It estimates thenumber of studies that would be needed to eliminate the effects significance whenthose 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 aspossible. Coefficients of variation for the two kinds of characters were compared inpaired t-tests after log,,,-transformation.All statistical tests reported are two-tailed. Values reported are means (SE).

ResultsHeritability of developmental stability

Heritabilities or other estimates of resemblance among relatives exist for 34studies of which 31 are positive and 3 negative. Nine out of 34 estimates werestatistically significant which is five times the number of studies predicted to reachstatistical significance by chance. Test statistics from all studieswere transformed toPearson product-moment correlation coefficients and thus to effect sizes using themethods described in Rosenthal (1991) and Kirby (1993). The average weightedeffect size was 0.188, which is highly significantly different from the null hypothesisof no effect when using the Stouffer method to convert one-tailed P-values intostandard normal deviates (z = 5.76, P < 0.0001). The heritability and effect sizeestimates 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 issignificantly different from zero (one-sample t-test, t = 3.39, df = 13, P = 0.0049). Atotal of 13 mean heritability estimates from the same number of studies werepositive while only one was negative. The cumulative frequency distribution ofmean heritability estimates for the 14 species s shown in Fig. 1. It is clear from thegraph 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 thatwould be needed to eliminate the effects significance when those studies showed noeffect (Rosenthal, 1991). This number exceeds hundred with z = 5.76 and P

8/14/2019 A Meta-Analysis of the Her It Ability of Developmental Stability

6/16

Te1Hae

odoma

sayaao

inomo

ogcsue

Se

Cae

Hay

(S

Eesz

Su

N

mh

F

Inen

Een

Ree

te

vdy

vdy

Baccms

Aadstha

IOtas

0100

01

Sb

D

tofsfown

apahg

04

s

Eoumaoum

Paleh

E

y

eh

1aswns

Gyo

sgau

Win

Ee

ms

poa

4e

ea

tas

Do

ama

e

Ca

Do

ama

e

Ca

Do

ama

e

Ca

Do

ama

e

Ca

Do

ama

e

Ca

Do

ama

e

Ca

Do

ama

e

Ca

Do

afae

Ca

Pp

ogs

Fewn

leh

Geoe

aeu

G

ras

Smgd

Msc

Oh

ms

Msc

Lavvpa

Se

Hu

ruc

8as

Hm

se

Dmoyc

Hm

se

Datas

Hm

se

Dmoyc

0100

03

P

-

o1

P

-0002

P0

P

- 00009

0000

- 02 I004s

0601@

00 0000~

0300

00

P

05

s

05Q

s

02

P

05

s

07

s

00

S

00

P

02

P

04

P

03

P

02

P

00

P

009

P

03

P

-o0

P

o02

P

01

P

7fam

I

I

12

1

1

5

1

I

2

1

0

2

I

0

11

I

I

2g

0

I

4

0

1

33

0

0

5IOg

0

I

4g

0

1

IOg

I

I

I4ln

I

1

4

I

0

2se

I

0

9fam

0

1

I4fam

0

I

18am

0

I

9

1

0

5

I

0

1

0

0

I3

0

0

1fam

I

0

0 I I I I I 1 1 1 I 1 I I I I I I I I I I I I

E

ea(M

B

aIym

(1Me

(9

M

ea(1

E

a

Su

(9Coea(M

Mh

(1

T

(1

R

(9

R

(1

Bdme

(9

Tnaea

(1Snea

(1PaaJk

uTn

a

S

(1

H

(1

Lyea(1

s

Lyea(1

s

C

(1

F

Me

(1

ga

uH

(1

2

B

ea(1

3

Sn

(9

E

8/14/2019 A Meta-Analysis of the Her It Ability of Developmental Stability

7/16

Hm

se

Dmoyc

016002

00

PSb

7

0

0

1

Ma

R

(1

1

B

(1

I

B

aEk

(1

I

Tw

a

Bow

(1

1

Cun

a

Pe(1

1

L

a

Mn(1

1

Mnea(9

1

Lvsa

Ka

(1

1

MGahea

(1

1

Lm

(1

0

Pk

a

Lm(1

005

PSb

4

I

00

PSb

4

1

Hm

se

Dmoyc

Hm

se

Dmoyc

Hm

se

Datas

0 0

00

Sb

3

1

0

Datas

0000=

Dmoyc

02002

Dmoyc

0302

Mpo

-

Seo

0301~

00

Sb

7

1

Hm

se

0

Hm

se

02

Sb

3

1

0

03

P

2

1

02

P

2

1

0 0

Hm

se

Hm

se

M

maa

00

P

1

0

0

M

muu

M

muu

Datas

Seatas

06

s

01

P

1g

I

2

1

I 0

Su

mh

P-emeb

opeosn

reeo

Seme

b

oseoem

Sb

emeb

osbays

Fte

tefofuun

amy

(wh

lemng

cae

vu

weram

whre

tosdao

wh

fe

dsbo

olemng

cae

vu

wenm

wham

vuozoismk

wh1weaa

oaeismk

wh0

Inen

vdy

Ihg

Oow

Een

vdy

1hg

Oow

*emesgcy

(P