Received: 18 December 2019 Revised: 13 April 2020 Accepted: 19 April 2020

DOI: 10.1002/ar.24471

SPECIAL ISSUE ARTICLE

Selective breeding in domestic dogs: How selecting

for a short face impacted canine neuroanatomy

Molly C. Selba1 | Emily R. Bryson1 | Ciele L. Rosenberg1 | Hock Gan Heng2 |

1
Valerie B. DeLeon

1
University of Florida, Gainesville, Florida
2
Purdue University, West Lafayette,
Indiana
Correspondence
Molly C. Selba and Valerie B. DeLeon,
University of Florida, Gainesville, FL.
Email: mollyselba@ufl.edu (M. C. S.) and
vdeleon@ufl.edu (V. B. D.)
Abstract
The range of cranial morphology seen in domestic dogs (Canis lupus
familiaris) is a direct result of thousands of years of selective breeding. This
article is the first to investigate how selection for reduced faces in brachyce-
phalic dogs impacted the neuroanatomy of the canine brain through the analy-
sis of endocasts. Previous research has demonstrated global effects on the
shape of the bony cranium as the result of these breeding practices; however,
these studies have largely focused on the bony structures of the skull and failed
to consider the influence of facial reduction on the soft tissues of the brain. We
generated endocasts from an existing set of clinically-obtained CT scans rep-
resenting a variety of dogs with various cranial morphologies. These dogs
represented four breeds as well as a comparative sample of dogs of unknown
breed. We recorded three-dimensional coordinate data for 31 landmarks rep-
resenting various gyri, sulci, and other neuroanatomical landmarks that
allowed us to analyze differences in shape of the endocasts. Through geometric
morphometric analyses, we determined that the endocast shape variance in
this sample is correlated with cephalic index, and thus the selection for facial
reduction has caused a perceivable effect on canine neuroanatomy. Addition-
ally, we found the majority of the shape variance in the sample to be associated
with olfactory anatomy; however, the rest of the morphology also correlates
with cephalic index. The results of this article indicate that modern breeding
practices and the selection for dogs with short faces have significantly
influenced canine neuroanatomy.

KEYWORDS
brachycephaly, canine, endocast, geometric morphometrics

1 | INTRODUCTION reduction affects the craniodental complex in domestic

Domestic dogs, Canis lupus familiaris, are characterized
by their extremely diverse cranial morphology. This
diversity is a direct result of hundreds of years of human-
imposed selective breeding. Our previous research dem-
onstrated how artificial breeding for extreme facial
dogs (Selba, Oechtering, Heng, & DeLeon, 2020). This
research identified that most of the cranial shape vari-
ance seen in that sample of dogs was associated with
cephalic index (CI). Furthermore, the shape changes seen
in the cranium covary with the shape changes seen in the
mandible. The selection for facial reduction produced

Anat Rec. 2020;1–15. wileyonlinelibrary.com/journal/ar © 2020 American Association for Anatomy 1

2 SELBA ET AL.
global changes in the canine cranium. These findings
were consistent with other studies on this topic, which
have demonstrated the diversity of cranial morphology
among domestic dogs and that the breeding of these dogs
has produced correlated patterns in skull proportions,
cranial base angles, and so on (Drake, 2011; Drake &
Klingenberg, 2010; Wayne, 1986). Brachycephalic dog
breeds allow for a nonlaboratory experiment on facial
reduction, providing additional insight into this well
studied phenomenon associated with the evolutionary
history of other animals including primates. Additionally,
studying canids offers researchers a unique opportunity
to study cranial variation due to their well-documented
history and morphological diversity (Frantz et al., 2016).
Despite evidence that selection for facial reduction has
led to global effects on the morphology of the canine cra-
nium, researchers have largely neglected the soft tissue
contents of the endocranial cavity. This study addresses
the impact of facial reduction on canine neuroanatomy
through the geometric morphometric analysis of digitally
created endocasts. This research will help us better under-
stand the interplay between the bony cranium—which has
been drastically altered as a result of human-imposed
selection for facial reduction—and the highly plastic
canine brain. The study of endocasts to better understand
the neuroanatomy of various organisms (living and
extinct) has a long history within the fields of anthropology
and vertebrate paleontology (Balanoff et al., 2016; Bruner
& Ogihara, 2018). Endocasts may be the result of natural
processes (Falk & Clarke, 2007; Iurino et al., 2015;
Neubauer, 2014) or can be made from latex (Neubauer,
2014; Radinsky, 1971; Sakai, Arsznov, Lundrigan, &
Holekamp, 2011) or generated virtually from CT image
volumes (Ahrens, 2014; Bertrand et al., 2019; Racicot &
Colbert, 2013; Zollikofer & Ponce De León, 2013). Data
can be collected from the virtual endocasts, using two
dimensional measurements (Bruner, 2004), volume and
surface area (Racicot & Colbert, 2013; Sakai et al., 2011;
Zollikofer & Ponce De León, 2013), or placement of three
dimensional (3D) landmarks (Ahrens, 2014; Bruner &
Ogihara, 2018; Iurino et al., 2015).
The neuroanatomy of a variety of organisms has
been studied through the analysis of endocasts, including
both human and nonhuman primates (Balzeau &
Gilissen, 2010; Bienvenu et al., 2011; Fischl et al., 2007;
Neubauer, Gunz, & Hublin, 2010). These studies often
focus on ontogeny, asymmetry, and more general compara-
tive anatomy. Balanoff & Bever (2016) described the role of
endocasts in the study of brain evolution, including their
use in understanding the origins of the class Mammalia.
Silcox, Dalmyn, & Bloch (2009); Silcox, Benham, &
Bloch (2010) used endocasts to make inferences about phy-
logeny and behavior of fossil Primates. In Cetacea, porpoise
endocasts have been studied to better understand six
extant species of Phocoenidae through the analysis of sev-
eral variables including asymmetry, degree of gyrification,
gross brain shape, and volumetric measurements (Racicot
& Colbert, 2013). Through examination of the volumetric
measurements, the authors found that the relative brain
size varied among the specimens and that some species,
such as Phocoena sinus and Neophocaena phocaenoides,
may exhibit extreme paedomorphic characteristics as
evidenced by their proportionally large endocranial cavities.
In Rodentia, endocast analysis was used to better
understand the phylogenetic relationships of members
of the squirrel-related clade (Bertrand et al., 2019). Geo-
metric morphometric analysis of endocasts has also
been used to study the order Carnivora, including studies
focusing on procyonid species (Ahrens, 2014), felids
(Iurino et al., 2015), and members of the family Hya-
enidae (Sakai et al., 2011). Using geometric morphomet-
rics to study endocasts can also be helpful when working
with natural endocasts of unknown species. Iurino et al.
(2015) compared a Late Pleistocene endocast with a charac-
teristically felid shape to brains of living Felidae and found
that the endocast best resembles that of a lynx species. All
of these studies evaluate the morphology of the entire brain
through the use of landmarks distributed across the surface
of the endocasts. These landmarks are positioned at key
neural structures, such as prominent gyri and sulci, and
were compared across the different specimens through geo-
metric morphometric and visual analyses.
Fossil hominins have also been studied in depth
through the analysis of endocasts (Bienvenu et al., 2011;
Bruner, 2004; Falk & Clarke, 2007; Neubauer, 2014;
Schepers, 1946, 1950; Zollikofer & Ponce de León, 2013).
For example, endocasts have been used to better understand
the emergence of language through the analysis of petalias
indicating Broca's and Wernike's areas (Beaudet, 2017).
Additionally, the study of endocasts has been used to exam-
ine social behaviors (Sakai et al., 2011; Vinuesa et al., 2016),
cognitive flexibility (Vinuesa et al., 2016), and even handed-
ness (Knecht et al., 2000). Researchers also make inferences
about social behavior based on the observed correlation
between the size of the frontal cortex and the amount of
sociability (Sakai et al., 2011; Vinuesa et al., 2016).
Canine neuroanatomy has been researched quite
extensively in the past using a variety of methods includ-
ing the analysis of natural endocasts (Radinsky, 1973), the
creation of latex endocasts (Lyras & Van Der Geer, 2003;
Radinsky, 1971), and the analysis of neuroimaging includ-
ing MRI and fMRI (Czeibert, Andics, Petneházy, &
Kubinyi, 2019; Datta et al., 2012; Roberts, McGreevy, &
Valenzuela, 2010). Lyras & Van Der Geer (2003) consid-
ered the sulcal pattern medial to the coronal sulci and the
shape and relative size of the proreal gyrus across 29 species
SELBA ET AL.
to inform phylogenetic interpretations of the Caninae sub-
family. Roberts et al. (2010), in contrast, considered only
domestic dogs and found that cranial proportions were sig-
nificantly correlated to a progressive ventral pitching of the
primary longitudinal brain axis, thus suggesting human-
induced reorganization of the brain of modern canines
(seemingly without any corresponding changes in behavior
or cognition). Datta et al. (2012) and Czeibert et al. (2019)
presented a canine brain atlas and a brain label map for neu-
roimaging analysis (respectively). Both authors expanded
upon what is already known about the neuroanatomy of
modern dogs and created novel highly-detailed resources
that can be used to better understand the canine brain.
Dogs, in particular, are a good taxon for endocast
research because they have a brain that nearly fills the
cranial cavity and thus produces a strong correlation
between the morphology of the endocast and the neuro-
anatomy of the brain (Balanoff et al., 2016). Despite this
fact, no research has been done using 3D landmarks from
the digital endocasts from a number of breeds to better
understand the neuroanatomy of domestic dogs.
Additionally, the specific effects of facial reduction on
the neuroanatomy of these dogs remains unclear. There
is evidence that humans have altered the neuroanatomi-
cal configuration of modern dogs. According to Roberts
et al. (2010), there is a relative reduction in cranial length
compared to width, which was significantly correlated to
a progressive ventral pitching of the primary longitudinal
brain axis, as well as a change in the position of the olfac-
tory lobe. This demonstrates that there has been human-
induced repositioning of elements of the canine brain.
Additionally, Czeibert et al. (2019) noted differences in
brain shape that correlate with head shape; however,
there are very few studies that address this phenomenon,
and the results of these studies are largely inaccessible
and have not been incorporated into canine brain atlases.
Although it is a phenomenon that has been studied in
brachycephalic cats, the analysis of canine endocast mor-
phology using geometric morphometric analysis has yet
to be undertaken but is an inquiry that would be valuable
to comparative anatomists, clinical veterinarians, neuro-
anatomists, and many others (Schmidt et al., 2017).
2 | HY POTH ES E S
Previous research has identified extreme effects of the
selection for facial reduction impacting the global canine
cranium. We hypothesized that morphological variation seen
in the endocasts of this canine sample would demonstrate
differences in shape that correlate with CI. We predicted that
the selection for facial reduction has produced correlated
patterns of brachycephaly and facial reduction, and that
3
these patterns are concurrent with previous research (Selba
et al., 2020).
In our previous study of the skull, we found notable
differences in the position and shape of the cribriform
plate (Selba et al., 2020). We expected that the olfactory
bulbs would show high variation in shape between the
normocephalic and brachycephalic condition. We also
anticipated some consistencies in morphology between
the generated endocast and the bony morphology of the
endocranial cavity. Results in Selba et al. (2020) showed
relatively less variance in cranial base structures, and
we expected that the endocast landmarks associated
with features in the middle and posterior cranial fossae
would show little variation between the normocephalic and
brachycephalic condition. This includes landmarks indicat-
ing the position of the optic chiasm and the rostral and
caudal boundaries of sella turcica. As opposed to other
landmarks of the cerebral hemispheres that demonstrate
much more plasticity, we predicted that the landmarks on
the base of the endocast would be much more conserved.
3 | MATERIALS AND METHODS
3.1 | Sample
The study was conducted on clinically obtained canine CT
scans from the University of Leipzig, Germany and Purdue
University (West Lafayette, Indiana) representing 57 domes-
tic dogs. This sample was previously used to study cranial
morphology in Selba et al., 2020. This database included
17 crania from Purdue University and 40 crania from
University of Leipzig, all of which were of unknown sex.
All specimens were adults of unknown age (confirmed
by visual inspection of dental eruption) and were free of
pathology and trauma. The specimens from University
of Leipzig consisted of dogs of four well-known breeds:
English bulldogs (n = 10), French bulldogs (n = 9), pugs
(n = 9), and beagles (n = 11), with one dog being of
unknown breed. A Philips Brilliance 6 CT Scanner (power:
120 kVp; current: 120 μA) was used to generate DICOM
images with square pixels ranging from 0.2 to 0.3 mm and
a slice thickness of 0.5 mm. The specimens from Purdue
University were all of unknown breed and represented
a variety of cranial morphologies, including both the
normocephalic and brachycephalic condition. These scans
were created using a GE LightSpeed VCT CT Scanner
(power: 120 kVp; current: 200–300 μA), producing DICOM
images with square pixels ranging from 0.2 to 0.5 mm and
a slice thickness of 0.625 mm. The combined sample con-
tains a variety of dog breeds, and yet, admittedly this wide
range does not encompass the full range of cranial mor-
phologies present within Canis lupus familiaris. Because
4 SELBA ET AL.
the body masses of the dogs in the sample were unknown,
neurocranium centroid size was calculated to better under-
stand the distribution of body sizes. Confounding effects of
allometry were minimized by selecting brachycephalic and
normocephalic dogs with approximately equal distributions
of body size as estimated by neurocranial centroid size.
Reconstructions of the crania were generated using the
image postprocessing software Amira 6.4 and 6.5 (FEI,
Houston).
3.2 | Determination of CI and other
metrics
In Selba et al. (2020), a variety of metrics were calculated
on this sample set including neurocranium centroid
size and CI. CI was determined through cranial measure-
ments taken using Amira software. Cranial length and
width were measured for each dog, and a ratio of width
(right zygomatic arch to left zygomatic arch) to length
(rhinion to most posterior point on the occipital protu-
berance) was used to determine CI. Based on the
established CIs, the dogs were then divided into two
groups: normocephalic dogs (CI ≤ 0.80, n = 25) and
brachycephalic dogs (CI > 0.81, n = 32; Roberts
et al., 2010). Using this distinction, the normocephalic
dogs have long snouts and crania that are longer than
they are wide, and brachycephalic dogs have short
snouts and crania that are wider than they are long. The
separation between normocephalic and brachycephalic
dogs was originally based on methods used by Roberts
et al. (2010).
3.3 | Data processing
The endocast was extracted from the CT scan of each
of the dogs in the sample by one author (E. R. B.)
using a semi-automated segmentation method in Amira
(Figure 1). A threshold representing the density of the
bone was established and all the pixels representing the
cranium were assigned to an initial material. The bone
threshold was determined individually for each dog to
best encapsulate the bones of the cranium without mak-
ing the bone artificially thin or adding extra unneeded
voxels to the bone. All foramina were closed manually to
the level of the inner table using the “paintbrush” tool,
allowing for semi-automated selection of voxels in the
endocranial cavity without including the volume of any
canals or foramina. The foramen magnum was closed
using a technique established by Balanoff et al. (2016).
Segmentation of the endocranial space was conducted
from the most superior slice in the transverse plane and
proceeded inferiorly. The endocranial cavity volume of
interest (VOI) was selected slice-by-slice using either
the paintbrush or continuous selection tool. Thinner
bones that were not collected in the initial “cranium”
material were manually added using the “paintbrush”
tool as needed. The segmentation of endocranial voxels
was adjusted as needed by reviewing slices in a coronal
plane and then a sagittal plane. The resulting VOI con-
tained the entirety of the endocranial space and excluded
all of the surrounding bone as well as any open spaces
such as foramina.
The generated endocast included the sagittal sinus
and portions of the transverse and sigmoid sinuses.
Although these spaces do not reflect the brain morphol-
ogy, they contribute to the endocranial space and thus
were included as part of the endocast. This protocol is
similar to other studies where endocasts are generated
(Bienvenu et al., 2011; Neubauer et al., 2010)
3.4 | Landmark data collection
The program Amira was used to collect 3D coordinate data
for 31 biologically relevant landmarks on the generated
endocasts (Figure 2; Table 1). These landmarks were col-
lected in two separate trials by one author (M. C. S.). Mea-
surement error was addressed by calculating the linear
distance between each landmark position of trial one and
trial two for each specimen. For landmarks that had over
4 mm distance between the two trials, a third trial was col-
lected, and the closest two trials were retained for analysis.
Both trials were averaged to further minimize the effect of
measurement error. There did not appear to be an effect of
brachycephaly on the frequency of problematic landmarks
(i.e., distances of >4 mm between trials). Dogs with prob-
lematic landmarks included approximately equal numbers
of brachycephalic (N = 13) and normocephalic (N = 12)
dogs. The three landmarks that had the lowest average
imprecision were landmarks 29–31: optic chiasm at midline
(0.508 mm), anterior dorsum sellae (0.553 mm), posterior
dorsum sellae (0.483 mm). They all represent prominent
neuroanatomical features on the cranial base. The three
landmarks with the highest imprecision were landmarks
14, 15, and 24: right (1.304 mm) and left (1.351 mm) ansate
sulcus and right rostral-most part of the lateral rhinal sul-
cus at the olfactory bulb (1.304 mm). These landmarks
are placed in various sulci, the boundaries of which can be
difficult to determine. The points placed on the endocasts
represent a variety of previously-established canine neuro-
anatomical landmarks including prominent gyri and sulci,
cranial nerves, as well as other functionally-important
structures. The landmarks were chosen based off landmark
definitions used in the analysis of endocasts by Lyras &
SELBA ET AL.
F I G U R E 1 A computer-generated endocast of a beagle (normocephalic) from (a) a lateral view within the cranium, (b) a lateral view
with the cranium showing a sagittal cut, and (c) a superior view with the cranium showing a transverse cut
Van Der Geer (2003) and Bienvenu et al. (2011), which
focused on dogs and hominids, respectively. They represent
a global distribution of landmarks on the cerebrum of the
endocasts and do not include cerebellar or brainstem land-
marks, corresponding with Lyras & Van Der Geer (2003)
and Radinsky (1971).
3.5 | Geometric morphometric analysis
MorphoJ 1.06d and R 3.3.1 (using the geomorph package)
were used to analyze the three-dimensional landmark
coordinate data (Adams, Collyer, Kaliontzopoulou, &
Sherratt, 2017; Klingenberg, 2011). Data representing the
shape of the endocast were analyzed assuming object
symmetry in order to emphasize inter-individual varia-
tion and minimize the effect of asymmetric variance
5
(following Klingenberg, Barluenga, & Meyer, 2002).
However, the asymmetric component of shape variance
was tested in geomorph to determine if normocephalic
and brachycephalic dogs have different patterns of direc-
tional asymmetry in their endocasts.
To address the shape of the endocasts in this sample,
the averaged landmark coordinate data were analyzed in
MorphoJ and R using generalized Procrustes superimposi-
tion and the symmetric component of variance. Procrustes
superimposition translates the raw data to a common cen-
troid, scales it to unit centroid size, and rotates the configu-
ration such that the sum of the squared distances between
corresponding landmarks is minimized. The shape variance
was visualized qualitatively in MorphoJ using principal
components analysis (PCA) of the transformed landmark
coordinates and vector plots. These plots display the shape
variance associated with each principal component (PC).
6 SELBA ET AL.
F I G U R E 2 Landmark placement from six views: (a) rostral (close-up of olfactory bulb), (b) inferior, (c) superior, (d) rostral, (e) caudal,
(f) left lateral. List of landmarks used can be found in Table 1
A broken stick distribution in the vegan package of R was
used to determine which PCs provided useful information
(Frontier, 1976; Jackson, 1993; Oksanen et al., 2017). To test
the effect of CI as a categorical factor (Normocephalic
vs. Brachycephalic, or NvB), we applied a Procrustes
ANOVA using the procD.lm function of the geomorph pack-
age in R.
In order to address possible allometric effects in these
endocasts, the sample included a selection of dogs in
which the normocephalic and brachycephalic groups
contained dogs of a comparable range of body sizes. Neu-
rocranium centroid size reported in Selba et al. (2020)
was used as a proxy for body size, and the sample was
chosen for that study to include dogs with a similar range
of neurocranial centroid sizes: 198.11 ± 26.70 mm s.d. in
the brachycephalic group and 210.49 ± 25.13 mm s.d. in
the normocephalic group. For this study, we tested the
correspondence of neurocranial centroid size and endo-
cast centroid size using a correlation analysis in R, and
we confirmed that endocast centroid size was comparable
in the normocephalic and brachycephalic groups using a
Welch's t-test in R to test the effect of categorical CI
(NvB) on endocast centroid size. Allometric effects in
endocast shape were identified using a procD.lm analysis
in geomorph (shape  endocast centroid size) and specifi-
cally by testing the correlation of PC1 scores with endo-
cast centroid size. The effect of CI as a categorical factor
(NvB) independent of endocast centroid size was tested
using a procD.lm analysis (model: shape  endocast cen-
troid size * NvB).
Additionally, we expected that much of the shape
variance would be apparent in the olfactory bulbs, and
we evaluated these results by visual inspection of vector
plots showing variance of landmarks in the PCA in Mor-
phoJ. We expected that this variance might obscure the
variance at other landmarks in the endocast. In order to
test the effect of facial reduction on the shape of the
endocast independent of the olfactory bulbs, a subset of
endocast landmarks (landmarks 1–6, 12–23, and 26–31)
that did not include any of the olfactory bulb landmarks
were analyzed. We took this subset of landmarks and
applied another Procrustes superimposition followed by
PCA in MorphoJ. To test the effect of CI on this subset
of landmarks, we applied another Procrustes ANOVA
using the procD.lm function of the geomorph pack-
age in R.
We also hypothesized that the endocast landmarks
corresponding with the cranial base would show little vari-
ation between the normocephalic and brachycephalic con-
dition. In order to observe the effect of facial reduction on
this area of the endocast, a subset of endocast landmarks
(landmarks 3–4, 19–22, 29–31) were analyzed through
visual assessment of vector plots of all 31 landmarks.
Finally, in order to address proportions of the brain
using metrics commonly referenced in endocast studies,
we also calculated the surface area and volume of each of
SELBA ET AL. 7

TABLE 1 Landmarks collected 4 | RESULTS

Landmark Description
Visual inspection of the endocasts of brachycephalic and
1 R frontal pole
normocephalic dogs shows a clear difference in overall
2 L frontal pole shape of the endocast (Figure 3). As expected, CI was
3 R temporal pole found to have a significant association with canine endo-
4 L temporal pole cast morphology. There was a significant effect of CI as a
5 R occipital pole categorical factor (NvB) on the asymmetric component of
shape variance (p < .001); however, only the symmetric
6 L occipital pole
component of variance was used for further analysis. When
7 R olfactory lobe—medial
the symmetric component of variance in endocast shape
8 L olfactory lobe—medial was analyzed using PCA after Procrustes superimposition,
9 R olfactory lobe—superior the majority of the variance (0.6486) was encompassed
10 L olfactory lobe—superior by PC1 (Figure 4). This variance is more than would be
11 Olfactory lobe—inferior and midline expected randomly (0.0812) as estimated by the broken
12 R coronal sulcus—most lateral point stick distribution. Approximately 5% of the variance was
encompassed by PC2 (0.0549), which is less than would be
13 L coronal sulcus—most lateral point
expected randomly (0.0637). The shape change along PC1
14 R ansate sulcus—most medial point
15 L ansate sulcus—most medial point
16 R pseudosylvian fissure—most medial point
17 L pseudosylvian fissure—most medial point
18 Base of olfactory peduncle—midline
19 R intersection of presylvian sulcus and rostral
part of lateral rhinal sulcus
20 L intersection of presylvian sulcus and rostral
part of lateral rhinal sulcus
21 R inferior-most point on the temporal lobe (on
caudal composite gyrus)
22 L inferior-most point on the temporal lobe (on
caudal composite gyrus)
23 Intersection of longitudinal fissure and R and L
cruciate sulci—midline
24 R rostral-most part of lateral rhinal sulcus at
theolfactory bulb
25 L rostral-most part of lateral rhinal sulcus at the
olfactory bulb
26 R middle ectosylvian sulcus—most superior and
posterior point
27 L middle ectosylvian sulcus—most superior and
posterior point
28 Longitudinal fissure-most posterior point
29 Optic chiasm at midline
30 Anterior dorsum sellae
31 Posterior dorsum sellae

Note: The 31 endocast landmarks (Figure 2) chosen for this study.

the endocasts in this sample. We compared the surface F I G U R E 3 Example endocasts of a brachycephalic pug (a–d)
areas, volumes, and the ratio of surface area-to-volume and a normocephalic beagle (e–h) in four views: (a,e) rostral, (b,f)
between the normocephalic and brachycephalic dogs inferior, (c,g) left lateral, (d,h) superior. In views b-h, rostral is to
using Welch's two-sample t-tests in R. the left
8 SELBA ET AL.

F I G U R E 4 Plot of principal component (PC) 1 and 2 scores for the symmetric component of variance using the total set of endocast
landmarks for all dogs in the sample (n = 57). The color indicates CI and the symbol indicates breed. Convex hulls indicate whether the dog
is normocephalic (with a CI lesser than or equal to 0.80) or brachycephalic (with a CI greater than or equal to 0.81). CI is strongly correlated
with position along PC1

is strongly correlated with CI (r = .91173, df = 55,
p < .001). The brachycephalic dogs with a high CI are posi-
tioned low on PC1, while normocephalic dogs with low CI
are positioned high on PC1. The dogs divide into clear (yet
slightly overlapping) groups based on whether they are
normocephalic or brachycephalic. Additionally, they also
cluster into breed groups: pugs, beagles, English bulldogs,
French bulldogs, and unknown. High scores on PC1
appear to represent normocephalic dogs who have a more
elongated endocast while low scores on PC1 indicate a
shorter and slightly wider endocast in the brachycephalic
dogs (Figure 5). The majority of the shape change on PC1
between the normocephalic and brachycephalic condition
is centered on the olfactory bulbs and olfactory peduncles
(Landmarks 7, 8, 9, 10, 11, 24, and 25). The medial land-
marks on the olfactory bulb are displaced caudally in the
brachycephalic condition while the more lateral landmarks
on the olfactory bulbs are displaced caudally and laterally.
Note that the assumption of object symmetry removes
any mediolateral (asymmetric) variance in midline land-
marks. There is some variation as well with the position of
the ansate sulcus (Landmarks 14 and 15), which marks
the boundary of the somatosensory area. Compared to the
normocephalic dogs, the ansate sulcus is more rostrally dis-
placed in the brachycephalic condition.
Additionally, on PC1, the majority of the other land-
marks show a slight medio-lateral widening in the brachy-
cephalic condition, resulting in a slightly wider endocast
in the brachycephalic dogs. From a lateral view, it appears
as though the landmarks on the dorsal aspect of the endo-
cast (1–2, 12–15, and 23) are displaced superiorly in the
brachycephalic condition and the landmarks on the ventral
aspect (21–22 and 29–31) are displaced more inferiorly,
resulting in a brain that is slightly wider and more expanded
supero-inferiorly. Interestingly, the most caudal point of the
median longitudinal fissure (Landmark 28) is only displaced
slightly ventrally in the brachycephalic condition (with no
change antero-posteriorly), supporting the conclusion that
the majority of the shape change is attributed to the rostral
portion of the endocast. Additionally, the landmarks of the
cranial base (3–4, 19–22, and 29–31), which include both
sella turcica and the optic chiasm, are highly conserved
between the two groups. These landmarks show very little
difference in shape between the normocephalic and the
brachycephalic condition.
Position on PC2 does not appear to correlate with
breed or CI (Figures 3, 4). The majority of shape change
on PC2 is seen in relation to the position of the post-
cruciate gyrus, with the dogs with a high PC2 score hav-
ing a much wider and caudally placed postcruciate gyrus
(Landmarks 12–15 and 23). Additionally, there appears
to be some difference in the position of the sylvian gyrus
(as bounded by landmarks in the pseudosylvian fissure
and middle ectosylvian sulcus). In dogs with a high value
on PC2, the sylvian gyrus is more rostrally and laterally
placed (Figure 5).
We wanted to know if allometric effects were an alter-
native explanation for the differences in shape observed in
SELBA ET AL. 9

F I G U R E 5 Shape changes associated with low scores on PC1 (a) and PC2 (b) scores based on endocast shape as represented by the
complete set of endocast landmarks (superior view on the left and lateral view on the right; in both cases, the rostral side of the endocast is
facing to the right). The point represents the mean form and the vector stem indicates a score of −0.15 on the PC

our canine sample. We determined that endocast centroid
size does correspond to the centroid size of the neuro-
cranium reported for this sample in Selba et al. (2020)
(r = .90; df = 55; p < .001), and there was no significant dif-
ference in endocast centroid size between normocephalic
and brachycephalic dogs in the sample (t = −1.3196,
df = 53.734, p = .1926). These results suggested that the
groups were of comparable overall body size. However,
procD.lm analysis indicated that there was a significant
allometric effect on endocast shape (F = 14.916; df = 1;
p < .001); and specifically, there was a correlation between
PC1 score and endocast centroid size (r = .5503, df = 55,
p < .001). To test whether there was an effect of CI as a cat-
egorical factor (NvB) on endocast shape independent of the
common allometric component (Mitteroecker et al., 2004),
we used a procD.lm analysis (model: shape  neuro-
cranium size * NvB). Main effects of neurocranium size
and NvB were both significant (p < .001), but the interac-
tion term was nonsignificant (p = .508), so we applied a
second procD.lm analysis (model: shape  neurocranium
size + NvB), confirming significant main effects of size
(F = 28.005; df = 1; p < .001) and NvB (F = 49.399; df = 1;
p < .001). A bivariate scatterplot of PC1 score against endo-
cast centroid size demonstrates that, for a given size,
normocephalic dogs have higher PC1 scores (Figure 6).
In order to understand how the morphology of the
olfactory lobes and peduncle impacted the overall vari-
ance of shape in the combined sample, a subset of the
landmarks excluding all of the landmarks specific to
the olfactory-related structures were analyzed separately.
When the variance in the shape of the cerebrum without
the inclusion of the olfaction-related structures was ana-
lyzed using PCA after Procrustes superimposition, the
majority of the variance (0.3836) was encompassed by
PC1 (Figure 7). Approximately 10% of the variance was
encompassed by PC2 (0.0999). These variances were more
than would be expected randomly (0.0812 and 0.0637,
respectively) as estimated by the broken stick distribution,
10
and so were deemed biologically relevant. Results of the
PCA excluding olfactory structures was similar to the
analysis of the full landmark set. Again, the shape change
along PC1 is correlated with CI (r = .87536, df = 55,
p < .001), and there was a significant effect of CI as a cate-
gorical factor (NvB) (F = 19.63; df = 1; p < .001). The
brachycephalic dogs with a high CI are positioned low on
PC1, while normocephalic dogs with low CI are
F I G U R E 6 Bivariate plot of endocast centroid size
(endocastCS) versus principal component 1 (PC1) score. For a given
endocastCS, normocephalic dogs (orange, n = 25) are higher on
PC1 than brachycephalic dogs (blue, n = 32)
F I G U R E 7 Plot of principal component (PC) 1 and 2 scores for the reduced set of endocast landmarks (excluding all olfaction-related
landmarks) for all dogs in the sample (n = 57). The color indicates CI and the symbol indicates breed. Convex hulls indicate whether the dog
is normocephalic (with a CI lesser than or equal to 0.80) and brachycephalic (with a CI greater than or equal to 0.81). CI is strongly
correlated with position along PC1
SELBA ET AL.
positioned high on PC1. The dogs divide into clear (yet
slightly overlapping) groups based on whether they are
normocephalic or brachycephalic, and they cluster into
breed groups.
With the olfactory-related landmarks removed, the
shape differences in the rest of the neuroanatomy become
much more apparent (Figure 8). The majority of the shape
change captured by PC1 is at the rostral portion of the
endocast. The rostral portion (represented by landmarks
1–2 and 12–13) of the endocasts of dogs with a low score
on PC1 (the brachycephalic condition) is displaced later-
ally and rostrally. Additionally, the optic chiasm and base
of the olfactory peduncle at the midline are positioned
much more caudally in dogs with a low score on PC1. On
PC2 there is an apparent lengthening and narrowing of
the endocast from the superior view in dogs with a low
score on PC2. Dogs with a low PC2 score are predomi-
nantly pugs and dogs of unknown breed. These differ-
ences in shape represent predominantly affine changes, or
generalized changes in proportion.
The surface areas and volumes of the endocasts in this
sample were also calculated (Figure 9). There was no sig-
nificant difference in the surface area or volume between
brachycephalic and normocephalic dogs (p = .506 and
.070, respectively); however, there was a statistically
significant difference between the surface-area-to-volume
ratio between brachycephalic and normocephalic dogs
(p < .001; t = −3.797; df = 51.599). This suggests that their
SELBA ET AL. 11

F I G U R E 8 Shape changes associated with low scores on PC1 (a) and PC2 (b) scores based on endocast shape as represented by the
reduced set of endocast landmarks which excludes any olfaction-related landmarks (superior view on the left and lateral view on the right;
in both cases, the rostral side of the endocast is facing to the right). The point represents the mean form and the vector stem indicates a score
of −0.15 on the PC

brains have a lower surface area relative to the volume of
their brains (Figure 9). This is the result of having brains
that are more globular than normocephalic dogs.
5 | DISCUSSION
Despite the fact that the bony morphology of the domestic
dog has been studied in depth (Drake, 2011; Drake &
Klingenberg, 2010; Selba et al., 2020; Wayne, 1986), there
is much that is still unknown about how the morphology
of the soft tissue structures housed by their crania differs
between the normocephalic and brachycephalic conditions.
The objective of this study was to better understand the
effects of the selection for facial reduction on the neuro-
anatomy of a sample of modern dogs. The results of this
study suggest that the breeding of dogs to have a variety of
cranial morphologies impacted the configuration of their
neuroanatomy. The largest difference in shape between
brachycephalic and normocephalic dogs is the olfactory
bulbs and peduncles, however, the rest of the endocast
morphology also reported a variance in shape that is corre-
lated with CI. These conclusions are consistent with previ-
ous studies reporting a change in neuroanatomy that is
the result of modern breeding practices (Datta et al., 2012;
Roberts et al., 2010).
The differences in olfactory neuroanatomy between
brachycephalic and normocephalic dogs coincide with the
established understanding that brachycephalic dogs are
worse at odor-discrimination tasks than normocephalic
dogs. Although there are some studies that support the idea
that normocephalic dogs are better smellers (e.g., Polgár,
Kinnunen, Újváry, Miklósi, & Gácsi, 2016), another study
complicates this assumption by demonstrating that pugs
outperformed German shepherds in the study of Hall,
Glenn, Smith, & Wynne (2015). Roberts et al. (2010)
12
FIGURE 9 Boxplots of surface area (a), volume (b), and surface area: volume (c) values in the normocephalic (n = 25) and
brachycephalic (n = 32) endocasts. (a) The dogs in this sample did not have a statistically significant difference in the surface area of their
endocasts (p = .57). (b) There was no statistically significant difference in the volume of their endocasts (p = .070). (c) Brachycephalic dogs
have a significantly lower surface area: volume ratio than normocephalic dogs (p < .001). Note that brachycephalic dogs also have a wider
range of ratios than normocephalic dogs
suggest that maybe it is the reorganization of the brain of
the brachycephalic dogs, which includes a compression of
the cranium and subsequent repositioning and compres-
sion of the olfactory lobe, that might be responsible for the
seemingly poor olfaction in these types of dogs. Instead of
just their physically shortened noses or crowded nasal
turbinals alone, the significant reduction in brain matter
devoted to olfaction in brachycephalic dogs could explain
why they have been found to perform poorly on odor dis-
crimination tasks (Polgár et al., 2016). In that case, their
reduced olfaction would be directly tied to the neurological
capacity for olfaction instead of the functional anatomy of
the nose.
Beyond the changes in the olfactory neuroanatomy,
the rest of the brain also experiences a spatial reorganiza-
tion as a result of selective breeding practices. Since
many of the different gyri and sulci of the canine brain
often correspond with specific functions (e.g., the middle
ectosylvian gyrus corresponds to auditory capabilities;
Evans & De Lahunta, 2013), it begs the question: how did
this spatial reorganization of the domestic dog brain
impact function and behavior, if at all? Some recent stud-
ies have pointed out potential differences in behavior that
are largely attributed to changes in CI. Stone, McGreevy,
Starling, & Forkman (2016), for example, attribute the
more forward-facing eyes and greater central visual
acuity of brachycephalic dogs to their lack of abilities
for detecting horizontal motion, thus making them less
inclined to demonstrate hunting behaviors. Dolichoce-
phalic dogs, in contrast, have a better ability to scan the
peripheral visual field while hunting, thus making them
better at chasing prey and more inclined to display hunt-
ing behaviors (Stone et al., 2016). McGreevy, Grassi, &
Harman (2004) also noted a difference in peak ganglionic
cell density that was highly correlated with skull length.
This, in addition to the presence of eyelids with less lat-
eral apertures, have produced a more pronounced area
centralis in brachycephalic dogs.
SELBA ET AL.
Research by Stone et al. (2016) tested a myriad of
behaviors to see if there was any correlation with CI.
They found that many behaviors did correlate with CI,
including possessiveness over a toy (with the higher CI
dogs being more possessive) and certain behaviors when
offered the same toy more than once (with dogs with a
high CI showing an increased desire to retain a toy when
it was offered for a second time). In another study, Gácsi
et al. (2009) found that brachycephalic dogs are better at
utilizing the human pointing gestures than dolichocephalic
dogs. Clearly, these studies point to some evidence of a
connection between CI and domestic dog behavior.
Despite these indications that there may be some
aspects of behavior that do correlate with CI, there may
not be a simple relationship between the two. McGreevy,
Brueckner, Thomson, & Branson (2010) found no associa-
tion between breed and laterality of paw use. Addition-
ally, Stone et al. (2016) found that body size and weight
might also be a predictor of behavior instead of (or in
addition to) CI. It is possible that changes in neuroana-
tomical configuration have not had an overwhelming
effect on the behavior of domestic dogs as a result of neu-
roplasticity. Neuroplasticity is the ability of the brain to
change throughout an individual's life. The malleability of
the brain has been observed in a variety of species includ-
ing dogs and humans in both developmental and clinical
contexts (Grafman, 2000; Lillard & Erisir, 2011; Nudo &
McNeal, 2013). According to Grafman (2000), one form of
neuroplasticity is homologous area adaptation. This type
of neuroplasticity is based off the premise that if a particu-
lar portion of the brain is compromised, the cognitive
operations that reside there can be compensated for by
shifting those operations to other brain areas that do not
include the impacted region. Several comparative studies
have assessed neuroplasticity in brachycephalic breeds
and found that they retain an early ontogenetic stage in
cranial development (Oechtering et al., 2016) as well as
juvenile behavior (McGreevy et al., 2013). Future studies
SELBA ET AL.
that include endocasts of neonate and juvenile dogs could
provide further evidence for neuroplasticity in brains of
domestic dogs.
The plastic nature of the brain is also the reason that
pathological conditions such as craniosynostosis conditions
and cultural practices in humans such as head binding can
occur without causing cognitive deficits (Aldridge et al.,
2005; Roberts et al., 2010; Tubbs, Salter, & Oakes, 2006).
Roberts et al. (2010) suggest that these conditions highlight
the fact that the development of the shape and size of the
brain are closely related to the configuration of the dura
mater and the co-developing cranial vault. Additionally, by
studying unicoronal synostosis, Aldridge et al. (2005) found
a large degree of developmental independence between
brain and skull. Thus, with changes in the shape of the
cranium vault in the adult form (e.g., through selective
breeding practices in dogs), there can be changes to the
morphology of the skull that can then impact the neuro-
anatomy just deep to it without impairing function.
Despite the potential value of studying endocasts, there
are limitations to what we can learn from them as they
only imperfectly estimate the underlying neural tissue.
For example, Selba et al. (2020) observed the presence of
a distinct keyhole defect in many of the brachycephalic
dogs in this sample. Occipital bone hypoplasia is a well-
documented neurological pathology that is common in
many toy breeds, especially in the Cavalier King Charles
Spaniel (Rusbridge & Knowler, 2003; Rusbridge &
Knowler, 2004). This defect is also represented in the endo-
casts of those dogs; however, one cannot infer from the
endocast that neural tissue is displaced (e.g., herniated)
through the cranial defect. It is possible that the bony
defect is filled by connective tissue that is sufficient to sup-
port the neural tissue but not dense enough to appear in
the CT image (Cagle, 2010). It is for this reason that infer-
ences from endocasts about neural tissue effects must be
made with caution and may not be suitable to support the
diagnostics and treatment of this and other cephalic
diseases.
This project is the first to collect 3D landmarks from
the digital endocasts for a number of breeds and by doing
so, serves to answer many of the questions overlooked
by previous research into the bony canine neurocranium.
By assessing the effects of selection for facial reduction
through the soft tissue analysis of domestic dogs, we can
better understand how modern breeding practices have
not only changed their crania, but also how they impacted
the soft-tissue brain that it houses. The use of endocasts
allows us to investigate the neuroanatomy of dogs in this
previously-researched sample from CT scan data alone.
The results of this project can shed light on cranial devel-
opment in dogs as well as the interplay between soft tissues
and the bony cranium as a whole and can help us better
13
understand the short faced morphotype seen in dogs. The
study of facial reduction in dogs may further elucidate the
growth processes of cranial development, many of which
might also apply to primates. The phenomenon of facial
reduction as it exists in both taxa will be the subject of
future research.
ACKNOWLEDGMENTS
We gratefully acknowledge Dr. Gerhard Oechtering and
the staff at the University of Leipzig for scanning many
of the specimens used in this study. Our thanks to Drs.
Kalman Czeibert and Vicente Aige Gil for their valuable
feedback on the placement of landmarks on the endo-
casts. We are also grateful to AR Associate Editor
Dr. Timothy Smith and three anonymous reviewers for
helpful advice that greatly improved the manuscript.
ORCID
Molly C. Selba https://orcid.org/0000-0003-4022-3172
Valerie B. DeLeon https://orcid.org/0000-0001-5004-
5977
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Additional supporting information may be found online
in the Supporting Information section at the end of this
article.
How to cite this article: Selba MC, Bryson ER,
Rosenberg CL, Heng HG, DeLeon VB. Selective
breeding in domestic dogs: How selecting for a
short face impacted canine neuroanatomy. Anat
Rec. 2020;1–15. https://doi.org/10.1002/ar.24471