Voje Et Al. - 2014 - Allometric Constraints and The Evolution of Allometry

O R I G I NA L A RT I C L E
doi:10.1111/evo.12312
ALLOMETRIC CONSTRAINTS AND THE

EVOLUTION OF ALLOMETRY
3
Kjetil L. Voje,1,2 Thomas F. Hansen,1 Camilla K. Egset,3 Geir H. Bolstad,3 and Christophe Pelabon
1
Department of Biosciences, Centre for Ecological and Evolutionary Synthesis, University of Oslo, Oslo, Norway
2
E-mail: k.l.voje@ibv.uio.no
Department of Biology, Centre for Biodiversity Dynamics, Norwegian University of Science and Technology, 7491
Trondheim, Norway
Received May 28, 2013

Accepted October 17, 2013
Morphological traits often covary within and among species according to simple power laws referred to as allometry. Such allometric relationships may result from common growth regulation, and this has given rise to the hypothesis that allometric exponents
may have low evolvability and constrain trait evolution. We formalize hypotheses for how allometry may constrain morphological
trait evolution across taxa, and test these using more than 300 empirical estimates of static (within-species) allometric relations
of animal morphological traits. Although we find evidence for evolutionary changes in allometric parameters on million-year,
cross-species time scales, there is limited evidence for microevolutionary changes in allometric slopes. Accordingly, we find that
static allometries often predict evolutionary allometries on the subspecies level, but less so across species. Although there is a
large body of work on allometry in a broad sense that includes all kinds of morphological traitsize relationships, we found
relatively little information about the evolution of allometry in the narrow sense of a power relationship. Despite the many claims
of microevolutionary changes of static allometries in the literature, hardly any of these apply to narrow-sense allometry, and we
argue that the hypothesis of strongly constrained static allometric slopes remains viable.
KEY WORDS:
Adaptation, evolutionary constraint, microevolution, macroevolution, ontogenetic allometry, static allometry.
Most quantitative traits are highly evolvable (Houle 1992; Hansen

et al. 2011) and respond rapidly to both artificial (e.g., Hill and
Caballero 1992) and natural selection (e.g., Endler 1986; Hendry
and Kinnison 1999; Kinnison and Hendry 2001; Hendry et al.
2008). At the same time there is ample evidence for inertia
(slow adaptation) from phylogenetic comparative studies (Hansen
2012), and prolonged episodes of stasis are commonly observed
in the fossil record (e.g., Simpson 1944; Eldredge and Gould
1972; Gingerich 2001; Gould 2002; Estes and Arnold 2007; Hunt
2007; Uyeda et al. 2011; Bell 2012). These contrasting patterns
have puzzled evolutionary biologists for decades and call for a
better understanding of the relative contribution of natural selection and evolutionary constraints on the location of species in
morphospace (Bradshaw 1991; Williams 1992; Bjorklund 1996;
Schluter 2000; Arnold et al. 2001; Hansen and Houle 2004;
Brakefield and Roskam 2006; Polly 2008; Futuyma 2010; Hansen

C
866
2012). Evolutionary stasis may be reconciled with high evolvability if individual traits are constrained by genetic correlations (e.g.,
Walsh and Blows 2009). In particular, many morphological traits
are strongly correlated with body size through scaling relations
that often follow a power law, Y = AXb , where Y is trait size and X
is body size (Huxley 1924, 1932; Huxley and Teissier 1936). Such
allometric scaling relationships are also common for physiological and life-history traits (e.g., Schmidt-Nielsen 1984; Charnov
1993; Kozlowski and Weiner 1997; West et al. 1997; Frank 2009).
On a loglog scale, a power law yields a linear equation with intercept log(A) and slope b. Ontogenetic, static, and evolutionary
allometries are recognized depending on whether the relation is
taken over the development of an individual, across individuals at
a similar developmental stage within a population, or across separate evolutionary lineages (Cock 1966; Gould 1966a; Cheverud
1982).
C 2013 The Society for the Study of Evolution.

2013 The Author(s). Evolution
Evolution 68-3: 866885
T H E E VO L U T I O N O F A L L O M E T RY
Hypotheses to explain evolutionary, cross-species, allometries fall in two broad classes: those based on functional adaptation
between traits and those based on developmental constraints on
the evolution of the traits. Huxley and others considered withinspecies allometry as a potential constraint on morphological trait
evolution (Huxley 1932; Simpson 1944; Rensch 1959; Gould
and Lewontin 1979; Gould 1971, 2002). This presupposes that
parameters of the ontogenetic and static allometries represent
meaningful biological traits that have limited potential to evolve.
A common interpretation of the ontogenetic and static allometric
slopes has been that they represent a ratio of proportional growth
between the trait and overall size (Huxley 1932; Savageau 1979;
Lande 1985; Stevens 2009) with low evolvability (e.g., Huxley
1932, p. 214). The interpretation and evolvability of allometric
intercepts have been less clear (but see White and Gould 1965;
Egset et al. 2012).
A strict form of the allometric-constraint hypothesis is that
evolutionary changes are bound to follow trajectories imposed by
ontogenetic or static allometries, so that evolutionary allometries
must resemble these. This requires that both the allometric slope
and intercept stay constant. Simpson (1944) used this assumption to derive selective explanations for seemingly maladaptive
extreme trait values such as the antlers of the Irish elk (Megaloceros giganteus), and Rensch (1959, p. 156) went as far as to
elevate it into a methodological principle when he claimed that
allometry is an important help to paleontologists, as one can find
out about the size of organs in animals of a body size exceeding
that of the types so far. A related argument is that evolutionary allometries would arise from static allometries if selection
acts solely on body size (Gould 1975; Lande 1979, 1985). Gould
also assumed a constant allometric slope when he used shifts in
allometric intercepts to measure heterochronic acceleration and
retardation across taxa (White and Gould 1965; Gould 1966a,
1971, 1977). Hence, there are different allometric-constraint hypotheses depending on whether it is the slope or the slope and the
intercept that are thought to be evolutionary fixed, and on whether
this happens at the ontogenetic or at the static level.
During the last decades, this complex of allometric-constraint
hypotheses has been the subject of many studies that have used
differences in static allometry as evidence for evolvability and
against the constraint hypotheses (e.g., Weber 1990; Emlen and
Nijhout 2000; Wilkinson 1993; Frankino et al. 2005, 2007; Shingleton et al. 2007; McGuigan et al. 2010). However, Houle et al.
(2011) pointed out that the majority of these studies have conceptualized allometry as any monotonic relation between trait
and body size, which is much broader than the classic narrow
sense of allometry as a power relation sensu Huxley (1932), Huxley and Teissier (1936), Gould (1966a, 1971, 1977), Cheverud
(1982), Lande (1979, 1985), Schmidt-Nielsen (1984), Eberhard
(2009), and many others. Houle et al. (2011) argued that it is
the derivation of the allometric power law from simple morphological growth regulation (Huxley 1924, 1932; Savageau 1979;
Lande 1985; Stevens 2009) or from allocation models (Bonduriansky and Day 2003) that motivates the constraint hypothesis.
Although studying the evolvability and evolution of broad-sense
allometry, as done by Emlen (1996), Baker and Wilkinson (2001),
Frankino et al. (2005, 2007, 2009), Okada and Miyatake (2009)
and others, is interesting and fully justified, it is not a test of
the classic allometric-constraint hypotheses. The current consensus of labile allometric relationships is therefore largely based
on studies that have neither estimated nor directly selected upon
narrow-sense allometric parameters as defined by Huxley.
In this study, we first clarify the theoretical relation between
the three levels of allometry (ontogenetic, static, and evolutionary)
to articulate different versions of the constraint hypothesis and to
provide testable predictions to distinguish between them. We then
test some of these predictions using morphological data from more
than 300 static allometric relationships. Finally, we evaluate the
evolutionary potential of the static allometric parameters based
on reports in the literature.
Theory
RELATION BETWEEN ONTOGENETIC, STATIC,
AND EVOLUTIONARY ALLOMETRY
Huxley (1924, 1932) showed that if two morphological traits

grew in proportion to each other, variation in growth rate would
necessarily produce a pattern of covariation between them that
follows a power law. Later this was refined by Savageau (1979),
who showed that the essential feature for the power law to arise
is that the growth dynamics is one dimensional in the sense that
the growth of the whole trait complex is regulated by a single
underlying variable (see also von Bertalanffy 1969 and Lande
1985). To illustrate this developmental model, let us assume that
the specific growth rate of two metric traits, Yt and Xt , at any one
point in time, t, is controlled by a common factor, zt , as
dYt /Yt dt = r y z t ,
(1a)
d X t / X t dt = r x z t ,
(1b)
where ry and rx are constants, and the common factor zt can follow
any form of complicated time-dependent dynamics. It follows that
trait values at any time fulfill the equations
ln(Yt ) = bZ t + ln(Y0 ),
(2a)
ln(X t ) = Z t + ln(X 0 ),
(2b)
t
where b = r y /r x , Z t = r x 0 z t dt is a complex biological variable describing growth regulation, and Xo and Yo are initial values
EVOLUTION MARCH 2014
867
K J E T I L L . VO J E E T A L .
species:
of the traits. This model implies

ln(Yt ) = b ln(X t ) + a,
(3)
where a = ln(Yo ) b ln(Xo ). Note that this allometric relation

does not depend on the common growth factor, Z.
If observations are made on the same individual at different
ages or developmental stages, represented by the parameter t, the
resulting different values of Zt give rise to different values of y =
ln[Y] and x = ln[X]. The variation in y with x during growth will
follow a linear relationship on log-scale according to equation (3),
which can be estimated by the ontogenetic allometric model
yo = bo xo + ao ,
(4)
where bo and ao describe the ontogenetic allometry. We use yo

and xo to signify that y and x vary over an ontogeny.
Any trait variation generated by genetic or environmental
differences in realization of the growth factor Z among individuals
in a population will also follow a power law summarized by the
static allometric model. We use
ys = bs xs + as
(6)
where bbo,x and bao,x are linear regression slopes of the ao and bo
on log size xs . Hence, the static allometric slope is a sum of the
average ontogenetic allometric slope in the population and two
regression slopes of the ontogenetic parameters on log size (see
Pelabon et al. 2013 for a related decomposition).
The effect of static allometry on the evolutionary allometric slope can be similarly derived by assuming a multivariate normal distribution of the underlying parameters across
(7)
where bbs,x and bas,x are the across-species linear regression coefficients of the parameters as and bs on species mean log size,
xe . Equation (7) tells us that an evolutionary allometric slope may
deviate from the static allometric slope if static slopes or intercepts are correlated with body size across species. For example,
a correlation between intercept and body size may arise from
selection if there is a functional relation between the trait and
body size. Hence, for static allometry to act as an absolute constraint on coadaptation between the trait and body size (or two
traits), it is necessary that both the static slope and the intercept
lack evolvability. In this case, different species must lie along the
static allometric trajectory (Fig. S1A). This is the basis of Landes
(1979, 1985) finding that selection acting exclusively on body size
will produce an evolutionary allometry along the static allometry
if additive genetic variances and covariances stay constant (i.e.,
constant genetic static allometric slope).
QUANTIFYING CONSTRAINTS ON TRAIT AND SHAPE
bs = Cov[ys ,xs ]/Var[xs ] = Cov[bo xs + ao ,xs ]/Var[xs ]
868
= E[bs ] + bbs,x E[xe ] + bas,x ,
(5)
to describe static allometry. Note that ontogenetic and static allometries are the same if there is no variation in bo and ao across
individuals. It does not matter if the sources of variation in Z
are different (genetic, environmental, or age related), because this
variation only places individuals at different points along the trajectory defined by the ontogenetic allometry without affecting the
shape of the relation.
Assume that the growth trajectories of x and y of every individual in a population follow the ontogenetic allometric model
yo = bo xo + ao , and that each individual is now observed at a
given developmental stage with size xo = xs and trait value yo =
ys , then, if the static allometric slope is estimated as an ordinary
least-squares regression coefficient, and we assume a multivariate normal distribution of all three parameters ao , bo, and xs , we
obtain
= E[bo ] + bbo,x E[xo ] + bao,x ,
be = Cov[ye , xe ]/Var[xe ] = Cov[bs xe + as ,xe ]/Var[xe ]
EVOLUTION
Assuming a static allometry between trait size ys and body size

xs (eq. 5) with body size centered on its mean and a multivariate
normal distribution of the parameters (as , bs , xs ), the variance in
trait size, Var[ys ], can be expressed as a function of variation in
the underlying parameters of the static allometry:
Var[ys ] = Var[bs xs + as ]
= Var[as ] + 2E[bs ]Cov[as ,xs ] + E[bs ]2 Var[xs ]
+ Var[bs ]Var[xs ] + Cov[bs , xs ]2 .
(8)
Equation (8) shows that the contribution of the different parameters to trait variance is not additive (i.e., not orthogonal),
and we will have to consider interactions when evaluating the
relative contribution of the different parameters. Both variation in
size and allometric intercept can generate some variation in the
trait by themselves, whereas variation in slope does not generate
trait variation unless size also vary (see Fig. S1 for a graphical
representation).
To quantify the constraints that arise, we can ask what happens if some of the allometric parameters or body size are held
constant in the sense that their means are not allowed to change.
This can be answered by calculating the trait variance conditional
on different parameter combinations. If the variation is considered to be additive genetic, this gives a direct measure of genetic
constraint as it is equivalent to computing conditional evolvabilities (Hansen et al. 2003; Hansen and Houle 2008). In Table 1,
Constraints on trait variance. The constraints are quantified by calculating the decrease in trait variance that results when
conditioning on the constraining parameter(s). Constraint refers to which variable(s) are kept fixed in the expression for trait variance
Table 1.
(eq. 8). Model gives the expression of the variance that is left in the trait given the specified constraint. Allometry refers to conditioning
on both the intercept, a, and slope, b, in the allometric relation. Shape is the trait variance conditional on size Var[y|x]. The constraint
intercept on Var[y|x] refers to keeping both the intercept and size constant, whereas slope on Var[y|x] refers to keeping both the
slope and size constant. All relations are computed under the assumptions of a multivariate normal distribution of a, b, and x and that
size, x, is mean centered across the compared taxa.
Constraint
Model
Size
Intercept
Slope
Allometry
Ex [Var[y|x]] = Var[a|x] + Var[b]Var[x] + Cov[b, x]2

Ea [Var[y|a]] = Var[x|a](E[b]2 + Var[b|a]) + Cov[b, x|a]2
Eb [Var[y|b]] = Var[a|b] + Var[x|b] (E[b]2 + Var[b])
Eb [Var[y|a, b]] = (E[b]2 +Var[b]) (Var[a]Var[b]Var[x] + 2Cov[a, b]Cov[a, x]Cov[b, x]
Cov[a, b]2 Var[x] Cov[a, x]2 Var[b] Cov[b, x]2 Var[a])/(Var[a]Var[b] Cov[a, b]2 )
Ex [Var[y|a, x]] = (Var[x]) (Var[a]Var[b]Var[x] + 2Cov[a, b]Cov[a, x]Cov[b, x]
Cov[a, b]2 Var[x] Cov[a, x]2 Var[b] Cov[b, x]2 Var[a])/(Var[a]Var[x] Cov[a, x]2 )
Var[y|b, x] = Var[a|b, x] = (Var[a]Var[b]Var[x] + 2Cov[a, b]Cov[a, x]Cov[b, x]
Cov[a, b]2 Var[x] Cov[a, x]2 Var[b] Cov[b, x]2 Var[a])/(Var[b]Var[x] Cov[b, x]2 )
Intercept on Var[y|x]
Slope on Var[y|x]
Note: Var[a|x] = Var[a] Cov[a, x]2 /Var[x], Var[x|a] = Var[x] Cov[a, x]2 /Var[a], Var[b|a] = Var[b] Cov[a, b]2 /Var[a], Var[a|b] = Var[a] Cov[a, b]2 /Var[b], and
Var[x|b] = Var[x] Cov[b, x]2 /Var[b]. Cov[b, x|a] = Cov[b, x] Cov[a, b]Cov[a, x]/Var[a].
we present the relevant conditional variances (see supplementary

Appendix for calculations). Interpreted as conditional evolvabilities these give the trait evolvability that would result if stabilizing
selection kept the mean of the conditioning parameter(s) constant
(Hansen et al. 2003). For example, the additive genetic variance
conditional on the allometric intercept, Var[y|a], gives the evolvability of the trait when the allometric intercept is under stabilizing
selection .
The trait variance conditional on size, Var[y|x], is simply
the residual trait variance around the allometric regression. We
can view this as a quantification of Goulds (1977) concept of
dissociation of trait from size. Hence, the conditional variances
Var[y|x, a] and Var[y|x, b] quantify the ability of the trait to dissociate from size (i.e., for shape evolution) when, respectively,
the intercept and slope are kept constant.
ASSESSING THE INFLUENCE OF ALLOMETRIC
PARAMETERS ON TRAIT EVOLUTION
The trait variance in equation (8) and the conditional variances

in Table 1 can be computed for allometric relations at any level
(ontogenetic, static, or evolutionary). We will use the conditional
variances at the among-taxa level to assess how much of evolution
in trait size and shape can be explained by changes in the different
static allometric parameters, as well as by changes in size. For
example, to assess the influence of changes in the allometric slope
on trait evolution, we compute how much the among-population
and among-species trait variances are reduced by conditioning
on the slope. The relative decrease in trait variance would then
indicate to what extent changes in slope have been important
in generating trait diversity across populations and species. This
procedure allows us to compare the influence of the different

parameters on a common scale set by the trait variance.
Materials and Methods

ASSESSING THE EVOLUTION OF ONTOGENETIC
AND STATIC ALLOMETRIES
To evaluate the extent to which allometries have evolved, we calculated the among-taxa (populations and species) variances in
allometric parameters in a set of published studies obtained by
searching for ontogenetic allometry and static allometry in
ISI Web of Knowledge. We also investigated citations in previous reviews on static allometries by Kodric-Brown et al. (2006),
Bonduriansky (2007), and Eberhard (2009). We constrained our
search to the animal kingdom and considered only studies that
estimated the allometric parameters on log-transformed morphological data analyzed using ordinary least-squares regression, that
reported standard errors of their estimates, and that reported comparable results for at least two taxa. We did not use studies in
which allometric exponents are estimated from loadings on first
principal components (Jolicoeur 1963), because it is then unclear
whether differences in the estimated exponents are due to differences in allometry or to differences in the direction of the principal
component (i.e., due to different measures of size). For completeness, we list such studies in supplementary Table S1. In total,
we were only able to use 14 of 75 studies that reported what they
defined as static (N = 52) or ontogenetic allometries (N = 23).
Excluded studies are listed in Tables S2 and S3. In one case, the
study of Kelly et al. (2000) on guppy, Poecilia reticulata, we reanalyzed the data, which were kindly provided by the authors. We
869
corrected for sampling error in the among-taxa slope and intercept

variances by subtracting the mean of the squared standard errors
of the parameters.
COMPARATIVE STUDIES OF THE EFFECTS OF STATIC
ALLOMETRIES ON TRAIT EVOLUTION
None of the studies we found in the literature reported all the

necessary parameters to analyze the relation between static and
evolutionary slopes using equation (7). We therefore reanalyzed
data from Baker and Wilkinson (2001), Kawano (2002, 2004,
2006), and Swallow et al. (2005) kindly provided by the authors.
These data from holometabolic insects enabled us to estimate a total of 304 morphological static allometries that could be organized
into 21 groups, each containing at least eight homologous static
allometries. Twelve groups consisted of static allometries from
populations belonging to the same species, whereas nine consisted
of static allometries from species belonging to the same genus. All
these are based on length measures of both the trait and body size.
We used the same data to investigate how trait and shape
variation across taxa depend on variation in body size and the
allometric parameters (eq. 8). We decided that a minimum of
10 homologous static allometries was necessary to estimate the
parameters in the models listed in Table 1. Eleven groups of
allometries satisfied this criterion, five within species and six
across species within the same genus. All analyses were conducted
in R (R Development Core Team 2012).
ASSESSING EVOLVABILITY BASED ON
QUANTITATIVE-GENETICS STUDIES
To assess the short-term evolvability of allometry, we searched the

literature for studies that had estimated additive genetic variation
in both intercept and slope of morphological narrow-sense allometries by breeding studies or artificial-selection experiments. Studies were obtained by complementing the search described in the
above section with a search for allometry combined with artificial selection in ISI Web of Knowledge. In total, we only found
two studies that provided estimates of additive genetic variances
in allometric slopes on appropriate scales: Atchley and Rutledge
(1980) on ontogenetic allometry and Egset et al. (2012) on static
allometry. In addition, we reanalyzed data from two studies: Tobler and Nijhout (2010), who used reduced major-axis regression
(data for reanalysis kindly provided by the authors) and Cayetano
et al. (2011), who did not report R2 values (data for reanalysis
obtained from Dryad).
Results
VARIATION IN STATIC ALLOMETRIC PARAMETERS
We were only able to use 10 of 52 studies that reported static

allometric parameters. Adding the insect data we reanalyze and
870
data on guppy populations from Kelly et al. (2000), we were able

to compare 37 sets of homologous static allometric slopes across
taxa (Table 2). All but three of these sets showed positive variance
after we controlled for sampling error, indicating that allometric
slopes do vary, but for the most part this variation was moderate
(Figs. 13). There were a few cases of extreme differences in
slope, but these involved allometries with very small or unreported
R2 . Among studies with a reasonable fit to the allometric model
(median R2 > 50%), the standard deviation (SD) of the slope
varied between 0.01 and 0.63 with a median of 0.19. The highest
variation in the slopes of well-fitting allometries was found for
mandible lengths within the beetle genus Odontolabis. The mean
static slope of the 23 analyzed species in this genus was 2.45, with
a SD of 0.63, which means that 95% of the slopes are expected to
be between 1.18 and 3.72 if normally distributed.
There was much less variation in static slopes at the subspecies level (SD = 0.07) than at the among-species level (SD
= 0.27). A SD of 0.07 means that 95% of the populations are
expected to fall within 0.14 slope units around the mean if
the slopes are normally distributed. This may not be more than
what could be expected due to phenotypic plasticity and sources
of error alone. Two exceptions provided clear evidence for slope
variation across populations. These involved the mandibles of the
Lucanid beetle Dorcus titanus and the eyestalks in the stalk-eyed
fly Cyrtodiopsis dalmanni, which had cross-population SDs of
0.26 and 0.25, respectively.
All 23 sets of comparisons of intercepts showed positive
variation with median SDs of 0.02 and 0.15 at the subspecies and
species levels, respectively (Table 2). The SD of a trait on log
scale is approximately equal to the coefficient of variation of the
trait on the original scale, and these two values hence mean that
differences in intercept generated trait differences with SDs of 2%
and 15% of the trait mean. As a benchmark, we may compare these
to the median within-population coefficient of variation of 7.5%
for quantitative traits from the review of Hansen et al. (2006).
Hence, differences in intercept across subspecies generate only
a small amount of trait variance, whereas there are substantial
differences across species.
VARIATION IN ONTOGENETIC ALLOMETRIC
PARAMETERS
Only four of 23 studies that reported homologous sets of ontogenetic allometries satisfied our criteria for inclusion, but these
yielded 29 sets for comparison. In general, these showed low levels of variation and 3 of the 29 sets even showed negative variance
after we controlled for sampling error (Table 2). The median SD of
ontogenetic slopes across species was 0.058 (range 0.0000.605).
A value of 0.058 means that 95% of the slopes are expected
to be between 0.88 and 1.12 if normally distributed around a
mean slope of 1 (i.e., isometry). We only found four homologous
Coleoptera
Pycnosiphorus (8 sp.)
Prosopocoilus (41 sp.)
Odontolabis (23 sp.)
Nigidius (8 sp.)
Lucanus (17 sp.)
Dorcus (37 sp.)
Aegus (10 sp.)
P. giraffa (8 pop.)
P. giraffa (8 pop.)
D. titanus (19 pop.)
D. titanus (19 pop.)
C. atlas (10 pop.)
C. causasus (10 pop.)
D. reichei (9 pop.)
X. gideon (13 pop.)
2 pop. of 3 sp. of Drosophila1

Dermaptera
Dermaptera (42 sp.)
C. dalmanni (8 pop.)
Diopsidae (30 sp.)
Insecta
Diptera
Scathophagidae (13 sp.)
Taxon
is indicated.
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Pronotum width
Pronotum width
Forceps
Elytra
Mandible length
Mandible length
Mandible length
Mandible length
Mandible length
Mandible length
Mandible length
Genitalia length
Mandible length
Mandible length
Genitalia length
Genitalia length
Genitalia length
Genitalia length
Genitalia length
Hind tibia (?)

Hind tibia (?)
Hind tibia (?)
Length
Length
Length
Length
Length
Length
Wing length
Size
Testis (?)
Clasper (?)
Mandible (?)
Eye span
Eye span
Torax width
Eye span
Torax width
Eye span
Sex comb
Trait
m
m
m
m
m
m
m
m
m
m
m
m
m
m
m
m
m
m
m
m
m
f
m
m
f
f
m
Sex
2.019, 0.341
2.253, 0.447
2.449, 0.633
1.396, 0.093
1.814, 0.303
2.366, 0.489
1.758, 0.270
2.122, 0.048
0.239, 0.050
1.533, 0.256
0.373, 0.055
0.438, 0.114
0.317, 0.066
0.260, 0.096
0.317, 0.043
1.344, 0.566
0.932, 0.397
0.695, 0.272
0.287, 0.270
1.002, 0.225
1.645, 0.455
1.188, 0.192
0.971, 0.011
1.818, 0.246
1.131, 0.000
1.188, 0.066
0.904, 0.138
Mean bs , SD
0.87 (0.84 0.90)

0.89 (0.88 0.95)
0.83 (0.77 0.91)
0.85 (0.77 0.90)
0.89 (0.82 0.94)
0.92 (0.90 0.96)
0.90 (0.87 0.95)
0.95 (0.94 0.96)
0.82 (0.78 0.84)
0.95 (0.94 0.98)
0.79 (0.71 0.86)
0.67 (0.57 0.76)
0.67 (0.61 0.76)
0.69 (0.63 0.73)
0.77 (0.70 0.83)
0.229, 0.058
0.941, 0.149
0.984, 0.277
0.464, 0.114
1.096, 0.117
0.932, 0.192
0.688, 0.112
1.398, 0.022
0.882, 0.018
1.245, 0.044
0.798, 0.049
1.111, 0.028
1.167, 0.020
0.649, 0.058
1.102, 0.033
0.56 (0.74 0.50)

0.41 (0.66 0.21)
0.83 (0.94 0.73)
0.90 (0.92 0.87)
0.89 (0.93 0.82)
0.80 (0.73 0.86)
0.94 (0.95 0.91)
0.85 (0.83 0.89)
0.92 (0.91 0.95)
0.16 (0.22 0.13)
Median R2
0.697, 0.697
0.638, 0.322
0.258, 0.019
0.896, 0.024
0.236, 0.012
0.730, 0.010
Mean as , SD
Kawano (2006)
Kawano (2006)
Kawano (2006)
Kawano (2006)
Kawano (2006)
Kawano (2006)
Kawano (2006)
Kawano (2004)
Kawano (2004)
Kawano (2004)
Kawano (2004)
Kawano (2002)
Kawano (2002)
Kawano (2004)
Kawano (2004)
(Continued)
Simmons and Tomkins (1996)

Simmons and Tomkins (1996)
Hosken et al. (2005)

Voje and Hansen (2013)
Sharma et al. (2011)
Reference
Variation in static slopes and intercepts across populations and species. Means and standard deviations (SD) of static slopes (bs ) and intercepts (as ) across a set of taxa.
A SD of zero means that the observed variance was less than the mean sampling variance of the parameter. Median R2 values and their 2575% quartiles (qt) are given for each
group of homologous static allometries. A question mark after trait or size means that the scale was not reported. All traits and overall size measures are in log mm if not otherwise
Table 2.
871
Continued.
872
Gonopodium
Gonopodium
Color spot (log mm2 )
Caudal fin
Eye orbit
Rostral horn
Carapace length
Total weight (log g)
Trait
Standard body length

Size measure4
Size measure3
Size measure3
Size measure3
Size measure3
Size
Reproductive tract
Length#
Length of penis
Length#
Variation in ontogenetic slopes and intercepts across populations and species
Aves
Fringillidae
Three species6
Bill width
Mass (log g)
Bill depth
Mass (log g)
Bill length
Mass (log g)
Tarsus length
Mass (log g)
Wing length
Mass (log g)
2 Gallus gallus domesticus
Shank length (log cm) Mass (log g)
F1 crosses
Shank length (log cm) Mass (log g)
Shank width
Mass (log g)
Shank width
Mass (log g)
Primates
Cercopithecidae
M. fascicularis, M.
Symphysis width
Mandibular length
nemestrina, M. mulatta, P.
cynocephalus
Mandibular arch width Mandibular length
P. reticulata (21 pop.)

Mammalia
Rodentia
Four species5
Actinopterygii
Cyprinodontiformes
B. episcopi (12 pop.)
P. reticulata (8 pop.)
Malacostraca
Decapoda
3 sp. of Chionoecetes2
Taxon
Table 2.
0.394, 0.013
0.256, 0.025
0.223, 0.049
f
m
f
Mix 0.955, 0.000
Mix 0.753, 0.000
(Continued)
Vinyard and Ravosa (1998)
Vinyard and Ravosa (1998)
Cock (1963)
Cock (1963)
Cock (1963)
Bjorklund (1994)
Bjorklund (1994)
Bjorklund (1994)
Bjorklund (1994)
Bjorklund (1994)
Cock (1963)
0.323, 0.023
0.353, 0.039
0.410, 0.000
0.593, 0.092
0.778, 0.230
0.399, 0.012
Mix
Mix
Mix
Mix
Mix
m
0.26 (0.48 0.10) Kinahan et al. (2008)

0.35 (0.50 0.18) Kinahan et al. (2008)
Jennions and Kelly (2002)
Kelly et al. (2000)
Kelly et al. (2000)

Egset et al. (2011)
Oh et al. (2011)
Oh et al. (2011)
Oh et al. (2011)
Oh et al. (2011)
0.24 (0.31 0.15)

0.08 (0.13 0.02)
0.17 (0.28 0.11)
0.95 (0.96 0.95)

0.92 (0.93 0.92)
0.89 (0.89 0.88)
0.95 (0.96 0.92)
Reference
-0.383, 0.093
-0.581, 0.437
Median R2
0.980, 0.000
0.245, 0.998
0.893, 0.067
0.649, 0.175
2.045, 1.220
0.781, 0.179
1.009, 0.027
0.950, 0.000
2.067, 0.146
2.969, 0.408
Mean bs , SD Mean as , SD
m
m
m
m
m
m
m
m
m
m
Sex
Snoutvent length
Snoutvent length
Snoutvent length
Snoutvent length
Snoutvent length
Mass (log g)
Mass (log g)
Mass (log g)
Mass (log g)
Mass (log g)
Jaw length
Jaw length
Jaw length
Jaw length
ENT length
ENT length
ENT length
ENT length7
Mass (log g)7
HG mass (log g)7
ACC and TP mass (log g)7
ACC mass (log g)7
Jaw length7
ENT length7
HG mass (log g)7
ACC mass (log g)7
ENT length7
HG mass (log g)7
ACC mass (log g)7
HG mass (log g)7
ACC mass (log g)7
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Mix
Sex
0.797, 0.058
2.993, 0.197
2.593, 0.333
2.340, 0.122
2.293, 0.171
0.281, 0.033
0.261, 0.014
0.860, 0.056
0.777, 0.059
0.753, 0.086
0.793, 0.074
2.933, 0.604
2.610, 0.185
2.543, 0.129
3.153, 0.323
2.813, 0.045
2.723, 0.150
0.870, 0.066
Mean bs , SD
Median R2
Mean as , SD
Anderson et al. (2012)

Reference
Data reanalyzed in this study. 1: D. simulans (2 pop), D. melanogaster (2 pop), D. pseudoobscura (2 pop). 2: C. japonicus, C. opilio, C. japonicus/opilio. 3: Longest distance across carapace of the lower lateral
Body size (x) variable centered on the population/species mean before the allometry was estimated.
Snoutvent length
Size
Jaw length7
Trait
Tip of nose to base of tail.
Front of head to tip of elytron.
Front of head to tip of wings.
accelerator linguae; ENT = entoglossal process; HG = m. hyoglossus; TP = tongue pad.
margin. 4: Tip of snout to insertion of the caudal fin. 5: C. damarensis, C. Hottentotus, G. capensis, B. suillus. 6: C. chloris, C. erythrinus, F. coelebs. 7: Trait explanations for Anderson et al. (2012). ACC = m.
Continued.
Reptilia
Squamata
C. calyptratus, F. pardalis, T.
johnstoni
Taxon
Table 2.
873
0.0
0.1
-0.3
0.2
-0.2
-0.1
0.0
0.1
0.9
0.8
0.7
0.6
0.5
be = 1.17 0.10, R2 = 95.6%

mean bs = 1.19 0.03, R2 = 92.3%
0.2
-0.2
-0.1
0.0
0.1
Cyrtodiopsis dalmanni
(females) N = 8
(males) N = 8
-0.1
0.0
0.1
-0.2
Log body size (mm)
-0.1
0.0
0.1
Log body size (mm)
0.2
0.3
0.2
0.1
be = 0.84 0.27, R2 = 62.2%

mean bs = 0.97 0.03, R2 = 80.0%
0.0
0.3
0.2
0.1
Log thorax widh (mm)
0.2
0.0
1.2
1.0
0.8
-0.2
be = 0.87 0.15, R2 = 84.8%

mean bs = 1.13 0.03, R2 = 85.0%
0.2
0.4
(males) N = 8
Log thorax width (mm)
Log body size (mm)
0.4
Log body size (mm)
be = 2.08 0.29, R2 = 89.4%

mean bs = 1.82 0.09, R2 = 93.7%
Figure 1.
Log eyespan length (mm)
1.4
1.2
1.0
0.8
Log mandible length (mm)
1.6
1.4
1.2
1.0
-0.1
be = 1.66 0.24, R2 = 73.6%

mean bs = 1.53 0.06, R2 = 95.2%
Log body size (mm)
0.6
Log eyespan length (mm)
-0.2
(females) N = 8
Dorcus titanus
(males) N = 19
be = 1.95 0.39, R2 = 80.69%

mean bs = 2.12 0.06, R2 = 94.69%
0.8
Prosopocoilus giraffa
(males) N = 8
-0.2
-0.1
0.0
0.1
0.2
Log body size (mm)
The relationship between evolutionary (stippled lines) and static (black lines) allometries of nongenital traits across popu-
lations within species. The regression of evolutionary slopes on mean static slope across the six groups in this figure is: evolutionary
slope = 0.24(0.31) + 1.14(0.21) mean static slope, R2 = 88%. Data for Prosopocoilus giraffa and Dorcus titanus originally published
in Kawano (2004) and for Cyrtodiopsis dalmanni in Swallow et al. (2005)
ontogenetic slopes estimated across population and their SDs

ranged from 0.012 to 0.049. None of the studies reported R2 ,
so we cannot judge how well these allometric relationships fit the
Huxley model, and ontogenetic allometries may often be nonlinear (e.g., Huxley 1932; Deacon 1990; Pelabon et al. 2013). None
of the ontogenetic studies reported intercepts.
EVOLUTIONARY ALLOMETRY AND THE STRICT

CONSTRAINT HYPOTHESIS
Under the strict constraint hypothesis, evolutionary allometry

should follow the static allometry, and most trait variation should
be generated by differences in mean body size across populations or species. For nongenital traits, we found a good match
between static and evolutionary allometries across populations
within species in all the six species we considered (Fig 1), but
the results were much more variable across species (Fig 2). This
may reflect static allometries acting as constraint on shorter time
scales, but less so on the million-year time scales that usually sep-
874
arate animal species. Genital traits showed a different pattern with

evolutionary allometries much steeper than the static allometries
in all cases (Fig 3).
Differences between static and evolutionary allometric slopes
were due to nonzero regressions of either the allometric intercept
or slope on body size across species (eq. 7; Table 3), although
these regression coefficients tend to have large standard errors.
The regression coefficient of intercept on log body size b(as,x)
ranged from 5.11 to 3.69 (median 0.44), whereas the minimum
and maximum coefficient of slope on log body size b(bs,x) ranged
from 1.98 to 4.31 (median 0.03). The two coefficients were
almost always opposite in sign and had compensatory effects on
the difference between the static and evolutionary regressions.
THE RELATIVE CONTRIBUTION OF ALLOMETRIC

PARAMETERS TO TRAIT EVOLUTION
Using the equations in Table 1, we can evaluate how much

trait variation across taxa is linked to variation in the allometric
-0.2
0.0
0.1
0.2
-0.20
-0.10
0.00
0.05
0.10
0.5
0.4
0.3
0.2
0.1
0.0
0.9
0.8
0.7
0.6
0.5
Log eyestalk length (mm)
0.3
be = 0.97 0.49, R2 = 39.0%

mean bs = 2.01 0.15, R2 = 87.0%
0.15
-0.15 -0.10 -0.05
0.00
0.05
0.10
0.15
Nigidius (males) N = 8
-0.2
-0.1
0.0
0.1
0.2
-0.2
0.0
0.2
0.7
0.6
0.5
0.4
0.3
0.2
0.1
1.5
1.0
-0.4
0.4
-0.15 -0.10 -0.05
0.00
0.05
0.10
-0.1
0.0
0.1
Log body size (mm)
0.2
-0.4
-0.2
0.0
0.2
Log body size (mm)
0.4
1.2
1.0
0.8
0.6
0.4
0.2
be = 1.27 0.09, R2 = 95.9%

mean bs = 1.76 0.10, R2 = 89.6%
0.0
1.0
0.5
0.0
1.6
1.4
1.2
1.0
-0.2
be = 1.28 0.09, R2 = 85.3%

mean bs = 2.37 0.09, R2 = 92.3%
0.15
1.4
Aegus (males) N = 10
Dorcus (males) N = 37
1.5
Lucanus (males) N = 17
Log body size (mm)
1.8
Log body size (mm)
0.8
0.6
0.4
0.5
0.3
be = 2.71 1.01, R2 = 54.4%

mean bs = 1.40 0.08, R2 = 84.5%
Log body size (mm)
be = 2.72 0.29, R2 = 85.4%

mean bs = 1.81 0.09, R2 = 88.9%
-0.3
be = 0.82 0.12, R2 = 70.7%

mean bs = 2.45 0.14, R2 = 83.0%
0.0
1.0
0.5
be = 0.87 0.17, R2 = 36.2%

mean bs = 2.25 0.08, R2 = 89.3%
0.8
Odontolabis (males) N = 23
Prosopocoilus (males) N = 41
Log body size (mm)
1.5
Log body size (mm)
-0.3
-0.1
be = 1.43 0.12, R2 = 93.0%

mean bs = 1.31 0.03, R2 = 90.1%
Log body size (mm)
0.0
-0.3
Pycnosiphorus (males) N = 8
Diasemopsis (females) N = 13
0.4
1.0
0.8
0.6
be = 1.78 0.18, R2 = 89.5%

mean bs = 1.91 0.10, R2 = 90.0%
0.4
Log eyestalk length (mm)
Diasemopsis (males) N = 13
-0.4
-0.2
0.0
0.2
0.4
Log body size (mm)
Figure 2. The relationship between evolutionary (stippled lines) and static (black lines) allometries of nongenital traits across species
belonging to the same genus. The regression of evolutionary slopes on mean static slope across the nine groups in this figure is:
evolutionary slope = 0.98(1.06) + 3.48(0.54) mean static slope, R2 = 32%. Data for Diasemopsis originally published in Baker and
Wilkinson (2001) and for Pycnosiphorus, Prosopocoilus, Odontolabis, Nigidius, Lucanus, Dorcus, and Aegus in Kawano (2006).
parameters. For nongenital traits, only a median of 26% (range:

759%) of log-trait variance across species remained after conditioning on body size, whereas a median of 60% (range: 20
92%) remained after conditioning on slope and intercept combined (Table 4). The variance left when conditioning only on
intercept (median 71%, range: 2196%) was slightly lower than
when conditioning only on slope (median 88%, range: 5196%).
The only nongenital trait we analyzed on the among-population

level showed qualitatively the same result as the across-species
analyses (Table 4).
For genital traits, the situation is different. Here, the allometric intercept was by far the most important parameter
(Table 4). The median variance left in (log) genitals after
conditioning on the intercept was 4.4%, whereas 41.0% and
875
0.0
0.1
-0.3
-0.1
0.0
0.1
0.2
0.8
0.7
0.6
0.5
0.4
be = 1.09 0.61, R2 = 31.4%

mean bs = 0.26 0.04, R2 = 69.2%
0.3
-0.3
-0.2
-0.1
0.0
0.1
0.2
0.00
0.05
0.10
0.15
-0.15 -0.10 -0.05
Log body size (mm)
0.00
0.05
0.10
Log body size (mm)
0.15
1.15
1.10
1.05
1.00
be = 0.93 0.26, R2 = 54.2%

mean bs = 0.32 0.02, R2 = 77.2%
0.95
1.20
1.15
1.10
1.05
be = 1.26 0.26, R2 = 63.1%

mean bs = 0.44 0.03, R2 = 67.1%
1.00
1.20
1.15
1.10
be = 1.74 0.18, R2 = 92.0%

mean bs = 0.32 0.03, R2 = 66.8%
0.3
1.20
Xylotrupes gideon
(males) N = 13
Log genitalia length (mm)
Chalcosoma atlas
(males) N = 16
1.25
Chalcosoma caucasus
(males) N = 10
Log body size (mm)
1.25
Log body size (mm)
-0.15 -0.10 -0.05
Figure 3.
-0.2
0.9
0.8
0.7
0.6
0.2
be = 0.77 0.26, R2 = 33.5%

mean bs = 0.37 0.02, R2 = 78.5%
Log body size (mm)
1.05
-0.1
0.95
0.90
be = 0.40 0.29, R2 = 24.8%

mean bs = 0.24 0.02, R2 = 81.5%
-0.2
Dorcus reichei
(males) N = 9
Dorcus titanus
(males) N = 19
0.85
0.80
Prosopocoilus giraffa
(males) N = 8
-0.2
-0.1
0.0
0.1
0.2
Log body size (mm)
The relationship between evolutionary (stippled lines) and static (black lines) allometries of genital traits across popula-
tions within species. The regression of evolutionary slopes on mean static slope across the six groups in this figure is: evolutionary
slope = 2.18 (0.96) + 0.33 (2.89) mean static slope, R2 = 12%. Data for Chalcosoma caucasus and Chalcosoma atlas originally
published in Kawano (2002) and for Prosopocoilus giraffa, Dorcus titanus, Dorcus reichei, and Xylotrupes gideon in Kawano (2004).
92.0% was left when conditioning on body size and slope,

respectively.
levels. For genital traits a median of 65.9% is removed. Given the

large effect of the intercept, most of the shape variance accounted
for by the slope must be due to interactions with the intercept.
THE RELATIVE CONTRIBUTION OF ALLOMETRIC

PARAMETERS TO SHAPE EVOLUTION
QUANTITATIVE-GENETICS STUDIES
Conditioning traits on body size generally removes the majority

of the variance across species and populations and the remaining (residual) variance can be considered as shape variance.
How much of this residual variance is due to variation in allometric slopes and intercepts indicates their relative importance for
shape evolution. The results in Table 4 show that this is overwhelmingly due to changes in the intercept. For nongenital traits,
the intercept removes a median of 96.3% of the shape variance
across species (Table 4). For genitals, a median of 99.8% of the
variance is removed across populations by conditioning on the
intercept (Table 4).
When shape is conditioned on the slope, a median of 80.9%
of the shape variance in nongenital traits is removed at the species
Almost all studies that claim to estimate the evolutionary potential

of allometric relations have either not analyzed the data on a
log scale or used line-fitting methods that are not appropriate
for estimation of parameters in the narrow-sense definition of
allometry (see Discussion; excluded studies are reported in Table
S4). Eventually, we were left with only four studies. Egset et al.
(2012) found no indication of evolvability of the static slope of
caudal fin area on body area in an artificial-selection experiment
in the guppy. In contrast, our reanalysis of Tobler and Nijhout
(2010) shows that females lines of tobacco hornworms selected for
smaller body mass have steeper static slopes for wing mass than
lines selected for larger body size (Fig. 4). The data of Cayetano et
al. (2011) on genital traits in Callosobruchus showed a very poor
876
877
Genital
Genital
Genital
Genital
Genital
Genital
Genital
Front of head to tip of wing.
Front of head to tip of elyton.
Mean
Median
Species
P. giraffa
D. titanus
D. reichei
C. atlas
C. caucasus
X. gideon
Mean
Median
Aegus
Dorcus
Lucanus
Nigidius
Odontolabis
Prosopocoilus
Nongenital
Mandible length
Mandible length
Eye span length
Eye span length
Thorax width
Thorax width
Species
P. giraffa
D. titanus
C. dalmanni
C. dalmanni
C. dalmanni
C. dalmanni
Mean
Median
Genus
Diasemophsis
Diasemophsis
Pycnosiphorus
Nongenital
Eye span
Eye span
Mandible length
(log mm)
Mandible length
(log mm)
Mandible length
(log mm)
Mandible length
(log mm)
Mandible length
(log mm)
Mandible length
(log mm)
Mandible length
(log mm)
Trait type
Taxon
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Length
Size measure
(7). All traits and overall size measures are in log mm.
8, m
19, m
9, m
16, m
10, m
13, m
10, m
37, m
17, m
8, m
23, m
41, m
13, m
13, f
8, m
8, m
19, m
8, m
8, f
8, m
8, f
N, sex
0.40 (0.29)
0.77 (0.26)
1.09 (0.61)
1.25 (0.26)
1.74 (0.18)
0.93 (0.26)
1.03
1.01
1.59
1.37
1.27 (0.09)
1.28 (0.09)
2.71 (0.29)
2.71 (1.01)
0.78 (0.11)
1.37 (0.17)
1.78 (0.18)
1.43 (0.12)
0.97 (0.49)
1.95 (0.39)
1.66 (0.24)
1.17 (0.10)
2.08 (0.29)
0.87 (0.15)
0.84 (0.27)
1.43
1.42
E. all. (SE)
0.41
0.79
1.17
1.25
1.74
0.98
1.06
1.08
1.65
1.42
1.28
1.25
2.82
2.76
0.81
1.42
2.05
1.48
0.96
1.94
1.67
1.14
2.08
0.91
0.87
1.44
1.41
Pred. be
24.81%
33.54%
31.44%
63.07%
91.99%
54.19%
49.84%
43.87%
74.89%
68.04%
95.94%
85.13%
54.39%
54.39%
68.04%
63.74%
89.49%
93.03%
38.97%
80.61%
73.64%
95.58%
89.43%
84.75%
62.14%
81.03%
82.68%
R2 e. all.
81.54%
78.54%
69.20%
67.09%
66.82%
77.22%
73.40%
73.21%
88.30%
89.28%
89.59%
92.28%
88.90%
84.52%
82.97%
89.28%
89.99%
90.09%
87.04%
94.69%
95.20%
92.38%
93.72%
85.02%
80.04%
90.18%
93.05%
Mean R2
s. all.
0.12 (1.85)
0.37 (0.90)
0.44 (2.38)
5.11 (2.20)
3.69 (3.77)
1.89 (0.95)
0.11
0.28
1.05
0.57
0.81 (0.55)
0.62 (0.81)
1.94 (1.65)
0.48 (3.14)
3.63 (1.49)
1.93 (1.10)
3.29 (1.13)
0.57 (0.45)
0.03 (5.42)
1.96 (4.73)
3.43 (2.68)
0.80 (0.98)
0.41 (2.86)
0.87 (0.58)
1.37 (0.62)
1.21
1.12
b(as,x) (SE)
0.03 (0.97)
0.47 (0.43)
0.32 (1.35)
3.36 (1.24)
1.23 (2.06)
0.77 (0.67)
0.36
0.18
0.75
0.77
1.06 (0.40)
1.20 (0.57)
1.96 (1.12)
0.73 (2.22)
1.30 (0.92)
0.77 (0.78)
4.31 (1.47)
0.91 (0.60)
1.00 (5.23)
1.27 (2.70)
1.98 (1.50)
0.95 (1.16)
0.19 (3.38)
1.40 (0.72)
1.81 (0.85)
0.95
1.34
b(bs,x) (SE)
0.24 (0.02)
0.37 (0.02)
0.26 (0.04)
0.43 (0.03)
0.32 (0.03)
0.32 (0.02)
0.32
0.32
1.92
1.91
1.76 (0.10)
2.37 (0.09)
1.81 (0.09)
1.40 (0.08)
2.45 (0.14)
2.25 (0.08)
1.91 (0.10)
1.31 (0.03)
2.02 (0.15)
2.12 (0.06)
1.53 (0.06)
1.19 (0.03)
1.82 (0.09)
1.13 (0.03)
0.97 (0.03)
1.46
1.36
E[bs ] (SE)
1.69 (0.01)
1.66 (0.01)
1.47 (0.01)
1.76 (0.01)
1.84 (0.00)
1.59 (0.01)
1.67
1.68
1.23
1.22
1.22 (0.07)
1.45 (0.02)
1.50 (0.02)
1.21 (0.01)
1.53 (0.03)
1.42 (0.02)
0.80 (0.02)
0.81 (0.01)
1.10 (0.01)
1.69 (0.01)
1.66 (0.01)
0.78 (0.01)
0.82 (0.01)
0.78 (0.01)
0.82 (0.01)
1.09
0.82
E[x] (SE)
Comparisons of evolutionary and static allometries. E. all. = slope of the evolutionary allometry; Pred. be = predicted evolutionary slope using equation (7); R2 E.
all. = the amount of variance explained by the evolutionary allometry; s. all. = static allometry; SE = standard error. The four last columns refer to the parameters in equation
Table 3.
Table 4. Groups of homologous allometries compared across populations. The numbers are percent of the predicted total trait variance
(eq. (8)) that remains when conditioning on different parameters as listed in Table 1. Intrasp. comp. = intraspecific comparisons; Intersp.
comp. = interspecific comparisons; m = male; f = female; N = number of taxa. All traits are linear measurements with units log mm.
Intercept on
Size
Intercept
Slope
Allometry
shape
Ex [Var[y|x]]/ Ea [Var[y|a]]/ Eb [Var[y|b]]/ Eb [Var[y|a, b]]/ Ex [Var[y|a, x]]/
Var[y]
Var[y]
Var[y]
Var[y]
Var[y]
Slope on
shape
Var[y|b, x]/
Var[y]
Genital
Genital
Genital
Genital
Mean
Median
19 Mandible
38.31%
8.43%
65.73%
43.65%
39.04%
40.98%
28.93%
4.84%
0.38%
6.93%
3.94%
4.02%
4.39%
59.97%
78.24%
96.43%
87.49%
99.04%
90.30%
91.96%
63.76%
3.69%
0.38%
4.96%
2.54%
2.89%
3.12%
55.23%
0.41%
0.19%
0.17%
0.19%
0.24%
0.19%
0.91%
37.90%
8.23%
38.11%
30.35%
28.65%
34.13%
14.26%
f
m
m
m
m
m
13
13
37
17
23
41
6.93%
11.41%
33.61%
17.43%
58.55%
47.54%
29.25%
25.52%
61.55%
74.70%
76.23%
21.43%
67.17%
96.16%
66.21%
70.94%
75.21%
51.14%
95.26%
79.81%
95.21%
95.93%
82.09%
87.51%
57.18%
43.24%
76.81%
20.36%
63.68%
92.15%
58.90%
60.43%
0.35%
1.47%
9.06%
1.01%
19.94%
6.02%
6.31%
3.75%
5.40%
9.04%
22.48%
15.78%
28.92%
40.75%
20.39%
19.13%
Taxon
Sex N
Intrasp. comp.
C. atlas
C. caucasus
D. titanus
X. gideon
m
m
m
m
16
10
19
13
Eye span
Eye span
Mandible
Mandible
Mandible
Mandible
Mean
Median
Not selected
-3.4 -3.2 -3.0 -2.8 -2.6 -2.4 -2.2
Log wing mass (gram)
D. titanus
Intersp. comp.
Diasemopsis
Diasemopsis
Dorcus
Lucanus
Odontolabis
Prosopocoilus
Trait
Down-selected
Up-selected
-1.0
-0.5
0.0
0.5
Log body mass (gram)

Figure 4.
The only known example of a change in a narrow-
sense static allometric slope under artificial selection. Based on

reanalysis of an experiment reported in Tobler and Nijhout (2010).
Static allometric relationships of log total wing mass, y, against log
fit to the allometric model (Fig. 5), and we argue in the discussion
that it is not informative about the evolvability of narrow-sense
allometry. Both Egset et al. (2012) and the reanalyzed results from
Tobler and Nijhout (2010) show strong evidence of evolvability of
the intercept whereas the results based on Cayetano et al. (2011) do
not. For ontogenetic slopes, the only study is Atchley and Rutledge
(1980), who found positive heritability for the slope of chest
circumference (h2 = 0.25 0.07) and tail length (h2 = 0.39
0.08) on body weight within six laboratory strains of rats selected
for more than 20 generations for bigger and smaller body weight.
They did not report the variance components, however, and the
genetic variances may thus have been very small and may also
have contained components of dominance and prenatal maternal
variance. Consistent with this possibility, there were no changes
in the allometric slopes over the 20 generations of selection (range
across lines: 0.350.37 for chest circumference and 0.450.47 for
tail length). We regard this study as inconclusive.
body mass, x, in females of the moth Manduca sexta are shown for
strains after 10 generations of artificial selection for larger body
Discussion
mass (crosses, stippled line), smaller body mass (circles, dotted

line), or not selected (triangles, unbroken line). The three regression lines are: up-selected: y = 2.460 (0.009) + 0.415 (0.038)x,
Although it was developed into its modern form by Julian

Huxley, the baptizer of the modern synthesis, allometry has rested
uneasily within the neodarwinian paradigm (Gayon 2000). On
a background of increasingly dominant functionalism, allometry
was one of few concepts associated with structuralist ideas (Gould
2002; Amundson 2005). Indeed, allometry played a central role
R2 = 52%; down-selected: y = 2.608 (0.030) + 0.639 (0.056)x,

R2 = 61%; not selected: y = 2.409 (0.007) + 0.581 (0.061)x,
R2 = 43%. The results for males are very similar (Fig. S2).
878
2.05
2.00
bs = 0.292 0.325, as = 2.074 0.004, R2 = 0.35%
-0.04
2.20
2.00
mono
-0.02
0.00
0.02
poly
2.15
Log flap length (micrometers)
poly
0.04
Log elytron length (micrometers)
bs = 0.465 0.265, as = 2.103 0.003, R2 = 3.63%
2.10
= 18.61%
2.05
bs = 1.302 0.353, as = 2.082 0.005,
R2
2.10
2.15
1.95
Log aedeagal spine length (micrometers)
mono
bs = 0.967 0.193, as = 2.102 0.003, R2 = 30.45%
-0.04
-0.02
0.00
0.02
0.04
Log elytron length (micrometers)
Figure 5. Reanalysis of the change in static allometry during the experimental-evolution study in the seed beetle Callosobruchus
maculatus from Cayetano et al. (2011). A and B show the differences in static allometries for two male genital traits after 1821
generations of monogamic (black dots and black line) and polygamic mating (gray crosses and gray dashed line). The size measure, log
elytra length, was centered on its mean before we estimated the allometric parameters. This means that the intercept gives the predicted
trait size for a mean-sized individual.
in Goulds structuralist challenge to the modern synthesis (e.g.,

Gould 1977, 2002; Gould and Lewontin 1979). For example, the
idea of evolution by heterochrony presupposes the existence of
ontogenetic constraints along which shape can evolve by shifts in
timing or rate of development. Allometry is the simplest and most
obvious example of such a constraint, and Gould (1974, 1977)
used it to support the hypothesis that the giant antlers of the Irish
elk had evolved by heterochrony extrapolating an ancestral allometry. This was not a new idea; architects of the modern synthesis
such as Huxley (1932), Simpson (1944, 1953), and Rensch (1959)
used extrapolations along ontogenetic allometries as alternative
Darwinian explanations for apparent patterns of orthogenesis in
which traits like antlers evolved beyond what seemed optimal for
the trait in isolation. In an extensive review of all known comparisons of ontogenetic allometries across species, populations and
lines of breeding, Cock (1966) concluded that well-established
differences in [the allometric slope] are relatively rare. Accordingly, it became popular to test for matches between ontogenetic
and evolutionary allometries, as in the well-debated case of horse
skull dimensions (see modern treatment in Radinsky 1984).
More recent research has shifted from allometry as constraints toward a more dynamical view of allometry as an evolving
and adapting entity (e.g., Kodric-Brown et al. 2006; Bonduriansky 2007; Eberhard 2009; Frankino et al. 2009). At first glance,
the evidence against allometry as a constraint seems overwhelming, but exactly how and at what time scales allometry may act
as a constraint is rarely precisely articulated. Moreover, allometry
has turned in into a hypernym with different meanings coexist-
ing in the literature, and the majority of evidence for evolving

allometry is evidence for various forms of shape evolution and
not evidence for changes in static allometric slopes in the original
narrow sense of the term (Houle et al. 2011). Although not denying the abundant evidence for evolvability of shape that has been
produced both with and without the label allometry attached,
we suggest that it is too early to conclude that the decades-old
view of allometries as constraints to evolution is inaccurate and
misleading (Emlen and Nijhout 2000, p. 663), because we cannot rule out that the subset of traits that do show a close fit to
the narrow-sense allometric model may indeed be constrained by
common growth regulation. Our survey of the literature has revealed that narrow-sense allometries are quite invariant and do
tend to predict evolutionary divergence below the species level,
but less so on longer time scales.
MORPHOLOGICAL ALLOMETRIES EVOLVE ON

MILLION-YEAR TIME SCALES
Even after controlling for sampling error, we found variation in

static allometric slopes and intercepts across species. This confirms that all aspects of static allometry are evolvable on the
million-year time scales that usually separate animal species, but
we have much less evidence of changes in ontogenetic allometries, which may simply reflect a lack of data. Some element of the
variation in static allometric parameters may be due to phenotypic
plasticity (Shingleton et al. 2009), but this is unlikely to account
for all the findings, and this explanation is also inconsistent with
879
invariable allometric parameters on short time scales as discussed

later.
ters may thus be reached along the highway of increasing body

size.
NO EVIDENCE THAT ALLOMETRIC SLOPES EVOLVE
ALLOMETRY AS A CONSTRAINT ON
FAST ON MICROEVOLUTIONARY TIME SCALES
MORPHOLOGICAL EVOLUTION
As expected, ontogenetic and static allometric slopes vary less

across populations than across species. Many interpopulation
studies of allometry involve traits with poor fit to the allometric model, and we could only identify two cases with both a good
fit and substantial variation in slope. One case concerns a single population of the stalk-eyed fly C. dalmanni, which differs
from six other populations in the static slope of eye-span (see
Voje and Hansen 2013, for detailed analysis). This is truly an
exception that confirms the rule, because these populations have
been separated for several million years (Swallow et al. 2005).
The other case involves populations of the stag beetle D. titanus.
Here we have no data on separation times, but it can not be ruled
out that these also have a long history of independent evolution.
Thus, although we found many cases of phenotypic differences in
static slopes across species, unambiguous examples of substantial differences in static slopes between recently diverged taxa are
absent. Furthermore, despite many general claims for evolvable
allometry in the literature, evidence for a response to selection
of well-fitting narrow-sense static slopes is currently limited to
the single case of a small change in wing allometry of Manduca
sexta (Tobler and Nijhout 2010 and Fig. 4). Hence, the hypothesis
that ontogenetic and static allometric slopes have low evolvability and are constrained on microevolutionary time scales is not
falsified.
Changes in the allometric slope seem negligible as a source of

morphological evolution. For most traits, changes in body size
are the most important source of evolutionary change, but changes
in intercept are also important, and for genital traits changes in
intercept explain more evolutionary variation than size.
These differences could reflect differences in selection pressures or in evolvability. Although selection pressures are difficult
to assess with our data, the numerous indications of low evolvability in the static slope opens the possibility that the lack of
influence of the slope may result from its low evolvability. The
relative influences of body size and intercept are more likely related to the frequency of directional selection acting on them.
Although one can argue that body size is more evolvable than the
typical trait intercept, because it is a complex many-dimensional
trait (Houle 1998), we have no indications that trait intercepts are
constrained on million-year time scales. Moreover, most of the
among-population variance in genitalia was generated by variation in the allometric intercept and not by body size. This is
not surprising given the generally shallow static allometries of
genitalia (Eberhard et al. 1998; Eberhard 2009).
GENITAL TRAITS
Genital traits differed from nongenital traits by showing a consistent difference between static and evolutionary slopes also on
the subspecies level. Static slopes of male genitalia are still near
constant, but consistently shallower than the evolutionary slopes.
Hence, differences in genitalia size must have arisen through
changes in the static intercept. This pattern extends the wellknown finding of a fascinatingly consistent tendency for male genitalia to show very shallow allometries within species of arthropods (Eberhard et al. 1998; Eberhard 2009). One of the suggested
explanations for this pattern is the one-size-fits-all hypothesis
(Eberhard et al. 1998), which postulates that the shallow slopes of
male genitalia is due to the fitness advantage of having a genital
size that is appropriately adjusted to the most common size of
females in the population (Eberhard et al. 1998). Our results suggest that differences in genital size across populations and species
are mainly due to selection operating on the genitals themselves.
Interestingly, secondary sexual traits like eyestalks in stalk-eyed
flies do not behave like genital traits, as most of their variation is explained by body size. Extreme secondary sexual charac-
880
LOW EVOLVABILITY OF THE STATIC ALLOMETRIC

SLOPE?
The minor effect of the static slope on trait size and shape variation across taxa does not in itself confirm a low evolvability of
this parameter. An alternative hypothesis is that the static allometric slope is under stabilizing selection to secure functional size
relationships between traits across different body sizes. One way
to differentiate between these two hypotheses is to compare the
evolvability of the static slope with the evolvability of the static
intercept.
Of the eight studies we found that had used artificial selection to test the evolvability of the static slope, only three had
estimated the relevant narrow-sense allometric parameters. In an
artificial-selection study with guppy, Egset et al. (2012) did not
find a response in the allometric slope of caudal fin area in relation
to body area despite a robust response in the intercept. Similarly,
Atchley and Rutledge (1980) detected no response in ontogenetic
slopes during selection on body size in lab rats. They did find positive heritabilities within the lines at the end of the experiment,
however, but in the absence of variance estimates these are not
informative of evolvability (see Hansen et al. 2011). Cayetano
et al. (2011) found changes in the allometric slopes of two of
11 genital traits in the seed beetle Callosobruchus maculates exposed to different levels of sexual selection. It is not clear that
this result is interpretable within the Huxley framework, however,

as the traits were almost unrelated to body size in the first place.
Size (log elytra length) explained 0% and 31%, respectively, of the
variance in log spine length and log aedagus flap length in monogamous lines and 19% and 4% in polygamous lines. The claim by
Cayetano et al. (2011) that their results provide the first experimental demonstration of evolution of static allometric slopes as a
function of sexual selection may therefore be technically correct
in the sense that the slopes are statistically significantly different,
but has little relevance in the framework of the narrow-sense allometric model. An alternative interpretation is that the traits do
not fit the allometric model and that the observed changes reflect
changes in nonallometric residual variation. We do not suggest
any cut-off value for how strongly two traits should correlate to
be meaningful in testing the constraint hypothesis, but we argue
that it is important to have these issues in mind when evaluating
the constraint hypothesis.
Currently, the only indication of evolvable narrow-sense allometric slopes in animal morphology is therefore the Tobler and
Nijhout (2010) artificial-selection study on M. sexta (Fig. 4). This
contrasts with several studies finding the allometric intercept to
be evolvable on microevolutionary time scales (e.g., Owen and
Harder 1995; Tobler and Nijhout 2010; Egset et al. 2012). To make
progress, we need more quantitative-genetics studies specifically
focused on investigating the evolutionary potential of narrowsense static or ontogenetic allometric slopes.
DO CHANGES IN SIZE INDUCE CHANGES IN SLOPE?
Gould (1966a,b) proposed that larger-sized animals would evolve

a shallower static slope to avoid nonadaptive extreme trait sizes in
larger individuals. Assuming that the body size range in our data
is large enough to detect such an effect, we found little support for
Goulds hypothesis; the regressions of static slope on body size
were just as likely to be positive as negative, and only two positive
and two negative slopes of our 21 regressions were statistically
significantly different from zero (see also Kawano 2006 and Voje
and Hansen 2013).
The results from Tobler and Nijhouts (2010) artificialselection study show that the evolution of static allometries may
be linked to size evolution. A better understanding of this relationship will help the evaluation of the constraint hypothesis
(Pelabon et al. 2013) and may also be crucial for understanding
the evolution of traits with other scaling relationships than the
power model, for example, threshold traits (e.g., Emlen 1996;
Moczek 1998, 2003; Emlen and Nijhout 2000). Following the
reasoning from Gould (1966a,b) and Pelabon et al. (2013), it may
be expected that larger morphs in polyphenic populations have a
shallower slope compared to smaller morphs. We are not aware
of any tests of this hypothesis.
CAVEATS IN STUDYING NARROW-SENSE

ALLOMETRY
How to best estimate allometric relations has been a subject of

much debate. Although some statisticians have viewed the fitting of allometric slopes merely as a descriptive exercise, it is
essential to understand that testing Huxleys hypothesis requires
the estimation of specific parameters from a mathematical model,
most saliently the narrow-sense allometric exponent. Reduced
major-axis regression and other nonparametric line-fitting methods are commonly used in studies of allometry, but these methods
simply do not estimate the narrow-sense allometric exponent, and
will often give wrong results if used for this purpose (Kelly and
Price 2004; Hansen and Bartoszek 2012). Reduced major axis
computes the slope as the ratio between the SDs of the variables.
Hence, changes in a reduced major-axis slope can result from
any change in the variation of either trait or body size, and therefore can not be taken as evidence for change in the narrow-sense
allometric exponent.
The errors that can result when interpreting reduced majoraxis slopes as estimates of narrow-sense allometric slopes are
illustrated by the study of Kelly et al. (2000), who investigated (among other things) whether differences in predator
regimes could affect the allometry between gonopodium length
(transformed anal fin) and body length in eight populations of
the Trinidadian guppy. Eight reduced major-axis regressions of
gonopodium length resulted in slopes ranging from 0.99 to 2.01,
and five of these were statistically significantly larger than 1 (Table S5). Negative allometry (slope < 1) is generally expected
for primary sexual traits (Eberhard et al. 1998, 2009; Bernstein
and Bernstein 2002) and these five significant regressions are,
according to the authors, the first examples of positive allometric
relationships between male genitalia and body size in a vertebrate
species. Our reanalysis of the data with ordinary least-squares
regression reveals that all eight regressions show negative allometry and three are statistically significantly less than unity (Table
S5). Hence, these results are consistent with the expected negative
allometric scaling of genital traits. Lupold et al. (2004) provide a
similar example in which a reduced major-axis slope of 2.09 is interpreted as falsifying negative allometric scaling of penis length
in the bat Nyctalus noctula, even though the ordinary least-squares
slope of 0.81 is consistent with the expected negative allometric
scaling.
Choosing a proper scale is essential when estimating allometric parameters as it determines what hypotheses are being tested.
Allometry sensu Huxley is about proportional differences in traits,
which is why fitting a linear regression on an arithmetic scale is
not estimating the relevant parameters in the allometric model.
However, whether one should fit the power model by nonlinear
regression on arithmetic scale or the linear model on log scale
is less obvious. Conceptually, these two approaches estimate the
881
same parameters, but the results can be very different (Zar 1968;
Smith 1980, 1984; Kerkhoff and Enquist 2009; Packard 2009,
2012; Packard et al. 2011). Fitting the model on an arithmetic
scale is justified if the residual deviations act additively on the
arithmetic scale while fitting a model on log-transformed data
is justified if the residual deviations act multiplicatively on the
arithmetic scale. It is not expected that parameters estimated on
a multiplicative (e.g., logarithmic) scale should minimize arithmetic deviations. The choice of scale should relate to a hypothesis
of whether multiplicative or additive processes generate the deviations from the model. The challenge is that observational errors
(the difference between the measured and the true value of the
entity) may cause additive deviations, whereas biological errors (the true biological deviations from the model; Riska 1991;
Hansen and Bartoszek 2012) are often multiplicative because biological phenomena like growth and metabolism are inherently
multiplicative (e.g., Gingerich 2000). Xiao et al. (2011) advocate
averaging between the two methods. In our opinion, this is hiding
and not solving the problem, and a solution should be based on
modeling and a principled argument as to what type of residual
deviation is expected. In most cases, linear regression on a logarithmic scale will be preferable as a first approximation, because
biological deviations are likely to be the dominant source of residual variation. Observational errors may also be multiplicative in
some cases, and if they are additive then their effects on the log
scale can be well approximated by use of mean-scaled arithmetic
variances, which can be incorporated into the regression analysis
as described in, for example, Hansen and Bartoszek (2012).
Conclusion
Eighty years have gone since Huxley (1932) suggested that common growth regulation was the cause of the commonly observed
pattern of a linear scaling relationship between morphological
traits and overall size on a loglog scale. Although early students of allometry interpreted this as a potential constraint on
phenotypic diversity, recent work has more or less dismissed the
constraint idea. In contrast, we have shown that the allometric
exponent may be difficult to change on short time scales for
traits that fits the model well, and may have biased the course of
trait adaptation. There is, however, good evidence that allometries
evolve on macroevolutionary time scales, and here they may be
less important as constraints.
ACKNOWLEDGMENTS
The authors thank R. H. Baker, K. Kawano, C. D. Kelly, H. F. Nijhout,
J. G. Swallow, A. Tobler, and G. S. Wilkinson for their helpfulness
and willingness to share their data with us. D. Houle and G. P. Wagner were helpful discussion partners at an early stage of this study and M.
Bjorklund, C. J. P. Firmat, . Holen, J. Merila, T. O. Svennungsen, and
two reviewers gave valuable comments on the manuscript. The work was
882
supported by grant 196434/V40 from the Norwegian Research Council

to CP at NTNU.
DATA ARCHIVING
The doi for our data is 10.5061/dryad.v460h.
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Associate Editor: P. David Polly
Supporting Information
Additional Supporting Information may be found in the online version of this article at the publishers website:
Figure S1. Graphical illustration of how variation in static allometric parameters produces trait variation across taxa.
Figure S2. Allometries for selection lines of male and female Manduca sexta reanalyzed from Tobler and Nijhout (2010).
Table S1. Studies reporting the multivariate generalization of allometry using principal component analysis in which the coefficients of the first principal
component (PCl) are used to estimate the allometric exponent.
Table S2. Studies reporting at least two homologous static allometries, but which did not match all our criteria for being part of the study.
Table S3. Studies reporting at least two homologous ontogenetic allometries, but which did not match all our criteria for being part of the study.
Table S4. Artificial selection studies on what they define as static allometry, but which we have excluded from our literature review.
Table S5. Static allometric relationships between log gonopodium length as a function of log body length in eight populations of the Trinidadian guppy
(Poecilia reticulata).
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O R I G I NA L A RT I C L E

ALLOMETRIC CONSTRAINTS AND THE

Received May 28, 2013

Adaptation, evolutionary constraint, microevolution, macroevolution, ontogenetic allometry, static allometry.

Most quantitative traits are highly evolvable (Houle 1992; Hansen

C 2013 The Society for the Study of Evolution.

Huxley (1924, 1932) showed that if two morphological traits

EVOLUTION MARCH 2014

of the traits. This model implies

where a = ln(Yo ) b ln(Xo ). Note that this allometric relation

where bo and ao describe the ontogenetic allometry. We use yo

EVOLUTION MARCH 2014

bs = Cov[ys ,xs ]/Var[xs ] = Cov[bo xs + ao ,xs ]/Var[xs ]

= E[bs ] + bbs,x E[xe ] + bas,x ,

= E[bo ] + bbo,x E[xo ] + bao,x ,

be = Cov[ye , xe ]/Var[xe ] = Cov[bs xe + as ,xe ]/Var[xe ]

Assuming a static allometry between trait size ys and body size

Ex [Var[y|x]] = Var[a|x] + Var[b]Var[x] + Cov[b, x]2

we present the relevant conditional variances (see supplementary

The trait variance in equation (8) and the conditional variances

procedure allows us to compare the influence of the different

Materials and Methods

EVOLUTION MARCH 2014

corrected for sampling error in the among-taxa slope and intercept

None of the studies we found in the literature reported all the

To assess the short-term evolvability of allometry, we searched the

We were only able to use 10 of 52 studies that reported static

EVOLUTION MARCH 2014

data on guppy populations from Kelly et al. (2000), we were able

2 pop. of 3 sp. of Drosophila1

Diopsidae (30 sp.)

Hind tibia (?)

0.87 (0.84 0.90)

0.56 (0.74 0.50)

Simmons and Tomkins (1996)

Hosken et al. (2005)

EVOLUTION MARCH 2014

EVOLUTION MARCH 2014

Standard body length

P. reticulata (21 pop.)

Mix 0.955, 0.000

Mix 0.753, 0.000

Vinyard and Ravosa (1998)

Vinyard and Ravosa (1998)

0.26 (0.48 0.10) Kinahan et al. (2008)

Jennions and Kelly (2002)

Kelly et al. (2000)

Kelly et al. (2000)

0.24 (0.31 0.15)

0.95 (0.96 0.95)

Anderson et al. (2012)

Anderson et al. (2012)

Tip of nose to base of tail.

Front of head to tip of elytron.

Front of head to tip of wings.

accelerator linguae; ENT = entoglossal process; HG = m. hyoglossus; TP = tongue pad.

EVOLUTION MARCH 2014

be = 1.17 0.10, R2 = 95.6%

Log body size (mm)

Log body size (mm)

be = 0.84 0.27, R2 = 62.2%

Log thorax widh (mm)

be = 0.87 0.15, R2 = 84.8%