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Large-Scale Diversification of Skull Shape in Domestic Dogs: Disparity and Modularity

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Abstract: The variation among domestic dog breeds offers a unique opportunity to study large-scale diversification by microevolutionary mechanisms. We use geometric morphometrics to quantify the diversity of skull shape in 106 breeds of domestic dog, in three wild canid species, and across the order Carnivora. The amount of shape variation among domestic dogs far exceeds that in wild species, and it is comparable to the disparity throughout the Carnivora. The greatest shape distances between dog breeds clearly surpass the maximum divergence between species in the Carnivora. Moreover, domestic dogs occupy a range of novel shapes outside the domain of wild carnivorans. The disparity among companion dogs substantially exceeds that of other classes of breeds, suggesting that relaxed functional demands facilitated diversification. Much of the diversity of dog skull shapes stems from variation between short and elongate skulls and from modularity of the face versus that of the neurocranium. These patterns of integration and modularity apply to variation among individuals and breeds, but they also apply to fluctuating asymmetry, indicating they have a shared developmental basis. These patterns of variation are also found for the wolf and across the Carnivora, suggesting that they existed before the domestication of dogs and are not a result of selective breeding.
vol. 175, no. 3 the american naturalist march 2010
Large-Scale Diversification of Skull Shape in Domestic
Dogs: Disparity and Modularity
Abby Grace Drake
*
and Christian Peter Klingenberg
Faculty of Life Sciences, University of Manchester, Michael Smith Building, Oxford Road, Manchester M13 9PT, United Kingdom
Submitted June 1, 2009; Accepted October 27, 2009; Electronically published January 22, 2010
abstract: The variation among domestic dog breeds offers a unique
opportunity to study large-scale diversification by microevolutionary
mechanisms. We use geometric morphometrics to quantify the di-
versity of skull shape in 106 breeds of domestic dog, in three wild
canid species, and across the order Carnivora. The amount of shape
variation among domestic dogs far exceeds that in wild species, and
it is comparable to the disparity throughout the Carnivora. The
greatest shape distances between dog breeds clearly surpass the max-
imum divergence between species in the Carnivora. Moreover, do-
mestic dogs occupy a range of novel shapes outside the domain of
wild carnivorans. The disparity among companion dogs substantially
exceeds that of other classes of breeds, suggesting that relaxed func-
tional demands facilitated diversification. Much of the diversity of
dog skull shapes stems from variation between short and elongate
skulls and from modularity of the face versus that of the neuro-
cranium. These patterns of integration and modularity apply to var-
iation among individuals and breeds, but they also apply to fluc-
tuating asymmetry, indicating they have a shared developmental
basis. These patterns of variation are also found for the wolf and
across the Carnivora, suggesting that they existed before the do-
mestication of dogs and are not a result of selective breeding.
Keywords: Canis familiaris, Carnivora, geometric morphometrics,
morphological integration, novelty, selection.
Introduction
Evolutionary change in morphological traits can be very
rapid, as has been documented by a range of studies (Rez-
nick et al. 1997; Hendry and Kinnison 1999; Huey et al.
2000; Grant and Grant 2006). Most of the changes found
in natural populations are at a relatively small scale, how-
ever, and therefore the question is raised as to whether
there are inherent limits to the amounts of change that
can occur by microevolutionary mechanisms or whether
special macroevolutionary processes are required to
* Corresponding author. Present address: Department of Biology, College of
the Holy Cross, P.O. Box B, Worcester, Massachusetts 01610; e-mail:
abbygracedrake@googlemail.com.
Am. Nat. 2010. Vol. 175, pp. 289–301. 2010 by The University ofChicago.
0003-0147/2010/17503-51313$15.00. All rights reserved.
DOI: 10.1086/650372
achieve large-scale change (Stanley 1998; Gould 2002).
Similarly, studies of adaptive radiation face difficulties in
extrapolating from microevolutionary data recorded in ex-
tant species to the larger scale of the entire radiation (e.g.,
Gavrilets and Losos 2009). These problems can be ad-
dressed directly in domesticated organisms, where sus-
tained selection by breeders has long been known to cause
large-scale phenotypic change (e.g., Darwin 1868).
Although large-scale variation has been indicated for
other domesticated species such as pigeons (Darwin 1868;
Helms and Brugmann 2007), and the morphological var-
iation of these species has been studied quantitatively (e.g.,
Johnston 1992), the variation among the breeds of the
domestic dog (Canis familiaris) is particularly suitable for
examining large morphological changes that originated ex-
clusively from microevolutionary processes (Darwin 1868;
Stockard 1941; Wayne 1986a, 1986b; Clutton-Brock 1995;
Coppinger and Coppinger 2001; Chase et al. 2002; Fondon
and Garner 2004; Parker et al. 2004; Lindblad-Toh et al.
2005; Wayne and Ostrander 2007). Many dog breeds were
established by selecting limited numbers of individuals for
breeding from larger populations (such as a regional pool
of farm dogs) or from one or more existing breeds; there-
fore, these breeds are equivalent to new lineages resulting
from founder events and hybridization (Parker et al. 2004;
Lindblad-Toh et al. 2005; Sampson and Binns 2006; Ra¨ber
2008). The reproductive separation and limited effective
population sizes of established breeds provide extensive
opportunity for divergence by genetic drift (Parker et al.
2004; Wayne and Ostrander 2007; Bjo¨rnerfeldt et al. 2008;
Calboli et al. 2008). Moreover, breeds are under selection
for a variety of morphological and behavioral traits (Cop-
pinger and Coppinger 2001; Parker et al. 2004; Ostrander
et al. 2006; Ra¨ber 2008). For instance, selection by breeders
for specific traits of the head has been shown to yield
sustained and substantial change in skull shape (Drake
and Klingenberg 2008). As a result, domestic dogs have a
vast spectrum of cranial variation (Darwin 1868; Stockard
1941; Nussbaumer 1982; Wayne 1986a; Young and Ban-
nasch 2006), which has clear functional consequences, for
290 The American Naturalist
instance, on bite forces (Ellis et al. 2009) or breathing
(Koch et al. 2003). In many ways, this situation corre-
sponds to an adaptive radiation (Schluter 2000; Gavrilets
and Losos 2009), but at the intraspecific level.
To what extent morphological variation is modular or
integrated throughout an entire structure is widely con-
sidered to be a key determinant of evolutionary flexibility
(Cheverud 1984; Wagner and Altenberg 1996; Klingenberg
2005). Because strong integration among parts may act as
a constraint if they are under opposing selection regimes,
modularity may enhance the capacity of morphological
traits to evolve. Moreover, the patterns of integration can
influence the direction of evolution and therefore may
have long-term consequences, for instance, if there are
multiple fitness peaks (Schluter 1996; Arthur 2001). In
turn, the patterns of morphological integration are also
expected to evolve under the influence of selection and,
as a consequence, to reflect functional associations among
traits (Cheverud 1984; Wagner and Altenberg 1996). Both
integration and modularity can vary in strength and are
not all-or-nothing phenomena (Klingenberg et al. 2003).
Integration and modularity can be studied by analyzing
the covariation among traits. Covariation of traits among
individuals reflects all differences, including evolutionary
divergence of taxa or breeds, whereas the covariation of
fluctuating asymmetry can reveal integration and modu-
larity of the developmental processes that are generating
the traits of interest (Klingenberg 2003, 2005).
Domestic dogs show abundant variation in the arrange-
ment of the nasomaxillary complex in relation to the neu-
rocranium (Stockard 1941; Nussbaumer 1982; Fondon
and Garner 2004; Drake and Klingenberg 2008), suggest-
ing that the two cranial complexes may be separate mod-
ules. Moreover, there is integrated shape variation along
a spectrum, from dolichocephalic breeds, which have slen-
der and elongate skulls, to brachycephalic breeds, which
have short and broad skull shapes (Wayne 1986a; Haworth
et al. 2001; Young and Bannasch 2006). Although parts of
the skull can be involved to different degrees, this type of
variation tends to have effects on most of the parts and
suggests integration throughout the whole skull. Similar
patterns of variation were also reported in domestic cats
(Ku¨nzel et al. 2003), in interspecific comparisons in Car-
nivora, and even in marsupials (Sears et al. 2007; Wroe
and Milne 2007), which raises the question as to whether
the process of domestication and divergence of breeds dis-
rupted ancestral constraints or exploited pre-existing pat-
terns of modular and integrated variation.
Here we use geometric morphometrics to characterize
and quantify shape variation in the skulls of domestic dogs,
and we compare this variation to variation in the three
most closely related wild species (Lindblad-Toh et al.
2005), the gray wolf (Canis lupus), the coyote (Canis la-
trans), and the golden jackal (Canis aureus). Because cra-
nial variation in domestic dogs is known to exceed that
in the family Canidae (Wayne 1986a), we use represen-
tatives from the entire order Carnivora as the basis for
comparison. In addition to quantifying the shape disparity
in these taxa, we also examine the patterns of integration
in the skull. Integration in the average shapes of the left
and right sides of the skull provides information about
variation among individuals in the samples, including the
differentiation of breeds or species. Cranial asymmetries,
however, arise from perturbations in the development of
each individual and can thus provide information about
the inherent tendency of skull development to produce
new morphological variation (Klingenberg 2005, 2008b).
By comparing integration in domestic dogs, in the wolf,
and across the Carnivora, we investigate whether domes-
tication changed the patterns of integration and modu-
larity, thereby disrupting ancestral evolutionary con-
straints, or whether the diversification of domestic dogs
used conserved patterns of cranial covariation.
Material and Methods
Data Set
Our study includes 677 adult dogs from 106 breeds (num-
bers of individuals per breed range from one to 62). The
sample of Carnivora includes one species each from 122
genera representing all major groups within the order
(Flynn et al. 2005), and care was taken to include the full
range of disparity. In addition, we examined samples of
adult gray wolves ( ), coyotes ( ), andnp288 np57
golden jackals ( ). Skulls were obtained from thenp49
following collections: the Smithsonian Institution’s Na-
tional Museum of Natural History (Washington, DC); the
private collection of Bonnie Dazell; the University of
Alaska Museum in Fairbanks, Alaska; the Museum of Ver-
tebrate Zoology at the University of California in Berkeley,
California; the Natural History Museum (London); the
Natural History Museum in Bern, Switzerland; the Powell-
Cotton Museum (Birchington, United Kingdom); and the
Oxford University Museum of Natural History (Oxford,
United Kingdom).
A set of 50 landmarks (12 median landmarks and 19
pairs on the left and right sides; fig. 1; table 1) was digitized
in three dimensions on the dorsal and the ventral aspects
of each skull using a MicroScribe digitizer. The landmarks
of the dorsal and the ventral aspects were combined by a
least squares fit (translation and rotation only) using four
landmarks that were digitized from both the dorsal and
the ventral views. Every skull was digitized twice.
Diversification of Skull Shape in Dogs 291
Figure 1: Landmarks on the dorsal and ventral sides of the skull that
were digitized (for anatomical definitions, see table 1). The dashed circles
indicate the hypothesis of modularity; the landmarks inside these circles
belong to the neurocranial module, whereas the landmarks outside the
circles are included in the facial module.
Shape Analysis
We quantify shape variation in the skulls of dogs by using
the methods of geometric morphometrics as implemented
in the MorphoJ software (Klingenberg 2008a). Shape var-
iation was extracted from the coordinate data by a full
Procrustes fit and projection to the shape-tangent space
(Dryden and Mardia 1998), using a procedure that takes
into account the object symmetry of the skull (Klingenberg
et al. 2002). An initial Procrustes ANOVA (Klingenberg et
al. 2002) confirmed that the Procrustes mean squares for
individual variation and fluctuating asymmetry substan-
tially exceeded measurement error, such that measurement
error is negligible (particularly for the analyses of variation
among individuals). For the remaining analyses, we av-
eraged the shape data from the replicate measurements of
each specimen. To explore the shape variation in the total
data set, we used a multivariate ordination of skull shapes
by a principal component (PC) analysis based on the co-
variance matrix of the symmetric component of shape
variation (Klingenberg et al. 2002). Visualizations of
shapes at the extremes of the PC axes were performed by
warping the scanned surface of a wolf skull, using the
Landmark software (Wiley et al. 2005).
Comparisons of Disparity
As a direct measure of the differences in shape, we computed
Procrustes distances between all possible pairs of specimens
in the dog sample and in the carnivoran sample. Procrustes
distances between specimens were computed as Euclidean
distances in tangent space (Dryden and Mardia 1998). Even
the greatest pairwise distances between specimens were
within the range of distances where the tangent-space ap-
proximation performs well (Marcus et al. 2000).
Two measures of shape disparity were computed. The
first is the Procrustes variance of observations in each
group, which is the mean squared Procrustes distance of
each specimen or breed average from the mean shape of
the respective group or, equivalently, the sumof the sample
variances of all Procrustes coordinates (Klingenberg and
McIntyre 1998; Zelditch et al. 2003). Procrustes variance
quantifies the average dispersion of data points around the
mean shape. The second measure is the volume of the
convex hull (de Berg et al. 2000) enclosing the data points
of each group, which quantifies the portion of shape space
occupied by the group. This is a measure of the degree of
difference among opposite extremes in each group, and
therefore it does not consider observations located near
the center of the scatter of data points. Convex hulls were
computed from the first three PCs because they contained
most of the variation in the sample and because com-
putation of higher-dimensional volumes presented com-
putational difficulties (dimensions with small amounts of
variation produce volumes near 0 for all samples, which
led to problems with numerical precision). The statistical
significance for pairwise comparisons of samples was es-
tablished with permutation tests (Good 2000) that sim-
ulated the null hypothesis of equal dispersion within
groups by randomly exchanging the deviations of data
points from the respective sample mean.
Allometry is a major factor in the diversification of dogs
(e.g., Wayne 1986a). To correct for the effects of allometry
on shape disparity, we computed the same disparity mea-
sures for the residuals from pooled within-group regres-
sion of shape on size. Because of the large amount of
variation in and the sample size of the dogs, this common
estimate of allometry is likely to be a better fit for dogs
than for the other groups in this study. It is therefore
expected to eliminate the allometric component of shape
variation more effectively from dogs than from the other
groups and, thus, to reduce the total shape disparity for
the dogs to a greater degree than for the other samples.
Analyses of disparity were conducted to compare dogs,
Table 1 : Osteometric landmarks collected on each skull, and their definitions
Landmark Definition
1 Midline point on the premaxilla at the inferior tip of the bony septum between the upper central incisors (F)
2 Premaxillary-maxillary suture, anterior, left side (F)
3 Premaxillary-maxillary suture, anterior, right side (F)
4 Nasal, anterior tip, left side (F)
5 Nasal, anterior tip, right side (F)
6 Nasale, nasal, anterior, midline (F)
7 Premaxillary-maxillary suture, posterior end in dorsal view, left side (F)
8 Premaxillary-maxillary suture, posterior end in dorsal view, right side (F)
9 Frontal-maxillary-nasal suture, left side (F)
10 Frontal-maxillary-nasal suture, right side (F)
11 Nasion, nasal-frontal suture, midline (F)
12 Frontal-maxillary suture, posterior, left side (F)
13 Frontal-maxillary suture, posterior, right side (F)
14 Frontal-parietal-sphenoid suture, left side (N)
15 Bregma, frontal-parietal suture, midline (N)
16 Frontal-parietal-sphenoid suture, right side (N)
17 Lambda, parietal-occipital suture, midline (N)
18 Asterion, posterior at occipital-parietal-temporal suture, left side (N)
19 Asterion, posterior at occipital-parietal-temporal suture, right side (N)
20 Opsithion, dorsal lip of foramen magnum, midline (N)
21 Occipital condyle (widest point of foramen magnum), left side (N)
22 Occipital condyle (widest point of foramen magnum), right side (N)
23 Basion, ventral lip of foramen magnum, midline (N)
24 Zygo-maxillare inferior, left side (F)
25 Squamosal-jugal suture, anterior projection of zygomatic process of temporal bone, left side (F)
26 Optic canal (ventral lip), left side (N)
27 Squamosal-jugal suture, posterior projection of jugal, ventral, left side (F)
28 External auditory meatus, posterior, left side (N)
29 Zygo-maxillare inferior, right side (F)
30 Squamosal-jugal suture, anterior projection of zygomatic process of temporal bone, right side (F)
31 Optic canal (ventral lip), right side (N)
32 Squamosal-jugal suture, posterior projection of jugal, ventral, right side (F)
33 External auditory meatus, posterior, right side (N)
34 Premaxillary-maxillary suture, lateral end in ventral view, left side (F)
35 Premaxillary-maxillary suture, lateral end in ventral view, right side (F)
36 Premaxillary-maxillary suture, posterior at midline (F)
37 Maxillary-palatine suture, anterior at midline (F)
38 Palatine, posterior at midline (F)
39 Presphenoid, anterior tip at midline (F)
40 Palatine-pterygoid suture posterior, right side (N)
41 Palatine-pterygoid suture posterior, left side (N)
42 Presphenoid-basisphenoid suture, midline (N)
43 Tympanooccipital fissure, anterior lip, right side (N)
44 Tympanooccipital fissure, anterior lip, left side (N)
45 Canine (posterior buccal corner), right side (F)
46 Premolar 3 (posterior buccal corner), right side (F)
47 Premolar 4 (posterior buccal corner), right side (F)
48 Canine (posterior buccal corner), left side (F)
49 Premolar 3 (posterior buccal corner), left side (F)
50 Premolar 4 (posterior buccal corner), left side (F)
Note: The letters F and N indicate whether a landmark belongs to the face or to the neurocranium, respectively.
Diversification of Skull Shape in Dogs 293
Figure 2: Hypothesis of modularity and adjacency graph for the land-
marks. The filled circles denote the landmarks of the facial module; the
open circles denote the landmarks of the neurocranial module (see also
fig. 1 and table 1). The lines connect landmarks that are deemed to be
anatomically adjacent to one other, and they are used to define spatial
contiguity of partitions of landmarks (Klingenberg 2009). A subset of
landmarks is spatially contiguous if all of its landmarks are connected
by the edges of the adjacency graph. A partition of the configuration is
contiguous if all subsets of landmarks are contiguous themselves (Klin-
genberg 2009).
the three wild canid species, and the Carnivora (see “Data
Set” for sample sizes). Moreover, we also compared the
disparity of dogs according to the following functional
groups (as defined by the United Kennel Club): Com-
panion Dog ( , 20 breeds), Guardian Dog (np138 np
, 23 breeds), Gun Dog ( , nine breeds), Herding246 np42
Dog ( , 10 breeds), Northern Breed ( , 12np44 np51
breeds comprising various sledge, hunting, and guard
dogs), Scenthound ( , six breeds), Sighthound andnp19
Pariah ( , 13 breeds, including the dingo and thenp68
New Guinea singing dog), and Terrier ( , 13 breeds).np69
Integration and Modularity
Because differences in the arrangement of the snout rel-
ative to the braincase—for instance, the variation between
klinorhynchy and airorhynchy (Nussbaumer 1982; Fon-
don and Garner 2004)—are an important component of
cranial variation in domestic dogs, we examine the hy-
pothesis that the face and the neurocranium are separate
modules (fig. 1; table 1). Modules are regions that are
integrated internally but that are relatively independent of
each other. The hypothesis of modularity therefore implies
that the covariation between the landmarks of the face and
those of the neurocranium should be weaker than the
covariation for other partitions of the landmarks into sub-
sets of the corresponding sizes (Klingenberg et al. 2003;
Klingenberg 2008b, 2009).
To assess the strength of modularity, we compared the
strength of covariation between subsets of landmarks for
the hypothesized modules with that of alternative partitions
of the total set of landmarks into subsets (Klingenberg
2009). To quantify the strength of covariation between sub-
sets of landmarks, we used the RV coefficient (Escoufier
1973), which can be interpreted as a multivariate general-
ization of the bivariate R
2
value (for detailed explanations,
see Klingenberg 2009; Laffont et al. 2009). The RV coeffi-
cient for the subdivision of landmarks into facial and neu-
rocranial regions was compared with the distribution of RV
coefficients for randomly generated subdivisions. Random
subdivisions were formed from the paired landmarks of one
side and the median landmarks such that the numbers of
landmarks matched those in the facial and neurocranial
regions (Klingenberg 2009). We limited this comparison to
those subdivisions where both subsets of landmarks were
spatially contiguous (i.e., connected by the edges of a graph
indicating landmarks that are anatomically adjacent; fig. 2;
for details, see Klingenberg 2009).
For the analysis of modularity in the symmetric com-
ponent of shape variation in the Carnivora, we used in-
dependent contrasts (Felsenstein 1985) to take into ac-
count the phylogenetic structure of the data, using the
supertree of Bininda-Emonds et al. (2007). This adjust-
ment was not required for the asymmetric component,
because the left-right differences are computed within in-
dividuals and are therefore independent with respect to
phylogeny.
For quantifying overall similarity of covariance matrices,
we computed matrix correlations and the associated per-
mutation tests, using procedures adapted for geometric
morphometrics and object symmetry (Klingenberg and
McIntyre 1998; Klingenberg et al. 2002; Klingenberg
2008a).
Results
Patterns of Morphological Diversification and Novelty
The first three PCs account for 71.8% of the total shape
variation, and therefore, they provide a reasonable ap-
proximation of the total variation (no other PC accounts
for more than 5%). PC1 primarily contrasts brachyce-
phalic and dolichocephalic skulls; PC2 opposes elongate
skulls, where the braincase is aligned posterior to the muz-
zle, to broader and higher skulls, where the braincase is
raised above the rostrum; and, finally, PC3 sets skulls with
enlarged faces and broad and high rostra against others
with relatively larger braincases and muzzles that taper
markedly toward the front (fig. 3D). The scatter of PC
scores (fig. 3A–3C) shows that the amount of variation is
much greater in dogs than it is in wolves, coyotes, and
golden jackals and that the dispersion of data points for
dogs is comparable to that across the Carnivora.
294 The American Naturalist
Figure 3: Principal component (PC) analysis for skull shape in the complete data set. A–C, Plots of the PC scores. D, Shape changes associated
with the PC axes. For each PC, the shapes corresponding to the observed extremes in the positive and negative directions are shown as a warped
surface of a wolf skull (Wiley et al. 2005).
Closer inspection of the PC plots for shape variation
(fig. 3) clearly shows that domestic dogs have only limited
overlap with the other carnivores (see particularly fig. 3C).
The samples of wolves, coyotes, and golden jackals are
located in the region of the intersection between dogs and
the other carnivores. It is clear from this analysis not only
that domestic dogs occupy a large region of shape space
that is outside of the range of the ancestral species, the
wolf, and the other members of the family Canidae (Wayne
1986a) but also that much of the shape variation in do-
mestic dogs is novel relative to the range of skull shapes
in the order Carnivora as a whole.
Quantifying Disparity
The greatest Procrustes distance between specimens in the
dog sample is 0.477 (between a Collie and a Pekingese),
which exceeds the distance of 0.424 between the most
divergent specimens in the Carnivora sample (walrus
Odobenus rosmarus and falanouc Eupleres goudotii).
Among domestic dogs, pairwise distances greater than 0.45
involve other pairings of breeds (Borzoi-Pekingese, Collie–
Japanese Chin, Borzoi–Japanese Chin, Borzoi-Pug, Aire-
dale Terrier–Pekingese, Scottish Deerhound–Pekingese,
Collie-Pug). All of these contrasts are between dolicho-
cephalic and brachycephalic breeds. In the sample of the
Carnivora, all other Procrustes distances greater than 0.4
also involve the walrus, in combination with the mountain
coati (Nasuella olivacea, 0.405), the Malagasy civet (Fossa
fossana, 0.404), Owston’s palm civet (Chrotogale owstoni,
0.404), and the servaline genet (Genetta servalina, 0.401).
To compare the amounts of shape variation in the entire
sample of domestic dogs, the three wild species, and the
Carnivora, we used two measures of disparity that capture
Diversification of Skull Shape in Dogs 295
Figure 4: Skull shape disparity in the different samples. A, Total shape
disparity, quantified by Procrustes variance. B, Total shape disparity,
quantified by the volumes of the convex hulls for the first three dimen-
sions. C, Shape disparity corrected for the effects of size, quantified by
Procrustes variance. D, Shape disparity corrected for the effects of size,
quantified by the volumes of convex hulls for the first three dimensions.
Figure 5: Skull shape disparity in the different groups of dogs, according
to the breed classification of the United Kennel Club. A, Total shape
disparity, quantified by Procrustes variance. B, Total shape disparity,
quantified by the volumes of the convex hulls for the first three dimen-
sions. C, Shape disparity corrected for the effects of size, quantified by
Procrustes variance. D, Shape disparity corrected for the effects of size,
quantified by the volumes of convex hulls for the first three dimensions.
The last column in each panel (“All non-Companion”) includes all groups
other than Companion Dog. The size correction for Cand Dwas com-
puted for dogs separately, and therefore it differs from the one used in
figure 4; Aand Bare directly comparable to figure 4Aand 4B, respectively.
different aspects of shape diversification within samples:
Procrustes variance and the volume of the convex hull
enclosing the data points. Both measures of shape disparity
give similar results (fig. 4A,4B). The variation among
average shapes of dog breeds is less than that among in-
dividual dogs (significantly so for the volume of convex
hulls, ; nonsignificantly so for Procrustes vari-Pp.0004
ance, ). The disparity within dogs, both amongPp.12
individuals and among breed means, is consistently much
greater than the disparity within wolves, coyotes, and
golden jackals (for both measures of disparity; all P
). Finally, the variation among individual dogs is of a.002
magnitude similar to that in the carnivore sample (sig-
nificant difference for Procrustes variance, ; noPp.0028
significant difference for the volume of convex hulls,
). The fact that this match between dogs and car-Pp.99
nivores is closer for the volumes of the convex hulls (fig.
4B) than for the Procrustes variances (fig. 4A) reflects the
fact that the disparity among dogs is dominated particu-
larly by some breeds that are highly divergent, whereas
many breeds retain a skull shape that is closer to the an-
cestral shape (fig. 3).
Because allometry is a major factor in the diversification
of dog breeds, we repeated these comparisons with data
that were corrected for the effects of allometry. The esti-
mates of disparity based on the residuals from allometric
regression (fig. 4C,4D) are similar to the uncorrected
values, with substantially greater disparity for domestic
dogs than for the wild canid species. Because the estimate
of allometry is dominated by domestic dogs, the amounts
of variation are reduced more for the dogs than for the
other groups (fig. 4C,4D; the slight increase for the car-
nivore sample is due to differences in allometries). Nev-
ertheless, this analysis shows conclusively that the dispro-
portionate amount of shape variation in domestic dogs is
not simply due to allometric scaling.
Among the groups of dog breeds as defined by the
United Kennel Club, the Companion Dog group has a far
greater disparity than do any of the other groups, regard-
less of which of the two disparity measures is used or
whether a correction for allometric effects is made (fig. 5;
all ). If the Companion Dog group is contrastedP.0001
to all other groups jointly (rightmost columns in the panels
of fig. 5), it still has a much greater Procrustes variance
( ), but it has a comparable volume of the convexP!.0001
hull ( and .82 for analyses without and with thePp.99
correction for allometric effects, respectively). The differ-
ence in the results reflects the manner in which the two
measures of disparity consider the average versus the ex-
treme deviations from the shape averages in the groups
under comparison.
296 The American Naturalist
Figure 6: Analysis of modularity in the skull. Graphs show the RV
coefficients (interpreted as multivariate generalizations of the bivariate
R
2
values; Escoufier 1973) for the subdivision of landmarks into facial
and neurocranial regions (arrows) and the distribution of RV coefficients
for 10,000 alternative partitions of landmarks into anatomically contig-
uous subsets (histograms). A, Domestic dogs, symmetric component of
variation. This includes the shape variation among breeds. B, Domestic
dogs, asymmetric component. This is the component of fluctuating asym-
metry, and it provides a measure of the tendency of cranial development
to produce new variation. C, Wolves, symmetric component of variation.
D, Wolves, asymmetric component. E, Carnivora, independent contrasts
(Felsenstein 1985) for the symmetric component of variation. F, Car-
nivora, asymmetric component.
Integration and Modularity of the Skull
In the sample of domestic dogs, the RV coefficient between
facial and neurocranial landmarks is 0.87 for the sym-
metric component of variation, which indicates a very
strong association. This value shows the tight integration
of the entire skull in dogs (PC1, which represents a contrast
between dolichocephalic and brachycephalic breeds, alone
accounts for more than 63% of the symmetric variance in
the sample). Nevertheless, the RV coefficient between the
facial and neurocranial subsets is lower than those for most
other subdivisions of the landmarks ( ; fig. 6A).Pp.0475
Analyses with a correction for allometric variation yield
very similar results. Overall, therefore, the face and the
neurocranium possess a degree of modular separation de-
spite the strong integration, particularly in the differences
between breeds (e.g., breeds with short skulls vs. those
with long skulls).
For asymmetry in dogs, integration is generally lower
than it is for the symmetric component (fig. 6B), and the
RV coefficient between facial and neurocranial regions is
0.32. This RV coefficient is lower than those for most
alternative partitions ( ). The matrix correlationPp.0052
between the covariance matrices for the symmetric and
the asymmetric components of variation in dogs is 0.20
( ), indicating a weak but statistically discerniblePp.044
relationship between the diversification of skull shapes
across breeds and the intrinsic pattern of cranial variation.
Integration in the symmetric component of shape var-
iation in the wolf is substantially weaker than it is for the
domestic dogs (fig. 6C). The RV coefficient between facial
and neurocranial landmarks is 0.32, which is lower than
the RV coefficients for most alternative partitions (Pp
). For asymmetry in wolves, the RV coefficient for.0538
the subdivision into facial and neurocranial sets is 0.21,
and only 26 of 10,000 random subdivisions yield a lower
covariation. The range of RV coefficients is fairly limited
for both symmetric and asymmetric components (fig. 6C,
6D), because all partitions have a similar, low-to-moderate
covariation. Whereas this result is consistent with the hy-
pothesis of facial and neurocranial modules, the limited
range of RV coefficients indicates a fairly weak modularity.
The matrix correlation between the covariance matrices
for the symmetric and asymmetric components of varia-
tion in the wolf sample is 0.63 ( ). The asymmetricP!.0001
components of the dog and the wolf samples have a matrix
correlation of 0.77 ( ) and are thus quite similar,P!.0001
suggesting shared patterns of developmental variation in
wolves and dogs. The patterns of variation in the sym-
metric component are less similar (matrix correlation:
0.47; ).P!.0001
In the analysis of the symmetric component of shape
variation in the Carnivora, the RV coefficient for the sub-
division into facial and neurocranial sets is 0.44, and it is
less than the values for most random partitions (Pp
; fig. 6E). For fluctuating asymmetry in the Carnivora,.0293
the RV coefficient between the hypothesized modules is
0.29, which is lower than the RV coefficients for most
random partitions ( ; fig. 6F). These results arePp.0231
consistent with the hypothesis of modularity. The patterns
of variation of the symmetric and asymmetric components
are moderately similar (matrix correlation: 0.45; Pp
). The correspondence between the asymmetric com-.0016
ponent in the Carnivora and those in dogs and wolves is
considerably better (matrix correlation: 0.73 and 0.72, re-
spectively; both ). Moreover, there is a significantP!.0001
similarity between the covariance matrix of independent
contrasts in the Carnivora and that for the symmetric
Diversification of Skull Shape in Dogs 297
component of variation in domestic dogs (matrix corre-
lation: 0.54; ), indicating that the patterns of di-P!.0001
versification in domestic dogs are moderately similar to
those in the Carnivora.
Discussion
The breeds of domestic dogs have long been known for
their great variety of skull shapes (Darwin 1868; Stockard
1941; Nussbaumer 1982; Wayne 1986a; Clutton-Brock
1995; Young and Bannasch 2006). Our analyses show that
the variation of cranial shape in dogs is comparable to
that across the entire order Carnivora (figs. 3, 4) and that
differences in skull shape between extreme dog breeds even
exceed the maximal distances we found among the species
of Carnivora.
This massive disparity among dogs has evolved in a few
hundred to several thousand years (Clutton-Brock 1995;
Lindblad-Toh et al. 2005), a very brief time span by com-
parison with the evolution of natural clades with com-
parable disparity, which raises the question as to whether
the diversification in dogs can be representative of large-
scale evolution in nature. Studies in natural populations
have documented rapid change due to selection (Reznick
et al. 1997; Hendry and Kinnison 1999; Huey et al. 2000)
and, in some cases, also hybridization (Grant and Grant
2002), but the changes observed in these populations were
much smaller than the differences among dog breeds. At
a larger scale, bursts of relatively rapid increase in disparity
have been inferred for clades of species (e.g., Harmon et
al. 2003; Ricklefs 2004), and speciation itself may be a
factor in this process (Ricklefs 2004; Mattila and Bokma
2008). Because dogs are a single species, however, with
separation of breeds maintained only by human interven-
tion, it is not speciation per se that is the driving force
producing morphological disparity, although population
bottlenecks and founder effects during establishment of
breeds might cause genetic conditions similar to those in
new species or island populations (Meffert 2006; Millien
2006; Losos and Ricklefs 2009). As a consequence of these
effects, nonsynonymous mutations have accumulated in
the dog genome (Cruz et al. 2008), which may facilitate
morphological divergence. Some of the divergence be-
tween dog breeds has been linked to single mutational
steps with large effects (Sutter et al. 2007; Parker et al.
2009), but there are also reports of mechanisms producing
incremental change in dog breeds as well as among car-
nivoran species (Fondon and Garner 2004; Sears et al.
2007). There is little information on the dynamics of
change in dog breeds, but a detailed study of the historical
change of skull shape in St. Bernard dogs found that the
features that were described as desirable in the breed stan-
dard gradually became more accentuated (Drake and Klin-
genberg 2008). Overall, it appears that the processes of
morphological diversification in dog breeds are broadly
comparable to those in natural lineages. Dogs are therefore
an excellent model system for the study of evolutionary
processes, including adaptive radiation and the origin of
large-scale morphological disparity.
By comparison, there is only little quantitative infor-
mation about the degree of variation in other domesticated
animals. Although cranial variation in domestic cats is
considerable (Ku¨nzel et al. 2003), it is not clear whether
it is comparable to the variation across the family Felidae
(Christiansen 2008). This apparently smaller scale of var-
iation may reflect the fact that genetic distance among cat
breeds tends to be clearly less than that among dog breeds
(Menotti-Raymond et al. 2007). For domestic pigeons,
widely different cranial shapes have been reported (Helms
and Brugmann 2007), but no quantitative studies of cra-
nial variation have been published. Divergence of skeletal
traits among pigeon breeds is much greater than the dif-
ferences between rock pigeons (Columba livia) and feral
pigeon populations (Johnston 1992). Unfortunately, the
differences in measurements and methods make it difficult
to compare across these studies, and none of these studies
includes more than a small number of breeds. Moreover,
except for those of domestic dogs (this article; Wayne
1986a, 1986b), no study directly compares the morpho-
logical variation in a domesticated species with that in the
larger clade to which it belongs.
In addition to the great amount of variation in domestic
dogs, a striking result is that most of the range of skull
shape variation is outside the range of that for the Car-
nivora (fig. 3C). Even if allowance is made for intraspecific
variation, for which the range of variation in the three
wild canid species can serve as a basis of comparison, a
substantial part of the domain of variation for the dogs is
still outside the zone of overlap (fig. 3). These shapes
represent novel arrangements of the skull in domestic dogs
that are not found in other carnivorans.
These novel skull shapes, as well as the disparity in dog
breeds and in wild species (figs. 4, 5), suggest that diver-
sification of dog skull shapes is due, at least in part, to the
radical change of the selective regime, as dog breeds were
derived from wolves through domestication and the later
establishment of modern breeds (Lindblad-Toh et al. 2005;
Pollinger et al. 2005; Bjo¨rnerfeldt et al. 2006; Wayne and
Ostrander 2007). Domestication relaxed selective pressures
in contexts such as foraging, and the requirement to process
hard or tough foods was reduced. This new selective regime
may tolerate changes in cranial morphology even if they
affect aspects of performance such as bite force (Ellis et al.
2009) or breathing, which is impeded in brachycephalic dogs
(Koch et al. 2003; similar problems for cats are discussed
in Ku¨nzel et al. 2003). One would expect the functional
298 The American Naturalist
demands on skull shape to be most permissive for the Com-
panion Dog group, intermediate for breeds selected to per-
form work (such as hunting, herding, or guarding), and
most stringent for the wild species. In agreement with this
expectation, the greatest amounts of disparity are found in
the Companion Dog group, fewer are found in the other
groups of breeds, and the smallest amounts are found in
the three wild species (figs. 4, 5). Furthermore, this argu-
ment predicts that feral dogs should be less variable than
pet dogs and other domestic breeds. This is difficult to
assess, because only a few specimens were available: three
dingos and two New Guinea singing dogs, which are ancient
populations derived from feral dogs (Savolainen et al. 2004).
The Sighthound and Pariah group, which contains both
breeds, is not unusually variable by comparison with the
other functional groups. Stronger support for such an ar-
gument was found for skeletal measurements in pigeons,
where feral pigeons resemble wild rock pigeons, whereas
domestic pigeon breeds are much more different from each
other, suggesting that feral pigeons were under selection for
trait values similar to those of their wild ancestor but that
domestic pigeons were not (Johnston 1992; Sol 2008). No
comparable evidence appears to be available for cranial
shape in pigeons or for any skeletal structure in other feral
animals.
Since the establishment of modern dog breeds, artificial
selection for behaviors or appearance desired by breeders
specifically favored divergence (Kemp et al. 2005; Drake
and Klingenberg 2008). Direct selection for head shape is
expected to be strongest for pet dogs, which is consistent
with the large disparity of the Companion Dog group (fig.
5). In addition, the process of domestication itself may
bring about a variety of changes due to selection for tame-
ness (Trut et al. 2004) and due to changes in the selective
regime (Bjo¨rnerfeldt et al. 2006) and direct mechanical
influence on skull growth (O’Regan and Kitchener 2005).
In addition to selection, bottleneck events in the estab-
lishment of new breeds and subsequent inbreeding (Lind-
blad-Toh et al. 2005; Bjo¨rnerfeldt et al. 2008; Calboli et
al. 2008) may have further enhanced diversification
through the fixation of mutations that affect cranial shape
(Haworth et al. 2001; Neff et al. 2004; Pollinger et al. 2005;
Bjo¨rnerfeldt et al. 2006; Cruz et al. 2008).
Morphological Integration and Modularity
The large-scale divergence of dog breeds in response to
selection by breeders raises the question about the devel-
opmental basis of variation. Was there any particular pre-
disposition in the developmental system of the skull that
facilitated this diversification? Or, did the processes of do-
mestication and artificial selection themselves produce a
reorganization of the patterns of integration and modu-
larity? If genetic and developmental modularity are molded
by functional associations of traits and selection (Cheverud
1984; Wagner and Altenberg 1996), a drastic change of the
selective regime such as domestication may be expected
to affect the integration and modularity of the skull.
The results of the comparisons of RV coefficients for
dogs (fig. 4) are generally consistent with the hypothesis
that the face and the neurocranium are morphological
modules, as the subdivision into face and neurocranium
produces RV coefficients that are lower than those for most
alternative partitions. Moreover, the relatively limited
range of RV coefficients in each of the analyses indicates
that modularity is relatively weak, that is, that the co-
variation within modules is not much stronger than the
covariation between modules (Klingenberg et al. 2003;
Klingenberg 2009). The high RV coefficients, particularly
for the symmetric component in dogs, also reflect the large
proportion of variation that is integrated throughout the
skull, such as the spectrum between brachycephalic and
dolichocephalic skull shapes (e.g., PC1 in fig. 3; Stockard
1941; Wayne 1986a; Haworth et al. 2001; Young and Ban-
nasch 2006). For fluctuating asymmetry, which originates
from random variation produced by the developmental
system, integration is weaker and the range of RV coef-
ficients tends to be greater than that for the symmetric
component of variation. Particularly for the dogs, the
modular structure of the skull is therefore more apparent
for this spontaneous developmental variation than it is for
the symmetric component of shape variation, which in-
cludes the evolved differences among breeds. A lower de-
gree of integration of asymmetry than for the among-
individual variation has also been found in similar analyses
for rodents and fly wings (e.g., Klingenberg 2009; Laffont
et al. 2009) and may therefore be a widespread phenom-
enon.
The patterns of developmental integration, as charac-
terized by the covariance matrices for fluctuating asym-
metry (Klingenberg 2003, 2008b), are similar in domestic
dogs, in the wolf, and across the order Carnivora (all ma-
trix correlations 10.7 and ). Accordingly, there isP!.0001
no indication that domestication changed the way in which
new morphological variation is generated. On the contrary,
the results are consistent with the possibility that the an-
cestral developmental system was mostly conserved
throughout the evolution of the carnivores and the do-
mestication of dogs, despite the long evolutionary time
spans and the large scale of morphological diversification.
We are not aware of similar comparisons of the patterns
of integration for fluctuating asymmetry, except at the
intraspecific level (Debat et al. 2006, 2008, 2009). At the
level of intraspecific variation, where factors other than
development may also influence the observed patterns, a
comparison across the order Carnivora found that patterns
Diversification of Skull Shape in Dogs 299
of cranial integration within species are mostly similar
(Goswami 2006b) and that there are some shared patterns
of integration even across therian mammals (Goswami
2006a; Porto et al. 2009). Despite this large-scale conser-
vation, patterns of integration can vary at small taxonomic
scales (Steppan 1997; Mitteroecker and Bookstein 2008;
Jamniczky and Hallgrı´msson 2009; Kulemeyer et al. 2009).
The matrix correlation between the symmetric and the
asymmetric components of shape variation for the wolf
(0.63) is stronger than the low-to-moderate matrix cor-
relations for domestic dogs (0.20) or Carnivora (0.45). For
both dogs and Carnivora, the symmetric component of
variation is dominated by the evolved differences among
breeds or species, whereas in the wolf it is mainly within-
population variation. The relatively high matrix correla-
tion between symmetric and asymmetric components of
the wolf suggests that new variation generated by the de-
velopmental system is incorporated into the pool of
within-population variation in a fairly equitable manner.
In contrast, the lower matrix correlations for the Carnivora
and for dogs suggest that patterns of diversification among
taxa or breeds differ substantially from the patterns of
variation spontaneously produced by the developmental
system because phylogenetic divergence of Carnivora and
artificial selection by dog breeders disproportionately fa-
vored some directions in shape space over others. These
matrix correlations correspond to the mixed results found
in similar comparisons between patterns of symmetric var-
iation and fluctuating asymmetry for other animals (e.g.,
Klingenberg and McIntyre 1998; Debat et al. 2000; Klin-
genberg et al. 2002; Willmore et al. 2005; Breuker et al.
2006), with the difference being that all of those studies
were based on intrapopulation variation.
The diversification of both the Carnivora and the do-
mestic dogs relies on a combination of the input of new
variation, which retains a mostly conserved pattern, and
selection that can favor particular aspects of shape. As a
result, diversification in skull shape is responsive to specific
selective inputs, but it follows general patterns concerning
the relative length of the skull (brachycephalic vs. doli-
chocephalic skulls) and the relative arrangement of the
facial and neurocranial parts of the skull (airorhynchy vs.
klinorhynchy, but possibly other rearrangements as well).
Investigating the contributions of the developmental sys-
tem and specific selective events, in dogs and other do-
mesticated species as well as in naturally evolved clades,
will be a promising approach for understanding the pro-
cesses responsible for morphological diversification.
Acknowledgments
We are grateful to the curators of the various collections
(see “Material and Methods”) for access to skulls in their
care. We thank E. Sherratt for crucial technical help with
visualizing three-dimensional surfaces and M. Nussbau-
mer and two anonymous reviewers for helpful comments
on drafts of this article. This research was supported by
grants from the Leverhulme Trust and the Royal Society.
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Associate Editor: Stephen B. Heard
Editor: Mark A. McPeek
... We explore the issue of whether goldfish diversity mirrors its evolutionary group's morphological disparity by quantifying and comparing overall phenotype within the clade, leading to also examine how the selection for ornamental traits has produced morphological innovations in diverse anatomical modules. This issue has been explored in studies of the skulls of pigeons (Young et al., 2017) and dogs (Drake & Klingenberg, 2010), providing a comparative context for assessing the impact of the domestication process. ...
... For analyses based on 3D geometric morphometrics, we used: a phylogenetically aligned component analysis (PaCA; Collyer & Adams, 2021) to integrate phylogeny into the analysis of the neurocranial complex shape including more than two species; a classical principal component analysis (PCA) to analyze the shape of the neurocranial complex between goldfish and C. gibelio; and a regularized consensus PCA (RCPCA) to investigate multipart objects such as Weberian ossicles (Thomas et al., 2023). Different levels of analysis are possible, notably through various considerations such as phylogeny and allometry (Drake & Klingenberg, 2010). Here, we have not considered allometry because this phenomenon is practically unsupported in our study (Supplementary Table S8). ...
... Evolution Letters (2024), Vol. 8 | 783 is notable and different in its totality from the reported partial overlap in skull morphospace between wild and domesticated dogs and pigeon. For pigeons (Young et al., 2017) and domestic dogs (Drake & Klingenberg, 2010), the outliers in the domestic morphospace in contrast to the wild ones are the "fancy pigeons" and the companion breeds, respectively. In goldfish as well, the intensity of breeding selection for ornamental purposes led to major morphological innovation. ...
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... Domestication experiments with wild foxes have shown that phenotypic variation can significantly increase via human selection within just a few generations [1,2]. Modern and ancient DNA studies of many domestic animals have revealed the emergence of variability in skull shape [3][4][5], coat colour [6,7] and other morphological characters such as the increase in vertebrae number in domestic pigs [8,9]. However, the rate at which phenotypes would have responded to human control remains unclear [10]. ...
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Domestication and subsequent human-induced selection has enhanced profound changes in animal morphology. On modern domestic pigs, those transformations encompass not only overall increases in body size but also modifications in skull morphology. While skull morphological differences between modern domestic pigs and wild boar are relatively well-documented, less understood is the variation and underlying mechanisms associated with intensive breeding. In this study, we investigated the rate and direction of phenotypic change of skull morphology using a unique dataset that includes two lineages of German domestic pig that were subjected to similar intensive industrial selection pressures throughout the twentieth century, alongside contemporaneous populations of German wild boar. Size and shape variation of 135 specimens was quantified through geometric morphometrics, with 82 three-dimensional landmarks. We find expected differences in skull shape between wild and domestic pigs, but also convergence between the two domestic lineages through the century of directed breeding, despite population segregation. Our results suggest that cranial morphologies have rapidly responded to selection pressure that is independent of genetic isolation. This also suggests that pig morphotypes quickly reflect human agency and impact upon domestic animal phenotypes, revealing a pathway to investigate early human breeding activity in ancient and historical contexts.
... In addition, there are also 26 unidentified canid elements (Canid ssp.) that are most likely also dogs but could also be intrusive coyote as well. It is difficult to distinguish coyotes, wolves (Canis lupus), and dogs solely based skeletal morphology (Drake and Klingenberg 2010;Howard 1949;Morey 1992), so our identification as dogs remains tentative until genetic testing allows confirmation. Nine of the dog bones show evidence of cutmarks, two show evidence of human impacts, and two are burned. ...
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... Modules are groups of traits that can change independently during development. Examples of this include the face and the neurocranium of domestic dogs (Drake and Klingenberg 2010) and other mammals (Marroig et al. 2009;Shirai and Marroig 2010). Yet, in other vertebrates, the mandible often evolves as a separate module, as in bats (Arbour, Curtis, and Santana 2019) and felids (Christiansen 2008). ...
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... However, it is interesting that modern humans lack a morphological pattern that reflects functional features of the human masticatory apparatus, suggesting a relative "disconnect" between form and function. This is not trivial since several clinical evaluations and decisions are based on this assumed relationship which is true for some mammals such as mice [57], wild carnivores [58], and others. However, this relationship appears to be more complex in humans. ...
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Purpose This pilot study aimed to assess the relationship between bite force variation and dental arch and facial shape using geometric morphometrics, an advanced method of statistical analysis that provides a detailed shape analysis of a structure considering the spatial relationship of its parts. Methods The sample consisted of 16 German adult men and women. For each individual, maximum bite force was recorded in four positions: maximum intercuspation, protrusion, laterotrusion to the right and to the left. Facial and three-dimensional (3D) dental reconstructions were obtained from 3D facial photographs and 3D scans of dental stone models. A total of 51 landmarks were placed. General shape variation was assessed by principal component analysis. Partial least squares analyses were performed to evaluate the covariation between bite force, facial shape, and dental shape. Results There was no clear pattern or statistically significant covariation between our variables. Conclusions Our results suggest a weak relationship between bite force, dental arch, and facial shape. Considering previous work in this field, we propose that low masticatory loads, characteristic in Western urban populations, may explain this. Further studies should, therefore, address this issue, taking into account effect size, the mechanical properties of the diet, and other relevant variables.
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Age-related patterns in cranial suture and synchondrosis obliteration in 371 known-age North American grey wolves (Canis lupus) are examined to assess their utility in estimating the age of archaeological and paleontological wolf crania. Differences in age-related obliteration patterns between these wolves and 576 known-age domestic dogs (Canis familiaris) also are explored. Domestication has likely altered the growth and development of dog crania in relation to that of wolves, but these processes remain poorly understood. Wolf total suture obliteration score and age were positively correlated, indicating that the level of suture obliteration can be used to track age to some extent. Wolf sex and dietary patterns had no meaningful effects on this correlation. Mesocephalic or dolichocephalic dogs generally begin exhibiting more extensive suture obliteration than wolves during early adulthood, at about 2-4 years of age. This pattern of more extensive obliteration persists throughout the lifespan, with dogs tending to experience more obliteration in the observed sutures and synchondroses. Several interrelated factors may contribute to this pattern, all outcomes of domestication, including differences in physical strains in the cranium, alteration of development and ageing, and the emergence of diverse head shapes that relate in part to suture closure timing.
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Since the time of Charles Darwin, the study of the mechanisms of domestication of animals as a model of rapid evolutionary transformations has been of general biological importance. Methods of Geometric morphometrics (GM) make it possible to assess the morphogenetic changes that occur during domestication. Using the experimental strains of American mink Neogale vison, selected for aggressive and tame behavior, significant differences in the centroid size (CS) and shape of the mandible were established between them. Cage non-selected and wild Canadian minks were used as controls. Selection has led to an increase in the CS of mandibles in aggressive and their decrease in tame ones. The greatest differences in the shape of mandibles were manifested between the aggressive and tame strains. The destabilization of mandible development, indirectly estimated by the volume of within-group morphospace (Vm) along the first canonical axes, turned out to be most pronounced in males and females of the tame mink strain, which is directly consistent with the theory of destabilizing selection by D. K. Belyaev. After 16–17 generations of mink selection for aggressive and tame behavior, morphogenetic effects were found, expressed in the divergence of the shape of their mandible, accompanied by destabilization of development, and reflecting the high rate of experimental domestication. The differentiation of the aggressive and tame minks by the shape of the mandibles exceeds the level of sexual differences and is comparable to the degree of morphological divergence between caged and wild Canadian individuals. It is accompanied by morphological hiatus and is formally close to the subspecific rank of intraspecific morphological differences compared with the morphological divergence of the American mink from another species – the Siberian weasel Mustela sibirica. The morphogenetic effects of American mink selection by behavior demonstrate the high adaptive and evolutionary potentials of this invasive species.
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Did the end-Cretaceous mass extinction event, by eliminating non-avian dinosaurs and most of the existing fauna, trigger the evolutionary radiation of present-day mammals? Here we construct, date and analyse a species-level phylogeny of nearly all extant Mammalia to bring a new perspective to this question. Our analyses of how extant lineages accumulated through time show that net per-lineage diversification rates barely changed across the Cretaceous/Tertiary boundary. Instead, these rates spiked significantly with the origins of the currently recognized placental superorders and orders approximately 93 million years ago, before falling and remaining low until accelerating again throughout the Eocene and Oligocene epochs. Our results show that the phylogenetic 'fuses' leading to the explosion of extant placental orders are not only very much longer than suspected previously, but also challenge the hypothesis that the end-Cretaceous mass extinction event had a major, direct influence on the diversification of today's mammals. Molecular data and the fossil record can give conflicting views of the evolutionary past. For instance, empirical palaeontological evidence by itself tends to favour the 'explosive model' of diversification for extant placental mammals 1 , in which the orders with living representatives both originated and rapidly diversified soon after the Cretaceous/Tertiary (K/T) mass extinction event that eliminated non-avian dinosaurs and many other, mostly marine 2 , taxa 65.5 million years (Myr) ago 1,3,4. By contrast, molecular data consistently push most origins of the same orders back into the Late Cretaceous period 5-9 , leading to alternative scenarios in which placental line-ages persist at low diversity for some period of time after their initial origins ('phylogenetic fuses'; see ref. 10) before undergoing evolutionary explosions 1,11. Principal among these scenarios is the 'long-fuse model' 1 , which postulates an extended lag between the Cretaceous origins of the orders and the first split among their living representatives (crown groups) immediately after the K/T boundary 8. Some older molecular studies advocate a 'short-fuse model' of diversification 1 , where even the basal crown-group divergences within some of the larger placental orders occur well within the Cretaceous period 5-7. A partial molecular phylogeny emphasizing divergences among placental orders suggested that over 20 lineages with extant descendants (henceforth, 'extant lineages') survived the K/T boundary 8. However, the total number of extant lineages that pre-date the extinction event and whether or not they radiated immediately after it remain unknown. The fossil record alone does not provide direct answers to these questions. It does reveal a strong pulse of diversification in stem eutherians immediately after the K/T boundary 4,12 , but few of the known Palaeocene taxa can be placed securely within the crown groups of extant orders comprising Placentalia 4. The latter only rise to prominence in fossils known from the Early Eocene epoch onwards (,50 Myr ago) after a major faunal reorganization 4,13,14. The geographical patchiness of the record complicates interpretations of this near-absence of Palaeocene crown-group fossils 14-16 : were these clades radiating throughout the Palaeocene epoch in parts of the world where the fossil record is less well known; had they not yet originated; or did they have very long fuses, remaining at low diversity until the major turnover at the start of the Eocene epoch? The pattern of diversification rates through time, to which little attention has been paid so far, might hold the key to answering these questions. If the Cretaceous fauna inhibited mammalian diversification , as is commonly assumed 1 , and all mammalian lineages were able to radiate after their extinction, then there should be a significant increase in the net per-lineage rate of extant mammalian diversification , r (the difference between the per-lineage speciation and extinction rates), immediately after the K/T mass extinction. This hypothesis, along with the explosive, long-and short-fuse models, can be tested using densely sampled phylogenies of extant species, which contain information about the history of their diversification rates 17-20. Using modern supertree algorithms 21,22 , we construct the first virtually complete species-level phylogeny of extant mammals from over 2,500 partial estimates, and estimate divergence times (with confidence intervals) throughout it using a 66-gene alignment in conjunction with 30 cladistically robust fossil calibration points. Our analyses of the supertree indicate that the principal splits underlying the diversification of the extant lineages occurred (1) from 100-85 Myr ago with the origins of the extant orders, and (2) in or after the Early Eocene (agreeing with the upturn in their diversity known from the fossil record 4,13,14), but not immediately after the K/T boundary, where diversification rates are unchanged. Our findings-that more extant placental lineages survived the K/T boundary than previously recognized and that fewer arose immediately after it than previously suspected-extend the phylogenetic fuses of many extant orders and indicate that the end-Cretaceous mass extinction event had, at best, a minor role in driving the diversification of the present-day mam-malian lineages. A supertree with divergence times for extant mammals The supertree contains 4,510 of the 4,554 extant species recorded in ref. 23, making it 99.0% complete at the species level (Fig. 1; see also
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We evaluate methods for measuring and specifying rates of microevolution in the wild, with particular regard to studies of contemporary, often deemed "rapid," evolution. A considerable amount of ambiguity and inconsistency persists within the field, and we provide a number of suggestions that should improve study design, inference, and clarity of presentation. (1) Some studies measure change over time within a population (allochronic) and others measure the difference between two populations that had a common ancestor in the past (synchronic). Allochronic studies can be used to estimate rates of "evolution," whereas synchronic studies more appropriately estimate rates of "divergence." Rates of divergence may range from a small fraction to many times the actual evolutionary rates in the component populations. (2) Some studies measure change using individuals captured from the wild, whereas others measure differences after rearing in a common environment. The first type of study can be used to specify "phenotypic" rates and the later "genetic" rates. (3) The most commonly used evolutionary rate metric, the darwin, has a number of theoretical shortcomings. Studies of microevolution would benefit from specifying rates in standard deviations per generation, the haldane. (4) Evolutionary rates are typically specified without an indication of their precision. Readily available methods for specifying confidence intervals and statistical significance (regression, bootstrapping, randomization) should be implemented. (5) Microevolutionists should strive to accumulate time series, which can reveal temporal shifts in the rate of evolution and can be used to identify evolutionary patterns. (6) Evolutionary rates provide a convenient way to compare the tempo of evolution across studies, traits, taxa, and time scales, but such comparisons are subject to varying degrees of confidence. Comparisons across different time scales are particularly tenuous. (7) A number of multivariate rate measures exist, but considerable theoretical development is required before their utility can be determined. We encourage the continued investigation of evolutionary rates because the information they provide is relevant to a wide range of theoretical and practical issues.
Chapter
Charles Fox and Jason Wolf have brought together leading researchers to produce a cutting-edge primer introducing readers to the major concepts in modern evolutionary genetics. This book spans the continuum of scale, from studies of DNA sequence evolution through proteins and development to multivariate phenotypic evolution, and the continuum of time, from ancient events that lead to current species diversity to the rapid evolution seen over relatively short time scales in experimental evolution studies. Chapters are accessible to an audience lacking extensive background in evolutionaryy genetics but also current and in-depth enough to be of value to established researchers in evolution biology.
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Applications of quantitative techniques to understanding macroevolutionary patterns typically assume that genetic variances and covariances remain constant. That assumption is tested among 28 populations of the Phyllotis darwini species group (leaf-eared mice). Phenotypic covariances are used as a surrogate for genetic covariances to allow much greater phylogenetic sampling. Two new approaches are applied that extend the comparative method to multivariate data. The efficacy of these techniques are compared, and their sensitivity to sampling error examined. Pairwise matrix correlations of correlation matrices are consistently very high (> 0.90) and show no significant association between matrix similarity and phylogenetic relatedness. Hierarchical decomposition of common principal component (CPC) analyses applied to each clade in the phylogeny rejects the hypothesis that common principal component structure is shared in clades more inclusive than subspecies. Most subspecies also lack a common covariance structure as described by the CPC model. The hypothesis of constant covariances must be rejected, but the magnitudes of divergence in covariance structure appear to be small. Matrix correlations are very sensitive to sampling error, while CPC is not. CPC is a powerful statistical tool that allows detailed testing of underlying patterns of covariation.
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Although fluctuating asymmetry has become popular as a measure of developmental instability, few studies have examined its developmental basis. We propose an approach to investigate the role of development for morphological asymmetry by means of morphometric methods. Our approach combines geometric morphometrics with the two-way ANOVA customary for conventional analyses of fluctuating asymmetry and can discover localized features of shape variation by examining the patterns of covariance among landmarks. This approach extends the notion of form used in studies of fluctuating asymmetry from collections of distances between morphological landmarks to an explicitly geometric concept of shape characterized by the configuration of landmarks. We demonstrate this approach with a study of asymmetry in the wings of tsetse flies (Glossina palpalis gambiensis). The analysis revealed significant fluctuating and directional asymmetry for shape as well as ample shape variation among individuals and between the offspring of young and old females. The morphological landmarks differed markedly in their degree of variability but multivariate patterns of landmark covariation identified by principal component analysis were generally similar between fluctuating asymmetry (within-individual variability) and variation among individuals. Therefore there is no evidence that special developmental processes control fluctuating asymmetry. We relate some of the morphometric patterns to processes known to be involved in the development of fly wings.
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Are measurements of quantitative genetic variation useful for predicting long-term adaptive evolution? To answer this question, I focus on gmax , the multivariate direction of greatest additive genetic variance within populations. Original data on threespine sticklebacks, together with published genetic measurements from other vertebrates, show that morphological differentiation between species has been biased in the direction of gmax for at least four million years, despite evidence that natural selection is the cause of differentiation. This bias toward the direction of evolution tends to decay with time. Rate of morphological divergence between species is inversely proportional to θ, the angle between the direction of divergence and the direction of greatest genetic variation. The direction of greatest phenotypic variance is not identical with gmax , but for these data is nearly as successful at predicting the direction of species divergence. I interpret the findings to mean that genetic variances and covariances constrain adaptive change in quantitative traits for reasonably long spans of time. An alternative hypothesis, however, cannot be ruled out: that morphological differentiation is biased in the direction gmax because divergence and gmax are both shaped by the same natural selection pressures. Either way, the results reveal that adaptive differentiation occurs principally along "genetic lines of least resistance."
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The domestic dog varies remarkably in cranial morphology. In fact, the differences in size and proportion between some dog breeds are as great as those between many genera of wild canids. In this study, I compare patterns of intracranial allometry and morphologic diversity between the domestic dog and wild canid species. The results demonstrate that the domestic dog is morphologically distinct from all other canids except its close relatives, the wolf-like canids. Following this, I compare patterns of static and ontogenetic scaling. Data on growth of domestic dogs are presented and used to investigate the developmental mechanisms underlying breed evolution. Apparently, most small breeds are paedomorphic with respect to certain morphologic characters. In dogs and other domestic animals, morphologic diversity among adults seems to depend on that expressed during development.
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The molecular chaperone protein Hsp90 has been widely discussed as a candidate gene for developmental buffering. We used the methods of geometric morphometrics to analyze its effects on the variation among individuals and fluctuating asymmetry of wing shape in Drosophila melanogaster. Three different experimental approaches were used to reduce Hsp90 activity. In the first experiment, developing larvae were reared in food containing a specific inhibitor of Hsp90, geldanamycin, but neither individual variation nor fluctuating asymmetry was altered. Two further experiments generated lines of genetically identical flies carrying mutations of Hsp83, the gene encoding the Hsp90 protein, in heterozygous condition in nine different genetic backgrounds. The first of these, introducing entire chromosomes carrying either of two Hsp83 mutations, did not increase shape variation or asymmetry over a wild-type control in any of the nine genetic backgrounds. In contrast, the third experiment, in which one of these Hsp83 alleles was introgressed into the wild-type background that served as the control, induced an increase in both individual variation and fluctuating asymmetry within each of the nine genetic backgrounds. No effect of Hsp90 on the difference among lines was detected, providing no evidence for cryptic genetic variation of wing shape. Overall, these results suggest that Hsp90 contributes to, but is not controlling, the buffering of phenotypic variation in wing shape.