Zoological Journal of the Linnean Society, 2008, 153, 187–211. With 12 figures
Shape variation in the mole dentary
(Talpidae: Mammalia)
EUGENIE BARROW1* and NORMAN MACLEOD2 FLS
1
2
Department of Earth Sciences, University of Oxford, Parks Road, Oxford OX1 3PR, UK
Department of Palaeontology, Natural History Museum, Cromwell Road, London SW7 5BD, UK
Received 11 April 2006; accepted for publication 6 July 2007
The clade Talpidae consists of specialized fossorial forms, shrew-like moles and semi-aquatic desmans. As with all
higher jawed vertebrates, different functional, phylogenetic and developmental constraints act on different parts
of dentary influencing its shape. In order to determine whether morphological variation in the dentary was unified
or dispersed into an integrated complex of structural–functional components, a morphometric analysis of the mole
dentary was undertaken. The dentary was subdivided into component parts – horizonal ramus; coronoid, condylar,
angular processes of the ascending ramus – and outline-based geometric morphometric methods used to quantify,
compare and contrast modes of shape variation within the clade. These were successful in revealing subtle
differences and aspects of shape important in distinguishing between mole genera. Closer examination of shape
variation within the two fully fossorial mole clades (Talpini and Scalopini) revealed several similarities in
ascending ramus shapes between genera from each clade. For example, the broad, truncated appearance of the
coronoid process in the talpine genera Talpa and Parascalops was shared with the scalopine genus Scapanus. Also,
the more slender, hook-shaped coronoid process of Euroscaptor and Parascaptor (Talpini) closely resembles that of
Scalopus (Scalopini). Interestingly, subspecies (one from each clade) more closely resembled genera other than their
own in coronoid process shape. Important distinctions in horizontal ramus shape were found to exist between the
two clades, such as the extent of curvature of the ventral margin and relative depth of the horizontal ramus.
Results show shape variation in this region is correlated with dental formulae and the relative sizes of the teeth.
The taxonomically important dentition differences characteristic of mammals are also reflected in the horizontal
ramus results. Moreover, these results suggest size may be affecting shape and the extent of variation in, for
example, the coronoid and condylar processes between the semi-aquatic moles Desmana and Galemys. It is likely
that the effects of morphological integration seen at this level of analysis – covariation between shapes of dentary
components – may exist because interacting traits are evolving together. Horizontal ramus and coronoid process
shape, for example, are similar across Scapanus and Parascalops, but both these shapes have diverged in
Scalopus. © 2008 Trustees of the Natural History Museum (London). Journal compilation © 2008 The Linnean
Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211.
ADDITIONAL KEY WORDS: ascending ramus – desmans – eigenshape analysis – fossoriality – horizontal
ramus – morphology – morphometrics – relative warp analysis – shrew moles – Talpinae.
INTRODUCTION
The analysis of shape is important for understanding
patterns of morphological evolution. Variation in
shape across taxa, clades, groups and/or samples may
result from many different factors such as response to
*Corresponding author.
E-mail: [email protected]
selective pressures, different functional roles, changes
in developmental processes and even disease or injury
(e.g. Zelditch et al., 2004). Shape has long been used
to describe and classify taxa and often provides useful
characters for phylogenetic studies. Improved understanding of shape variation may help to resolve taxonomic problems and may provide a method for finding
new phylogenetic characters (see MacLeod, 2002).
Studies of shape variation may also reveal the effect
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
187
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E. BARROW and N. MACLEOD
of ecological factors or developmental processes that
override phylogenetic signal and how such demands
limit or direct evolutionary change (e.g. Björklund
& Merilä, 1993; Schluter, 1996; Hallgrímsson et al.,
2005; Klingenberg, 2005). Unfortunately, finding
appropriate shape-based features that support good
group characterization and interspecies discrimination, and finding useful ways of describing those features is not always easy (Costa & Cesar, 2000).
Morphological examination may sometimes be more
instructive if it concentrates on substructures rather
than the structure as a whole as it is often small
aspects of the object that are important phylogenetically or taxonomically. Quantitative analyses can be
applied to parts of a structure, in separate analyses,
thereby retaining geometric information that would
otherwise be lost if the whole structure were examined in a single analysis (MacLeod, 2002). Considering the complete structure in a single analysis will
produce more generalized results and may obscure
important patterns of regional shape differentiation.
This is most likely to be a problem if the taxa under
study are closely related or only subtle differences
exist between individuals. Moreover, morphometric
analysis of small sets of landmarks scattered over
a shape, while sufficient for examining questions
related to the relative position of substructures across
a sample, often fail to capture shape differences existing among corresponding substructures themselves.
THE
MAMMALIAN DENTARY
The mammalian mandible is a complex morphological
structure that consists of two symmetrical dentary
bones. Several studies of mandibular morphological
variation have been performed (e.g. Atchley et al.,
1992; Atchley, 1993; Cheverud, 1996; Humphrey,
Dean & Stringer, 1999; Duarte et al., 2000; Badyaev
& Foresman, 2004; Hylander, 2005; Monteiro, Bonato
& dos Rees, 2005; Rees, 2005). Examination of
rodents has revealed parts of the dentary that are
more or less variable than others, but these findings
are based on relative landmark positions for the
whole dentary (Klingenberg, Mebus & Auffray, 2003;
Monteiro & dos Reis, 2005).
The dentary can be divided into different regions
(Fig. 1). The horizontal ramus supports the teeth and
the ascending ramus provides attachment sites for
several masticatory muscles (Hildebrand, 1982). The
ascending ramus consists of three processes. The temporalis muscle inserts onto the coronoid process and
the masseter and medial pterygoid muscles onto the
angular process. The condylar process provides an
attachment site for the lateral pterygoid muscle as
well as articulating with the cranium. These regions
also correspond to the morphogenetic components
described by Atchley & Hall (1991).
Figure 1. Regions of the mammalian (talpid) dentary.
Variation in dentary form arises from changes in
the development of its components, and variability in
the patterns of integration between those components
into a functioning complex structure (Atchley, 1993).
Development of the ascending ramus is governed by
the density of mesenchymal condensations (from the
neural crest cells in embryonic stages of development,
see Atchley et al., 1992) followed by development of
the associated muscles, whereas the horizontal ramus
is mostly dependent on tooth development (Cheverud,
1996). The adult form of the mandible therefore
results from interactions between these functional
and developmental processes. However, the extent to
which these factors interact may vary. For example,
the effect of a particular muscle on the ascending
ramus only determines the form of the individual
process to which the muscle attaches (Hall, 2003).
Nevertheless, the structure as a whole must be able
to perform effectively and at some level these processes must be integrated. Allometric effects, as well
as external factors (e.g. diet and food acquisition), will
also contribute towards functional needs. The evolutionary history of a group represents a combination of
these functional–developmental factors and factors
imposed by the group’s ancestry.
Moles are a diverse group with complex phylogenetic history. Here we consider the question of
whether shape variation occurs to different extents in
individual parts of the mole dentary, in the hope of
distinguishing between those regions primarily influenced by taxonomic/phylogenetic factors and those in
which other factors (e.g. functional and size differences) may be predominant. As the mole clade
contains two fully fossorial subgroups we will also
examine questions relating to the existence and
extent of intraclade functional convergence and/or
phylogenetic unity at a variety of organizational
levels within the overall dentary structure.
THE TALPIDAE
Diverse lifestyles have evolved among the Talpidae.
They are distributed throughout Eurasia and North
America and include species that are ambulatory
(the shrew-like moles), semi-aquatic (desmans), semi-
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
SHAPE VARIATION IN THE MOLE DENTARY
189
Table 1. Groups within the Talpidae, their functional category and distribution
Subfamily
Tribe
Genus
Common name
Functional category
Distribution
Asiatic shrew moles
Russian desman
Pyrenean desman
Star-nosed mole
Ambulatory
Semi-aquatic
Condylurini
Uropsilus (4)*
Desmana (1)*
Galemys (1)*
Condylura (1)*
Eurasia
Eurasia
Eurasia
N. America
Scaptonyx (1)*
Urotrichus (1)*
Dymecodon (1)
Neurotrichus (1)*
Scalopus (1)*
Scapanus (3)*
Parascalops (1)*
Scapanulus (1)
Talpa (9)*
Euroscaptor (6)*
Mogera (5)*
Parascaptor (1)*
Scaptochirus (1)
Long-tailed mole
Japanese shrew moles
Japanese shrew moles
American shrew moles
Eastern American mole
Western American mole
Hairy-tailed mole
Gansu mole
Old World moles
Southeast Asian moles
East Asian moles
Indian mole
Short-faced mole
Uropsilinae
Desmaninae
Talpinae
Scaptonychini
Urotrichini
Neurotrichini
Scalopini
Talpini
Semi-aquatic/
semi-fossorial
Semi-fossorial
Semi-fossorial
Fully fossorial
Fully fossorial
Eurasia
Eurasia
Eurasia
N. America
N. America
N. America
N. America
Eurasia
Eurasia
Eurasia
Eurasia
Eurasia
Eurasia
Taxonomy at the genus level follows Hutterer (2005) and includes Nesoscaptor within Mogera (Motokawa et al., 2001).
*Genera from which one species is represented in this study.
Numbers in parentheses indicate the number of species in each genus.
fossorial (shrew moles) and fully fossorial (Hutchison,
1976; Yates & Moore, 1990). Talpids are largely
faunivorous, but to varying degrees depending on
their habitat. Aquatic forms consume small crustaceans and fish whereas terrestrial forms concentrate,
to different degrees, on worms, insect larvae and
other small invertebrates (Raw, 1966; Nowak, 1999;
Silcox & Teaford, 2002).
There are 17 recognized extant talpid genera and
approximately 42 species (Nowak, 1999), separated
into several clades (Table 1). The Talpinae form the
largest group within the Talpidae and include both
fossorial and semi-fossorial moles. Shrews and hedgehogs are thought to be the most likely talpid sister
groups, and together these three groups form the
clade Eulipotyphla (Waddell, Okada & Hasegawa,
1999; Asher, Novacek & Geisler, 2003).
Recent phylogenetic studies have been based on
both morphological and molecular data and concur
that Uropsilus is the most basal talpid genus (Hutchison, 1976; Whidden, 2000; Motokawa, 2004; Cabria
et al., 2006; Sánchez-Villagra, Horovitz & Motokawa,
2006). However, the position of other groups within
the clade is less certain. For example, there is inconsistency in the relationship between the shrew moles
Urotrichus and Neurotrichus (from Japan and North
America, respectively; see Moore, 1986; Whidden,
2000; Shinohara, Campbell & Suzuki, 2003) and the
relationships between and within the two fully fosso-
rial clades, Talpini and Scalopini (Rohlf, Loy & Corti,
1996; Okamoto, 1997; Shinohara et al., 2004). The
most recent comprehensive talpid cladogram is that of
Sánchez-Villagra et al. (2006; Fig. 2). This is based on
a maximum-parsimony analysis of 157 morphological
characters and is an extension of Motokawa’s (2004)
research on talpid phylogenetics.
The fully fossorial lifestyle most likely evolved from
semi-fossorial moles, but uncertainties in their phylogenetic relationships have triggered some debate as
to whether it evolved in a single evolutionary step
(Whidden, 2000) or as a result of parallel adaptations
(Motokawa, 2004). The fully fossorial clade Talpini
ranges throughout Eurasia while the Scalopini is
known mostly from North America (one genus,
Scapanulus, appears endemic to China but only a few
specimens have been found to date). Sánchez-Villagra
et al. (2006) argued that the monospecific genus
Scaptonyx was sister group to the Talpini clade.
Nowak (1999) points out that little is known about
this mole but it is thought to be semi-fossorial, indicating that the fully fossorial lifestyle evolved at least
twice (Motokawa, 2004; Sánchez-Villagra et al., 2006).
Morphological studies have identified characters
of the dentary used in talpid phylogenetic studies,
for example by Motokawa (2004: characters 51–55).
These have also been used in species descriptions.
True (1896) described the form of the coronoid and
angular processes and features of the horizontal
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
190
E. BARROW and N. MACLEOD
ling 14 out of the 17 extant genera recognized in the
current taxonomy (see Table 1). Sample sizes for each
genus varied from three to 15 individuals. Specimens
used came from the mammalogy collections at The
Natural History Museum, London (BMNH), and the
Museum für Naturkunde, Humboldt University
(MNHU), Berlin. A full list of all specimens used in
this study is available from the senior author on
written request.
METHODS
Figure 2. Phylogenetic relationships among the Talpidae
proposed by Sánchez-Villagra et al. (2006) based on a
maximum-parsimony analysis of 157 morphological characters. Clades indicated (in grey) are discussed in the text
(see also Table 1).
ramus in his review of the American talpid species
and subspecies. A comparative study of the mole
Scalopus aquaticus and the shrew Blarina brevicauda
highlighted important differences in the dentary
(Gaughran, 1954). These include the scoop-like
angular process of Scalopus (monospecific) compared
with the narrow, spicular angular process of Blarina
brevicauda and the larger, heavier condylar process
but thinner coronoid process in the Scalopus as
compared with the shrew Blarina brevicauda.
Dental characters have also been used as a source
of information in talpid phylogenetic and taxonomic
studies. Absence of the lower canine in the East Asian
mole genus Mogera distinguishes them from the Old
World moles Talpa, with which they were once
included (Nowak, 1999). Ziegler (1971) examined how
tooth formula differentiations, including fossil talpid
taxa, related to their functional groups/lifestyles. The
effect of variation in dental formula (and tooth size) is
likely to contribute to aspects of the dentary form,
particularly the shape of the horizontal ramus.
MATERIAL AND METHODS
MATERIAL
A total of 124 mole specimens were used in this study.
One species was used to represent each genus, total-
Advances in techniques used to describe and compare
shapes, including imaging and data-acquisition
methods, provide powerful approaches to the study of
morphological variation (Rohlf, 1990). Geometric morphometrics offers an important tool in the analysis of
shape and have been used in biological systematic
and developmental studies (Zelditch et al., 2004).
The most appropriate method depends heavily on the
objects under study. Landmark-based techniques
require selecting discrete points on a form that are
locatable across all specimens comprising a data set
(Bookstein, 1991). Often the number of appropriate
landmark points is limited, particularly if the relationship among the study taxa extends beyond closely
related or intraspecific levels (MacLeod, 1999) and
may result in a highly biased summary of the true
shape variation. When there is a lack of landmarks,
or when the shape of an object’s outline is of interest
rather than its relationship to various landmarks,
outline methods are usefully employed (Rohlf, 1990).
One outline-based method is eigenshape analysis
(MacLeod, 1999). This technique can be used to study
an open curve between two landmarks and, by adding
internal landmarks, can constrain points along a
curve in order to maintain biological correspondence
of landmarks across the shape (extended eigenshape).
The following approach uses outline-based methods
to capture the complexity of the shape of each part of
the talpid dentary (otherwise limited to the small
number of possible landmarks). Standard eigenshape
analysis (MacLeod, 1999) is used to analyse the
outline curves defining each process of the ascending
ramus. In order to include information regarding the
position of the teeth with the horizontal ramus shape,
a combination of outline and landmark data are used
in a relative warp analysis (Rohlf, 2003).
The left dentary of each specimen was photographed in lateral view using a digital camera. If the
left dentary was damaged or not available, the right
was used instead and the image transformed so that
it could be included in the analysis. Left–right asymmetry of the mandible, which undoubtedly exists, is
assumed to be unlikely to affect the results significantly. To standardize the orientation of each object –
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
SHAPE VARIATION IN THE MOLE DENTARY
Figure 3. Landmark locations on a talpid dentary.
Anatomical descriptions of landmarks are as follows
(types correspond to classification of Bookstein, 1991).
(1) Anterior-most point of the dentary where the bone
meets the anterior edge of the first incisor (Type 1). (2)
Maximum curvature on the ventral border between the
angular process and the most ventral point on the horizontal ramus (Type 2). (3) Maximum curvature of the
posterior boundary between the angular process and the
condylar process (Type 2). (4) Maximum curvature of the
dorso-posterior boundary between the coronoid process
and condylar process (Type 2). (5) Point where posterior
edge of the 3rd molar meets the dentary bone, at the base
of the coronoid process (Type 1). (6) Point where anterior
edge of the 1st molar meets the dentary bone (Type 1).
with the lateral surface of the bone facing upwards,
parallel to the camera lens – each was positioned such
that when viewed from a ventral position a horizontal
line could be drawn from the most anterior point of
the dentary to the most posterior point of the condylar
process. Similarly, when viewed from a posterior position the ascending ramus, from coronoid to angular
process, was horizontal. The dentary bone in most
talpids is relatively flat, thus facilitating orientation.
However, in certain individuals the angular process
was slightly medially inverted, making orientation
more difficult.
Dentary (outline) shapes
Outline data were collected from each image using
the Media Cybernetics Image Pro Plus (v. 5.1) and
tpsDig (v. 2.0, Rohlf, 2004) image analysis software
packages. Between 150 and 200 semi-landmark coordinate points were judged to capture the complexity of
each curve and were recorded between selected landmarks representing different parts of the dentary.
Landmarks were chosen to represent skeletal areas
and associated sites of muscle insertion and tooth
development and are described in Figure 3. One Scalopus specimen was damaged at the anterior region of
the horizontal ramus and one Scaptonyx specimen
was missing its angular process. These specimens
were not used in analyses involving those particular
regions of the dentary.
Ascending ramus
The ascending ramus was divided into its three processes. The angular process was characterized by the
191
outline curve between landmarks 2 and 3, the condylar process between landmarks 3 and 4, and the
coronoid process between landmarks 4 and 5. Once
the x,y coordinate points had been collected they were
converted into the f shape functions (Zahn & Roskies,
1972) using the xy-phi program of MacLeod (see
MacLeod, 1999). One hundred evenly spaced coordinate points were specified for each outline segment.
The (unstandardized) f shape functions expressed
as patterns of deviation from the sample means shape
for the three processes were each submitted to standard eigenshape analysis. The between-shapes covariance matrix was used as the basis for the analysis
(rather than the correlation matrix) so the full range
of shape variation observed in the sample was
expressed (see MacLeod & Rose, 1993). The eigenshape analysis is essentially equivalent to a relative
warps analysis of the outputted shape variables
(eigenshape scores) explaining different proportions of
the f shape functions and results include a set of
singular values (expressing the amount of shape
variation represented by each eigenshape vector) and
a set of eigenshape vectors (= eigenshapes) expressing
a set of variance-maximized, composite shapevariation trends that are uncorrelated with each
other. The original mean-deviate shape functions can
then be projected onto these new eigenshape axes to
achieve a low-dimensionality representation of shape
similarity and difference patterns inherent in the
sample.
Ordinations for each process of the ascending
ramus were plotted using the resulting eigenshape
scores to ordinate the distribution of taxa across the
first three shape axes. These ordinations were used to
identify clusters relating to particular taxic groups
and to spot outliers. The mean shape and eigenshape
results for each region of the dentary were then used
to model shape change along each of the resulting
shape variables. Shape modelling procedures are
useful in the interpretation and subsequent analysis
of the eigenshape results and follow the discussion
provided in MacLeod (1999).
Horizontal ramus
The outline curve between landmarks 1 and 2 along
the ventral edge of the horizontal ramus was also
digitized. To include the relative depth of the horizontal ramus in the analysis, landmarks 5 and 6 were
employed. First, the xy-phi program was used to
interpolate 14 evenly spaced semi-landmark points
along the outline between landmarks 1 and 2. The
coordinate points from landmarks 5 and 6 were then
mean-centred and added to the 14 previously meancentred points outputted by the xy-phi program. This
provided a new set of 16 landmark points (12 of which
not strictly landmarks but semi-landmarks) that were
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
192
E. BARROW and N. MACLEOD
used in a relative warp analysis using the software
tpsRelw (Rohlf, 2003). Similar to eigenshape analysis,
the relative warp analysis outputs new shape variables (relative warps) that summarize the variation
among specimens. Thin-plate spine deformations
were then used to visualize changes in shape variation along each relative warp.
Talpini and Scalopini
There is a large representative of fully fossorial moles
in this study. These include four of the five genera
from the Eurasian clade Talpini, and the three North
American genera from the clade Scalopini. Shape
analysis of each part of the dentary was repeated
using just these two fully fossorial clades in order to
examine differences, if any, between genera within
each clade. New shape variables were obtained that
differed from the original set because they only
explained variation within this smaller sample and
were therefore not affected by the greater variation
across the larger group.
Measurement error
Measurement error was assessed following methods
discussed by Arnqvist & Martensson (1998). These
authors stress the importance of calculating measurement error in geometric morphometrics and its
possible sources. Potential sources of error relevant
(or measurable) in this study are largely associated
with personal error, namely orientation of the objects
and selecting landmark positions.
In order to assess measurement error a subset
(N = 6) of representative individuals was selected
from the whole sample. This subset included individuals that had both joined and separate dentary bones
(it was easier to orientate dentaries that were separate) and from within the same and separate genera.
Individual specimens were photographed three times
and outline data were collected from each image for
each region of the dentary. Furthermore, outline data
were recorded three times on the same photograph.
This totalled seven repeated measures for each specimen (one original, three from the same image and
three from separate images). Photographs and outline
data were collected over a 3-week period so that
sequential familiarity factors did not further complicate the analysis.
Shape variables were obtained for each repeated
measure in either eigenshape or relative warp analysis (with the rest of the sample) depending on dentary
region. A one-way ANOVA was performed on each
shape variable explaining up to 90% of the variance
and the repeatability was calculated using Arnqvist &
Martensson’s (1998) equation:
R = S2 A ( S2 W + S2 A )
(1.1)
2
where S A is the among-individual variance component (= (MSamong - MSwithin)/n; n is the number of
repeated measures per individual; and S2W is the
within-individual variance component (= MSwithin).
To compare the effect of error resulting from outline
and landmark selection with that caused by variation
in orientation of each specimen under the camera
lens, two repeatability scores were calculated: R1, the
repeatability of repeated measures for each individual
on the same image; and R2, the repeatability of measures taken from different images of the same individual (and same image).
RESULTS
MEASUREMENT
ERROR
Repeatability scores for shape variables explaining up
to 90% of the variation for each dentary region are
shown in Appendix 1. In each region of the dentary
repeatability values decrease as the percentage of
variation explained by each variable decreases. Generally, repeatability remains high in the first several
shape variables. This is an expected result as the
sample signal-to-noise ratio should be higher for
axes that explain greater proportions of variance.
However, repeatability analysis provides an indication of how far into the eigenshape (and relative
warps) decomposition it is ‘safe’ to go when making
interpretations.
On the whole those variables accounting for less
than 2% contribute to more than 20% of the measurement error (i.e. r < 0.80). Repeatability scores become
increasingly erratic, and below 90% were sometimes negative. The differences between R1 and R2
are minimal, demonstrating that orientation and
landmark/outline collection were equally likely to
affect measurement error. One might expect R1 scores
to be higher, as they were collected from the same
image. However, the outline was sometimes obscured
by associated connective tissue (particular on the
condylar process) or by the presence of the other
dentary bone if the dentaries were attached. Based on
these results we conclude that measurement error
should have a negligible impact on the results
presented below.
DENTARY
SHAPES
The 100 interpolated points along each outline proved
sufficient to achieve at least 90% shape characterization accuracy for the individual processes (coronoid,
condylar and angular) over the entire sample. It is
difficult to picture patterns of shape change along all
these axes, but scatterplots of the first three eigen-
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
SHAPE VARIATION IN THE MOLE DENTARY
shapes (ES-1 versus ES-2 and ES-2 versus ES-3), and
relative warps for the horizontal ramus shape (RW-1
versus RW-2 and RW-2 versus RW-3), enable visualization of the distribution of taxa within a threedimensional shape space. It should be remembered,
however, that a proportion of shape variation remains
undepicted (as much as 38% in the case of the coronoid process) on such plots. Nevertheless, eigenshapes and relative warps subsequent to the first
three were each responsible for a relatively small
proportion of the variation (l ⱕ 10%). In Figures 4–10
and 12 symbol shading corresponds to locomotory/
functional categories (see Table 1): black represents
ambulatory, semi-fossorial and semi aquatic moles,
white represents fully fossorial moles from the clade
193
Talpini and grey represents fully fossorial moles from
the clade Scalopini. Legends for each figure identify
individual genera. Models are used to represent shape
variation along the eigenshape axes and so provide a
generalized baseline for interpreting the geometries
depicted by the shape space.
Coronoid process shape
The first two eigenshapes account for 50.2% of the
variation about the mean shape (ES-1, l = 32.9%;
ES-2, l = 17.3%). Figure 4A shows that, when projected into the two-dimensional space represented by
these axes, the majority of taxa are clustered about
the mean shape (the origin of the coordinate system),
but extend from approximately -0.2 to 0.3 along ES-1.
Figure 4. Distribution of talpid coronoid process outline shape in the ES-1 versus ES-2 (A) and ES-2 versus ES-3 (B)
shape planes and corresponding outline shape models (C and D). l values = percentage variance accounted for by each
axis based on singular values. For symbol shading conventions see text.
© 2008 Trustees of the Natural History Museum (London)
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E. BARROW and N. MACLEOD
This cluster contains the fully fossorial moles (Talpini
and Scalopini clades) plus Urotrichus and Galemys.
Distinct from this group, with ES-1 scores of -0.3 and
lower, are Condylura and Neurotrichus. Uropsilus
and two of the three Scaptonyx specimens also have
relatively low ES-1 scores (the third Scaptonyx specimen is positioned close to the mean shape). Low ES-1
scores are indicative of a coronoid process outline
with a short posterior edge and a top that tapers into
an upward- and backward-pointing ‘tip’ (see models
along ES-1 in Fig. 4C). At ES-1 scores above -0.3 the
posterior edge increases in length and the tip rounds
off and becomes more upright, characteristic of taxa
in the larger cluster.
Condylura and Neurotrichus are also distinct along
ES-2 (Fig. 4A). Condylura has a relatively high ES-2
score (> 0.1), the outcome of a coronoid process that
is more triangular than those represented by lower
scores. The triangular shape results from the proximal ends of posterior and anterior margins extending
away from one another particularly along the anterior
margin to where it meets the tooth row. Like Neurotrichus, Uropsilus and Desmana, both have low ES-2
scores. This is attributable to a narrower, uncinate
(True, 1896) coronoid process (ES-2 < -0.1, see models
in Fig. 4C). Within-genus variation along ES-2 is
quite large in both Condylura (0.10–0.30) and Neurotrichus (-0.34 to -0.12). In each case the specimen
with the highest ES-2 score has a wider, less hooked
coronoid process outline. However, the distribution
along this axis is no greater than in those genera in
the larger cluster (which have larger sample sizes).
The third eigenshape (ES-3) summarizes a further
11.6% of observed shape variance information and is
plotted against ES-2 in Figure 4B. Variation along
ES-3 is largely associated with differences in Condylura compared with the rest of the sample. A low score
(< -0.2) indicates a coronoid process with a short
posterior margin and an irregularly shaped,
backward-directed vergence (as in Condylura). As the
posterior margin lengthens the outline over the coronoid process vergence smoothes and flattens (see
models along ES-3, Fig. 4D).
In order to model shape change within the ES-2/
ES-3 shape plane, variation along ES-1 has been
constrained at the mean shape (ES-1 = 0.0). As
Figure 4C shows, Condylura score particularly low
along ES-1. For this reason models for the region
occupied by Condylura in Figure 4D (positioned at the
mean ES-1 value) exhibit a generalized, but not a
close, representation of the true Condylura outline
shape (see models at top left of Fig. 4D). The apparent
model-reality discrepancy stems from the fact that
the Condylura specimens occupy a mean ES-1 position -0.45, not 0.0, and so occupy a region considerably more remote from the ES-2/ES-3 plane that
served as the basis for models. Moreover, some details
of the geometric distinction between Condylura and
the rest of the taxa used in this analysis are best
expressed on subsequent eigenshapes.
It is apparent in Figure 4B that, within the fully
fossorial clade Scalopini, the genus Scalopus is quite
separate from Parascalops and Scapanus along ES-3.
Similarly, in the Talpini clade Talpa is shown to be
distinct from Euroscaptor and Parascaptor, but overlapping with Mogera, along the same axis. Shape
variation among fully fossorial moles was examined
more closely in a separate eigenshape analysis.
Within the Talpini the distinction between Talpa
and Euroscaptor and Parascaptor remains in the
ES-1 versus ES-2 shape space (shown by the least
convex hulls on Fig. 5A). Mogera specimens in this
study are represented by the species Mogera wogura,
four of which are of the subspecies M. wogura kanai.
As indicated by the dotted line in Figure 5A, these
four specimens have low scores for ES-1 and are close
to the mean shape along ES-2, resembling Talpa,
whereas the rest of the genus Mogera is closer
to Euroscaptor and Parascaptor in this shape space.
A further two Mogera specimens (from MNHU
collection) also resemble Talpa along ES-1 (and are
included within the dotted line), but their subspecies
is unknown. Low ES-1 scores indicate broad, truncated coronoid process outlines. Those with higher
scores are more slender and uncinate and are represented by models in Figure 5E. It is important to note
that these are new eigenshapes and therefore do not
correspond with the models shown in Figure 4C.
Among the scalopine genera (Fig. 5C) Scapanus
and Parascalops are positioned in a region of the
shape space that also contains Talpa. These differ
from one another along ES-2 where Scapanus has a
more concave posterior margin than the straight posterior outline of Parascalops. Scalopus has a high
ES-1 score, closer (in this view of the overall highdimensional shape space) to that of the Talpini genera
Euroscaptor and Parascaptor. The genus Scalopus
is monospecific. One Scalopus aquaticus specimen
included in this study was of the subspecies S. aquaticus machrinus (BMNH: 29.11.7.11). It is more similar
to Parascalops and Scapanus than to the other Scalopus specimens along ES-1. A further two Scalopus
specimens (MNHU A2832.1 and MNHU 13645,
unknown subspecies) share a low ES-1 score with
S. aquaticus machrinus. The position of these three
specimens is indicated by the dotted line on
Figure 5C. The arrow identifies the S. aquaticus
machrinus specimen (BMNH: 29.11.7.11).
There is considerable overlap along ES-3 in both
Talpini and Scalopini clades (Fig. 5B, D). However,
the three Scalopus specimens mentioned above have
relatively high scores along this axis (indicated by
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SHAPE VARIATION IN THE MOLE DENTARY
195
Figure 5. Distribution of coronoid process outline shape among fully fossorial moles in the ES-1 versus ES-2 and ES-2
versus ES-3 shape planes for Talpini (A and B, respectively), Scalopini (C and D) and corresponding outline shape models
(E and F). Least convex hulls show position within the shape space that each genus occupies. Dotted lines/arrows refer
to position of specimens mentioned in the text.
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196
E. BARROW and N. MACLEOD
Figure 6. Distribution of talpid condylar process outline shape in the ES-1 versus ES-2 (A) and ES-2 versus ES-3 (B)
shape planes and corresponding outline shape models (C and D). l values = percentage variance accounted for by each
axis based on singular values. For symbol shading conventions see text.
dotted line on Fig. 5D), and are characterized by a
slight protuberance along the posterior margin of the
coronoid process (see models along ES-3 in Fig. 5F).
This resembles a ‘mammiform tubercle’ seen in the
subspecies S. aquaticus typicus but not usually found
in S. aquaticus machrinus according to True (1896).
Although size was not taken into account, Scalopus
specimens with higher scores along ES-3 (> 0.075)
were noticeably larger than those with lower scores.
Condylar process shape
The outline shape of this process shows no distinct
clustering of taxa in the most information-rich, threedimensional shape space. Instead there is a continuous
pattern of shape change exhibited along each axis
(Fig. 6A). The ES-1 axis represents 60.9% of the shape
variation about the sample mean with ES-2 representing 9.1% of the shape variation. Along ES-1, the
condylar process outline changes from having long
ventral and short dorsal edges at its lowest value
(ES-1 = -0.6, e.g. Uropsilus) to the reverse at its
highest value (ES-1 = 0.45, e.g. Euroscaptor, Fig. 6A).
At both ends of the scale the distal end is narrow, but
between these two extremes – close to the mean shape
– its depth increases and the two edges are more equal
in length (see models in Fig. 6C). Generally the fully
fossorial clades and Condylura and Galemys are
skewed towards high ES-1 values whereas Uropsilus,
Neurotrichus, Urotrichus, Scaptonyx and Desmana are
distributed along the lower end of the scale.
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SHAPE VARIATION IN THE MOLE DENTARY
Those familiar with multivariate ordination analyses will, no doubt, recognize the presence of a strong
‘horseshoe effect’ in the Figure 6A plot (see Greenacre, 1984; Reyment, 1991; Reyment & Jöreskog,
1993). The pattern reflects the existence of a particularly well-structured gradient of shape variation
within the condylar process data set. The Uropsilus
species exhibit condylar morphologies that are very
similar to one another, but very different from the
Euroscaptor species (which are, in turn, similar
among themselves). All other species within this data
set exhibit condylar morphologies intermediate
between these extremes such that essentially all
linear intermediate alternatives have been realized.
As a result, the eigenshape analysis is forced to
represent differences between pairs of Uropsilus and
Euroscaptor species as being subequidistant on the
plot and pairs of intermediate taxa (e.g. Uropsilis–
Urotrichus, Uropsilis–Scalopus. Euroscaptor–Talpa,
Euroscaptor–Desmana) as having well-structured,
intermediate, relative-distance values. This causes
the scores of the extreme morphologies to be ‘pulled’
in along ES-1 like a strung bow (see Greenacre, 1984,
for additional examples and discussion). This particular data set is noteworthy in that extremal morphotypes are represented by small numbers of species
relative to genera with intermediate morphologies. It
may well be the case that this horseshoe primarily
results from this taxonomic discrepancy. Methods
exist to ‘detrend’ such data and so remove the effect,
but these are ad hoc adjustments that may serve to
introduce other, much more difficult to interpret,
artefacts to the result. For the most part we agree
with Reyment & Jöreskog’s (1993) observation that
horseshoe plots tend to ‘frighten’ data analysts more
than they should. The reason for the effect is well
known and taking the time to interpret the pattern
correctly usually leads – as shown above – to a better
understanding of one’s data (see also MacLeod,
2006).
A low ES-2 score (< -0.2) represents a condylar
process outline that is broad and almost rectangular
at its distal end. This characteristic becomes narrow
with a narrow articular point and concave dorsal edge
at higher values (Fig. 6C). Uropsilus and Euroscaptor
have the lowest ES-2 values, but are very different
along ES-1. ES-3 accounts for 6.4% of the shape
variation about the mean shape and largely contributes to variation in the ventral edge of this outline
shape (Fig. 6B, D). Low ES-3 scores indicate a
concave ventral edge (for example in Galemys) while
high scores indicate a convex ventral edge. The dorsal
margin becomes increasingly concave at higher scores
resulting in an ‘upturned’ articular tip. This is most
distinct in (some) Condylura specimens and, to a
lesser extent, in Scaptonyx.
197
Examination of fully fossorial clades in a separate
eigenshape analysis revealed little distinction
between genera (Fig. 7A–D), particularly among
Talpini (shown by overlapping least convex hulls in
Fig. 7A, B). The Scalopini were found to have generally lower scores along ES-1, indicting that the condylar process outline has a longer ventral margin
(Fig. 7C, E) than some Talpini specimens. Although
Parascalops and Scapanus can be distinguished from
one another in the ES-1 versus ES-2 shape space,
Scalopus overlaps both these clusters. On the whole
Scalopus has the highest ES-2 score, representing a
narrow distal end of the condylar process. As ES-2
scores fall it becomes relatively wider in Scapanus
followed by Parascalops. The Scalopus aquaticus
machrinus specimen (BMNH: 29.11.7.11) has a relatively low score along ES-1 and ES-2 positioning it
within the shape space defined by Scapanus (as
labelled on Fig. 7C). Those specimens resembling the
Scalopus aquaticus machrinus specimen in coronoid
process outline shape are not distinguished among
Scalopus in condylar process outline shape. Although
similar geometric interpretation can be made along
these axes (Fig. 7E, F) they differ from those in
Figure 6 because they result from a separate eigenshape analysis.
Angular process shape
Eigenshapes 1 and 2 explain 41.3 and 13.5% of the
observed shape variation about the sample mean,
respectively. The scatterplot of scores along these axes
(Fig. 8A) shows that Condylura and Uropsilus have
high ES-1 scores making them distinct from the rest
of the group. In this case both sides of the process are
approximately equal in length, the dorsal edge is
somewhat concave and the distal end is relatively
narrow (Fig. 8C). Desmana and Galemys cluster
closely to one another and have a positive, relatively
high score along ES-1 and ES-2. This is indicative of
their broad but equal-sided, rectangular-shaped
angular process outline. At lower ES-1 scores the
outline becomes broader and the dorsal edge shorter
than the ventral edge. The distal end is broad (see
models in Fig. 8C). The rest of the taxa are widely
distributed along ES-1 (from -0.4 to 0.35) and ES-2
(from -0.21 to 0.27). Along ES-2 the angular process
outline changes from being narrow and uncinate
(ES-2 = -0.2) – for example in Neurotrichus – to a
broad and rectangular shape (ES-2 = 0.3) characteristic of Scalopus, Desmana and Galemys (see Fig. 8A, C).
ES-3 is responsible for 10.2% of the shape variation
about the sample mean. Positive scores indicate the
angular process outline has a proximal end narrower
or equal to the width of the distal end. The dorsal
margin is concave and the distal end rounded. At
negative ES-3 scores the dorsal margin is straight,
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E. BARROW and N. MACLEOD
Figure 7. Distribution of condylar process outline shape among fully fossorial moles in the ES-1 versus ES-2 and ES-2
versus ES-3 shape planes for Talpini (A and B, respectively), Scalopini (C and D) and corresponding outline shape models
(E and F). Least convex hulls show position within the shape space that each genus occupies. Arrow refers to position of
specimen mentioned in the text.
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SHAPE VARIATION IN THE MOLE DENTARY
199
Figure 8. Distribution of talpid angular process outline shape in the ES-1 versus ES-2 (A) and ES-2 versus ES-3 (B)
shape planes and corresponding outline shape models (C and D). l values = percentage variance accounted for by each
axis based on singular values. For symbol shading conventions see text.
the distal end is flattened and the proximal end is
wide (see models in Fig. 8D). No distinct clusters of
taxa are visible in the plot of ES-2 versus ES-3 in
Figure 8B. Condylura exhibits the highest scores
(ES-3 > 0.2) and Galemys the lowest (plus one Mogera
outlier – see below) (ES-3 < -1).
Differentiation among fully fossorial moles can be
seen in Figure 8A and B and is identified more clearly
following an additional eigenshape analysis on these
groups. Among the talpines, Talpa and Parascaptor
form adjacent clusters within the ES-1/ES-2 shape
space (Figure 9A), but Mogera and Euroscaptor
overlap these groups. The Mogera subspecies
M. wogura kanai are not distinguished from the rest
of the genus along these shape axes, but one other
Mogera specimen (BMNH: 1922.8.24.4) has particularly low scores along each axis (as indicated on
Fig. 9A). This results from a wide, relatively evensided angular process outline shape (see models
in Fig. 9E), resembling that of Galemys (see Fig. 8).
The three scalopine genera form distinct clusters in
this shape space (Fig. 9C). Scalopus is separated
from Parascalops and Scapanus along ES-1. The high
scores in Scalopus are characteristic of a short dorsal
margin and broad distal end to the angular process
outline. Parascalops and Scapanus are distinct along
ES-2. Parascalops (low ES-2) has a broad angular
process with relatively straight sides whereas Scapanus (high ES-2) maintains a broad ‘tip’ but has a
concave dorsal margin. Parascalops fills a shape
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200
E. BARROW and N. MACLEOD
Figure 9. Distribution of angular process outline shape among fully fossorial moles in the ES-1 versus ES-2 and ES-2
versus ES-3 for Talpini (A and B, respectively), Scalopini (C and D) and corresponding outline shape models (E and F).
Least convex hulls show position within the shape space that each genus occupies. Arrow refers to position of specimen
mentioned in the text.
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SHAPE VARIATION IN THE MOLE DENTARY
201
Figure 10. Distribution of talpid horizontal ramus shape in the RW-1 versus RW-2 (A) and RW-2 versus RW-3 (B) shape
planes and corresponding shape models (C and D). l values = percentage variance accounted for by each axis based on
singular values. For symbol shading conventions see text.
space similar to that of the Talpini genera in the plot
of ES-1/ES-2 whereas Scalopus and Scapanus are
positioned outside the Talpini shape space (see
Fig. 9A, C, E). The Scalopus aquaticus machrinus
specimen is not separated from the rest of the
Scalopus sample along any of the three eigenshapes
(Fig. 9C, D). Although there is considerable overlap
between the two clades along ES-3, the Talpini
genera Euroscaptor and Mogera and Scalopini genus
Parascalops have relatively low scores and an
angular process outline that has a longer ventral
margin and greater proximal width than those
genera from each clade with higher ES-3 scores
(Fig. 9B, D, F).
Horizontal ramus shape
The first three relative warps of these data explain up
to 91.1% of the total outline shape variation about the
sample mean. Plots of relative warps 1 and 2 (RW-1,
l = 58.3%; RW-2, l = 23.9%) separate shapes into
tight clusters (Fig. 10A). Galemys and Desmana have
RW-1 scores below -0.07, characterized by a horizontal ramus with a ventral outline that curves upwards
anteriorly. There is little posterior curvature where it
joins the ascending ramus (at landmark 2; see thin
plate spline deformation models, Fig. 10C and the
landmark positions, Fig. 11). Landmarks 5 and 6 (the
molar row) are positioned more posteriorly than in
the mean shape and the distance between them – the
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202
E. BARROW and N. MACLEOD
Figure 11. Horizontal ramus shape showing position of
landmarks (numbered coordinates, see Fig. 3) and semilandmarks (un-numbered coordinates) relating to models
in Figures 10C–D and 12E–F.
length of the molar teeth – is short. Consequently, the
distance along the antemolar region is relatively long.
RW-1 for Condylura is also relatively low (but not to
such a great extent). Fully fossorial and semi-fossorial
moles have similar positions along RW-1. A high RW-1
value (0.07) in Uropsilus is reflected in the relatively
flat anterior ventral margin, short antemolar region
and relatively long molar row length.
Condylura is distinguished from all other genera by
having a RW-2 score well below 0.0 (Fig. 10A). This is
depicted by a long, shallow horizontal ramus along
the anterior ventral margin and an extended antemolar region of the tooth row (see models in Fig. 10C).
The other extreme is seen in Urotrichus and Scalopus. Conversely, these have a deep horizontal ramus
curved upwards anteriorly and a short antemolar
length. This feature separates Scalopus from the rest
of the Scalopini clade and distinguishes between the
semi-fossorial Urotrichus and Neurotrichus genera.
Scaptonyx is closer along the second relative warp to
Neurotrichus than Urotrichus. Within the RW-1/RW-2
shape space Scaptonyx closely resembles the fully
fossorial mole Talpa from the Talpini clade.
Relative warp 3 accounts for 8.9% of the shape
variation about the sample mean in the horizontal
ramus. A high score in Neurotrichus, Scaptonyx and
Parascalops separates them from the Talpini cluster.
Similarly, higher scores among Urotrichus distinguish
them from Scalopus (Fig. 10B). Variation along the
third relative warp is concentrated in the anterior
region of the dentary. At high scores the point where
the dentary bone meets the first incisor (landmark 1)
is positioned below the level of where the dentary
meets the anterior edge of the first molar (landmark
6) resulting in a concave curve along the corresponding ventral edge of the dentary. At low values landmark 1 is positioned above the level of landmark 6
and the ventral edge is less concave (see models in
Fig. 10D).
The two fully fossorial clades are almost completely
separated in the RW-2/RW-3 shape space (Fig. 10B).
This is also apparent in the results of a separate
relative warp analysis performed solely on the fully
fossorial moles. Relatively high scores for RW-1 and
RW-2 among talpine genera distinguish them from
the Scalopini (Fig. 12A, C). Differences result from a
deeper horizontal ramus in Scalopini compared with a
shallow horizontal ramus in Talpini. The Talpini are
tightly clustered but on the whole Euroscaptor and
Parascaptor have slightly higher scores along RW-2
than Talpa and Mogera (Fig. 12A). Higher RW-2
values represent a flatter anterior portion of the
ventral margin compared with the more concave
nature of this margin at lower scores (Fig. 12E).
Within Scalopini, Scalopus is clearly distinct from
Parascalopus and Scapanus in the RW-1/RW-2 shape
space (Fig. 12C). A low score along RW-1 and relatively high score along RW-2 for Scalopus results from
a deep anterior region and straight ventral edge. In
Parascalops and Scapanus the horizontal ramus
has a shallower anterior region corresponding to a
considerable concave curve along the ventral edge
(Fig. 12E). Variation along the third relative warp is
minimal in both fully fossorial mole clades (Fig. 12B,
D). However, Scapanus can be distinguished from
Parascalops. The latter has a relatively greater distance between landmarks 2 and 5 and a longer molar
region, depicted by a relatively low RW-3 (see Figs 11,
12F). Scalopus is less distinct in this regard.
Summary of dentary shapes
Examination of dentary shapes within threedimensional shape spaces defined by various
eigenshape/relative warps axes reveals that shape
variation among genera is least distinct in the condylar process. There is a general pattern across the
shape space defined by the first two eigenshapes of
genera from Uropsilus, the most basal talpid genus,
through the semi-fossorial moles to a culmination of
fully fossorial moles. Genera are more distinct in
their coronoid and angular process outline shapes; for
example, Condylura and Uropsilus are separated
from other taxa along axes explaining the majority of
the variation in these two processes. The coronoid
process shape in the semi-fossorial mole Neurotrichus
is quite different from that of the semi-fossorial genus
Urotrichus, but they do share a closer resemblance in
outline shape of the condylar and angular processes.
Scaptonyx clusters amongst Urotrichus and the fully
fossorial moles in coronoid and angular process
outline shape. The semi-aquatic desmans, Galemys
and Desmana, only cluster with one another in the
shape of their angular process and horizontal ramus.
The Desmana coronoid and condylar processes are
closer in shape to those of Uropsilus and Neurotrichus
whereas Galemys bears a closer resemblance to
the fully fossorial moles. The fully fossorial mole
clades, Talpini and Scalopini, share a similar
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SHAPE VARIATION IN THE MOLE DENTARY
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Figure 12. Distribution of horizontal ramus shape among fully fossorial moles in the RW-1 versus RW-2 and RW-2 versus
RW-3 shape planes for Talpini (A and B, respectively), Scalopini (C and D) and corresponding shape models (E and F).
Least convex hulls show position within the shape space that each genus occupies.
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E. BARROW and N. MACLEOD
three-dimensional shape subspace across each
process of the ascending ramus, though the Scalopini
shape range is often smaller (this could be due to
smaller sample sizes for this clade).
Shape distinctions within the horizontal ramus
shape space are particularly striking. The desmans
are tightly clustered and well separated from the rest
of the taxa, as is Condylura. Talpini forms a tight
cluster that is almost completely separated from
Scalopini. Within Scalopini Scapanus and Parascalops closely resemble one another and are well separated from the Scalopus horizontal ramus shape. Of
the semi-fossorial moles, Urotrichus clusters closely
with Scalopus whereas Neurotrichus clusters with
Parascalops and Scapanus. Scaptonyx more closely
resembles Neurotrichus than Urotrichus in its
horizontal ramus shape.
DISCUSSION
In this study shape variation was explored across
talpid genera by dividing the dentary into separate
morphological units so localized or regional aspects of
shape variation could be studied in isolation. Outlinebased methods proved particularly appropriate as the
shape of each unit could be measured at high resolution. The concave or convex nature of the side
margins of each process, for example, is clearly important in shape characterization between genera, but
these would have gone unnoticed using landmarkbased methods. Problems do arise when using outline
analyses, for example non-correspondence within the
variable sequence. There are strategies that overcome
this to a large extent (e.g. extended eigenshape analysis; see MacLeod, 1999), but in many cases there is no
good information regarding interobject correspondences at this detailed level. Nevertheless, qualitative
taxonomists use outline-based clues to interobject
similarity and difference on a routine basis. Any
method that does not take similar information into
consideration can only be compared with qualitative
assessments/interpretations with difficulty (MacLeod,
2002). In the absence of such information, and especially in cases where detailed information about the
geometric character of outlines is needed, the analysis
of semi-landmarks placed at equally spaced locations
along the outline represents a geometrically rigorous
way of approaching quantitative morphological
analysis.
The relative warp analysis in this study used outline
information combined with landmark data (ventral
margin of the horizontal ramus with position of the
molar teeth) and provides another powerful method for
identifying and characterizing groups. Landmarks
focus on geometric changes in a small number of
discrete (or quasi-discrete) locations on the structure
whereas outline analyses summarize more information about the shape of the structure itself. Thus, in
many landmark analyses structures may appear more
(or less) distinct than they actually are because only a
very small part of the overall geometry is participating
in the analysis. This effect might be partly responsible
for the very tight clustering of taxa in the relative warp
plots for the horizontal ramus results.
The eigenshape and relative warp methods were
also useful because the shape characteristics of each
individual could be projected into the space defined by
the first three covariance-based shape vectors and the
distribution of individual specimens within this
ordination space examined. These ordinations clearly
show that differences exist between genera across
different parts of the talpid dentary. Some regions
show greater variation within genera and considerable overlap between genera along the outline shape
variables than others. Despite this, distinctions
between closely related genera can be made. These
results also demonstrate that common constraints
(e.g. geometric, developmental, functional) and/or
selective pressures appear to be determining the
shape of some parts of the dentary while others have
evolved more independently.
SHAPE
VARIATION
Condylura cristata, the star-nosed mole, differs from
other moles in that it has 22 fleshy appendages on its
muzzle used for navigation and food location
(Catania, 2002). A unique shape also characterizes its
dentary, which is more elongated and slender than
those of other talpids. The foraging apparatus is
thought to have been maximized for exploiting large
quantities of small prey at high speed (Catania &
Remple, 2005). It appears that development of a
unique nasomaxillary articulation and nasolabial
musculature associated with the starry-nose relates
to the evolution of the long proboscis. This has shifted
the plane of the anterior teeth, lengthened the mandibular ramus and weakened the masticatory mechanism (including a reduced size of the temporalis and
masseter muscles) compared with other talpids
(Grand, Gould & Montali, 1998). Correspondingly, our
results show that the Condylura dentary also displays unique outline shapes for each part of the
dentary. Among other moles in this study distinctions
could be made across one or more parts of the dentary
and factors contributing to the similarities or differences are discussed below.
Variation within the horizontal ramus
In this study the horizontal ramus provided the clearest distinction among genera compared with the parts
of the ascending ramus. It appears therefore that
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SHAPE VARIATION IN THE MOLE DENTARY
variation in horizontal ramus outline shape is more
tightly constrained within each genus than parts of
the ascending ramus. Furthermore, variation is not
evident between the (small number of) subspecies
within Mogera and Scalopus, unlike in the outline
shape of parts of the ascending ramus.
Shape of the horizontal ramus is mostly affected by
tooth development (Cheverud, 1996). Inclusion of
dental information has probably strengthened the
discriminant power of horizontal ramus shape in the
distinction between genera in this study. Position and
length of the molar row, and its distance from the
ventral margin (i.e. the depth of the horizontal
ramus), explained a large proportion of the horizontal
ramus variation about the mean shape. There are
also important distinctions in the antemolar formulae
among talpids (Ziegler, 1971) and differences, such as
the number of antemolar teeth or their relative sizes,
appear to determine the depth and curvature of the
horizontal ramus.
Dentition differences coincide with horizontal
ramus shapes found among genera in this study. In
Desmana and Galemys the first two incisor teeth are
large (particularly the second incisor) relative to the
rest of the antemolar dentition and the anterior
region of the horizontal ramus is deep. Similarly,
Urotrichus has an enlarged second incisor (the first is
missing in this genus) and a corresponding deep anterior region of the horizontal ramus. In the latter case,
however, our results indicate the horizontal ramus is
shorter as it supports a reduced number of antemolar
teeth, compared with the full complement held by
Desmana and Galemys (Ziegler, 1971). In Uropsilus
the number of antemolar teeth is also reduced and
the molars occupy the majority of the space along the
horizontal ramus. The anterior region of the horizontal ramus is similarly short but shallower, a result of
the enlarged, procumbent (shrew-like) incisor tooth.
Talpine genera are all characterized by an enlarged
first premolar tooth and small incisor and canine teeth,
unlike Scalopini. Scapanus and Parascalops, within
the Scalopini, have largely unspecialized and uniform
antemolar dentition. These differences appear to be
correlated with the outline shape of the anterior region
of the horizontal ramus. The horizontal ramus shape
in Neurotrichus was found to be similar to those of
Scapanus and Parascalops. Neurotrichus also has relatively unspecialized incisors and canine teeth, but
lacks two premolars (made up for by the remaining two
being relatively larger). The reduced number of antemolar teeth and enlarged second incisor in Scalopus
distinguish it from the other two Scalopini genera and
results in its horizontal ramus shape resembling that
of Urotrichus instead. In Condylura it is not so much
the number or size of the teeth as the substantial
elongation of the anterior region (i.e. antemolar
205
length) of the horizontal ramus that distinguishes this
genus from the rest, presumably relating to unique
features of the upper jaw and cranium.
Variation within the ascending ramus
Greater variation between and within some genera
was found in the outline shape of the ascending
ramus processes than in the horizontal ramus.
Changes in the shape of these parts are initially
determined by the density of mesenchymal condensations during development (Cheverud, 1996) followed
by variation in the development of masticatory
muscles (Atchley et al., 1992).
Outline variation is substantial in the coronoid
process of Mogera, Parascaptor, Scalopus and Urotrichus, both in the broadness of the process as a whole
and in the relative straightness or otherwise of the
posterior margin. Similarly, variation in the angular
process is quite substantial in some talpine genera
and Urotrichus in the width of the process, and the
length and degree of curvature of the dorsal margin.
[Note: potential source of error resulting in variation
in the angular process could be due to the fact that in
some individuals this process is slightly medially
inverted.] Despite variation within these two processes and their subsequent overlap within the threedimensional shape space, some genera were still
clearly distinguishable from the rest of the sample,
occupying their own place within the shape space.
Uropsilus, the most basal member of the Talpidae,
and Condylura both have a distinct angular process
shape. It is narrow and spicular (Gaughran, 1954),
resembling that of outgroup (shrew) taxa. This
feature has been used as a phylogenetic character
(Motokawa, 2004). Uropsilus, Neurotrichus and
Desmana have distinct coronoid process shapes. On
closer inspection of the fully fossorial moles, important distinctions became apparent in the coronoid and
angular process shapes among the Talpini and Scalopini genera. It is interesting to note the variation in
the coronoid process between subspecies of the same
species, and the extent of variation between subspecies could be examined further in a larger study. Some
specimens in the present study resembled the identified subspecies along measurements characterizing
coronoid process shape. One could tentatively assign
these individuals to the relevant subspecies, but to
determine this confidently would require additional
information not available (e.g. locality data).
The relationship between bone morphology and
muscle attachment has been known for some time
(Slijper, 1946; Grüneberg, 1952; Atchley & Hall, 1991).
The muscles that attach onto the ascending ramus
processes (see Introduction) are developmentally
linked and each underlying morphogenetic component
of the dentary is governed by relatively independent
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
206
E. BARROW and N. MACLEOD
direct genetic or epigenetic control. Hall (2003) showed
how congenital absence of the lateral pterygoid muscle
resulted in the condylar process failing to form but had
no effect on the other parts of the dentary. This might
explain the greater variation among genera in parts of
the ascending ramus than the horizontal ramus, if
during development additional factors ‘allow’ for
greater shape change in the processes.
Continuous distribution of genera along variables
representing the outline shape of the condylar process
shape (i.e. lack of any distinct groups) was found.
Even Condylura could not be clearly distinguished
along the first three eigenshapes for this outline.
Unlike other morphogenetic regions of the mammalian dentary the processes are capable of forming
specialized cartilage that is later replaced by endochondral bone (Hall, 2003). Therefore, in the condylar
process, for example, the basal portion forms by
intramembraneous ossification whereas the distal
end forms by development of the cartilage (known as
condylar cartilage). Similar, but more transitory cartilage is found on the angular and coronoid processes
(Hall, 2005). Development of the cartilage results
from supplementary growth in response to local
factors (i.e. mechanical factors such as strains and
stresses and muscle development) (Tomo, Ogita &
Tomo, 1997). The condylar process also articulates
with the cranium forming the temporomandibular
joint, and complex adaptive and compensatory growth
takes place in order to maintain this joint. It is
possible that this additional function and prolonged
development of condylar cartilage may restrict variation among talpid condylar process outline shape compared with the coronoid and angular processes.
SHAPE
AND PHYLOGENETIC RELATIONSHIPS
The semi-aquatic desmans, Desmana and Galemys,
undoubtedly form a monophylum as found in phylogenetic studies (Hutchison, 1976; Whidden, 2000;
Shinohara et al., 2003; Sánchez-Villagra et al., 2006).
Nevertheless, differences among their dentaries were
found and may result from a number of factors during
a separate evolutionary history of several million
years. This investigation has documented greatest
similarities in aspects of shape characterizing the
angular process and horizontal ramus. The outline
shapes of the condylar and coronoid processes were,
however, quite distinct; Galemys more closely
resembles the shape seen in the fully fossorial moles.
Similarity in the shape of the horizontal ramus is not
surprising given their dentition (see above). It is
possible that some other underlying factor has preserved the shape of the angular process and independent evolution of the coronoid and condylar process has
been occurring since the time the two lineages split.
Although size variation was excluded from our analysis, Desmana is clearly larger than Galemys. Size could
be constraining some aspects of the desman dentary.
The coronoid and condylar processes of Galemys more
closely resemble the outline shape of more similarly
sized, fully fossorial moles, suggesting that size has
acted on the evolution of the shape of these two
processes. Determining whether this is the case would
require examination of fossil Desmaninae species
(e.g. Desmagale & Mygalea; Hutchison, 1968, 1974).
Older considerations of talpid phylogeny hypothesized that the two semi-fossorial shrew moles
(Neurotrichus and Urotrichus) were sister groups
(Van Valen, 1967; Yates & Moore, 1990; Whidden,
2000). This analysis found that coronoid process and
horizontal ramus shape between these two genera are
quite distinct, supporting more recent phylogenetic
hypotheses that these two genera are not closely
related (e.g. Shinohara et al., 2003, 2004; SánchezVillagra et al., 2006; NB: given the variability in the
coronoid process shape the horizontal ramus provides
better ‘support’ for this). Sánchez-Villagra et al. (2006)
placed the Japanese shrew mole, Urotrichus, most
basal after Uropsilus and before the desmans while
Neurotrichus formed a sister group relationship with
the rest of the taxa (Scalopini, Talpini, Scaptonyx and
Condylura). Judging by the appearance of the shapes
of the ascending ramus in this study Urotrichus more
closely resembles the Talpini and Scalopini clades
than does Neurotrichus. However, in the shape of
the horizontal ramus Neurotrichus more closely
resembles the fully fossorial moles (excluding Scalopus – see below), particularly to Scapanus and Parascalops, and relates to greater similarities in their
dentition compared with Urotrichus.
The presumed semi-fossorial mole Scaptonyx has
been described as ‘[looking] like a mole with the feet
of Urotrichus, or like a Urotrichus with the head of a
mole’ (Allen, 1938: 66; ‘mole’ refers to a talpid adapted
to fossorial life in this instance). Hutchison (1968)
described a talpine appearance of the Scaptonyx lower
antemolars. Furthermore, the third incisor is sometimes missing (Ziegler, 1971), as in Mogera. Given
these facts it is not surprising that the Scaptonyx
horizontal ramus shape resembles that of the Talpini.
However, Scaptonyx also shows a close phenetic affinity with the American shrew mole, Neurotrichus, and
the American (fully fossorial) moles Scapanus and
Parascalops, in horizontal ramus shape. Scalopus has
changed considerably in relation to Scapanus and
Parascalops and has the most reduced antemolar
dentition of all known scalopine moles (Ziegler, 2003).
Sánchez-Villagra et al. (2006) positioned Scaptonyx as
sister group to the Talpini (suggesting that the fully
fossorial lifestyle evolved twice), forming a clade that
is in turn sister group to the Scalopini (see Fig. 2).
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
SHAPE VARIATION IN THE MOLE DENTARY
However, they recognized that this grouping was
weakly supported and required further testing.
The two fully fossorial clades could only be fully
distinguished from one another based on horizontal
ramus shape. It is important to note that in different
parts of the ascending ramus there are shape ‘equivalents’ in each clade. For example, the Parascalops
and Scapanus coronoid process and angular process
outline shape is similar to that of Talpa whereas the
coronoid process shape of Scalopus resembles the other
talpine genera (although its angular process does not).
Note, this difference could be interpreted as arising
due to chance (there are smaller sample sizes of
scalopine genera) or it could be a consequence of other
factors causing similar patterns of morphological
divergence among closely related talpids, such as
character displacement (e.g. Dayan & Simberloff,
1994) resulting in similar radiation patterns. Additional investigation will be needed to resolve this issue.
A clade consisting of Scalopus and Scapanus has
been strongly supported by numerous analyses
(e.g. Hutchison, 1976; Whidden, 2000; Shinohara
et al., 2003, 2004; Motokawa, 2004) and Parascalops
as sister group to them (Yates & Moore, 1990;
Shinohara et al., 2003, 2004). In outline morphology
parts of the Scapanus dentary are more similar to
Parascalops than to Scalopus along axes explaining
the majority of the variation (except in characteristics
of the angular process shape where Scapanus and
Scalopus are both distinguishable from Parascalops).
The Scalopus subspecies S. aquaticus machrinus
more closely resembles Scapanus than the rest of the
Scalopus specimens in aspects of coronoid and condylar process shape. Obviously, this observation is based
on only one specimen of this subspecies and so should
be treated with caution. Scalopus specimens previously mentioned that share similar coronoid process
shape characteristics with S. aquaticus machrinus do
not do so in condylar process shape. They are,
however, all of a similarly larger size than the rest of
the Scalopus sample. S. aquaticus machrinus is the
largest of the Scalopus subspecies (True, 1896). Scalopus has the largest range of any of the scalopine
moles (Yates & Schmidly, 1978) and, like Parascalops,
is from eastern North America whereas Scapanus is
restricted to the west coast. The Scapanus species
used in this study (S. townsendii) is the largest of the
three Scapanus species and is noticeably larger than
the more similarly sized Parascalops and Scalopus.
Sánchez-Villagra et al. (2006) hypothesized Talpa
as the sister group to a Mogera–Scaptochirus (not
used in this study) clade, followed by Euroscaptor and
Parascaptor. Measurements characterizing variation
among structures examined resulted in different
degrees of overlap in the pattern of variation between
these genera. For example, variables accounting for
207
angular process shape distinguished between Talpa
and Mogera, but variation in Euroscaptor and Parascaptor overlaps these two genera. Talpa can be
distinguished from the other three talpine genera
(except for the Mogera subspecies M. wogura kanai)
in the coronoid process shape. As mentioned above,
differences within subspecies suggest important
variation may also be evident at the species level. A
greater degree of overlap of shape measurements
among Talpini genera than Scalopini genera may be
partly due to smaller sample sizes in the latter.
In their study of morphological evolution in the
mandible of spiny rats, Trinomys (Rodentia: Echimyidae), Monteiro & dos Reis (2005) found that coronoid
process shape exhibited the greatest conservatism
during genetic divergence – the coronoid process was
responsible for shape differentiation between two
clades. Although the most basal genus Uropsilus is
fairly distinct in the coronoid process shape, Urotrichus and Galemys share a similar shape space with
the two fully fossorial clades to which they are not
closely related. Despite this there is subtle variation
among closely related genera (e.g. within Scalopini) in
addition to possible differences between subspecies.
The coronoid process plays a more dominant functional role in the mole dentary than in the rodent
dentary, which might explain the overlap of coronoid
process outline shapes between mole genera that are
not closely related. Among moles, movements are
mostly governed by the temporalis muscle pulling on
the relatively large coronoid process. But in rodents
the coronoid process is small and dentary movements
are dominated by action of the medial pterygoid and
masseter muscle on the angular process. The less
significant functional demands on the rodent coronoid
process might explain why this part of the dentary in
rodents is most closely associated with common
descent (Monteiro & dos Reis, 2005). Convergent morphologies are likely to confuse phylogenetic signal
and, as has been shown in carnivoran tarsal morphology, younger clades that have not had time to diverge
may not be affected by convergence (Polly, 2008).
Scalopini and Talpini clades probably diverged before
the Miocene (M. R. Sánchez-Villagra & E. C. Barrow,
unpubl. data) allowing substantial time for the morphospace to be explored. However, some genera
within each of these two clades and their subspecies
may have diverged more recently. It is tempting to
speculate that this might explain why shape differences are apparent at this level, but the entire question needs further investigation.
Another factor that might be important in determining shape variation in different parts of the
dentary could relate to morphological integration and
modular organization within this structure. Traits
interacting during development or function tend to
© 2008 Trustees of the Natural History Museum (London)
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208
E. BARROW and N. MACLEOD
be inherited together and therefore evolve together
(Olson & Miller, 1958; Cheverud, 1996). Functional
interactions between parts may affect performance
of the dentary, or developmental interactions may
occur during dentary formation. When integration is
stronger between some subsets of traits than others
they form ‘quasi-independent’ modules (Schlosser &
Wagner, 2004). An example might be the horizontal
ramus and coronoid process outline shape differences
in Scalopus compared with those of Scapanus and
Parascalops. The latter two genera closely resemble
one another in these parts of the dentary, but
Scalopus differs in both parts and it is possible that
the shape of one is, to a certain extent, dependent on
the other in order to function sufficiently.
Modules exist at different organizational levels
within an organism and their independence depends
on the level at which they are delimited (Bolker, 2000;
Duarte et al., 2000; Klingenberg et al., 2003; Klingenberg, Leamy & Cheverud, 2004; Hallgrímsson et al.,
2005; Monteiro et al., 2005). Klingenberg et al. (2003)
identified separate integrated units in the anterior
and posterior regions of the mouse dentary. Different
developmental processes act on these parts (Cheverud, 1996). Therefore, it is likely that traits within
the ascending ramus will be more strongly integrated
to one another than they will be to the horizontal
ramus. The modular structure of pleiotropic quantitative trait loci (QTL) effects have also been studied
in mouse mandible morphology and is it is likely that
the modular structure also exists at the level of the
processes of the ascending ramus (Klingenberg et al.,
2003, Klingenberg et al., 2004).
Closely related species are expected to share similar
patterns of covariation. But in order for a functioning
structure to be maintained greater integration
between certain traits may exist, regardless of phylogenetic relatedness. Functionally integrated traits
within the dentary have been identified across intergeneric, interspecific and within populations in the
rodent family Echimyidae (Monteiro et al., 2005).
Similarly, traits associated with muscle attachment
sites in the mole’s sister taxa, shrews, are more
strongly integrated than those that are not functionally related and the relationship persists at different taxonomic levels (Badyaev & Foresman, 2004;
Badyaev, Foresman & Young, 2005; Young & Badyaev,
2006). Covariation between different parts of the mole
dentary requires further study to identify patterns of
morphological integration in this functionally diverse
group.
CONCLUSIONS
Detailed analysis of individual regions of the dentary
has revealed important aspects of variation across
mole genera. This would not have been possible had
the dentary been considered as a whole. Our results
showed that morphological variation occurs to different extents in individual parts of the dentary.
The condylar process shape showed least variation
between genera, the coronoid process and angular
process shapes showed greatest convergence among
genera, and variation in horizontal ramus shape
provided the clearest distinctions between genera.
Horizontal ramus shape was more strongly influenced by taxonomic–phylogenetic patterns of variation
than other parts of the dentary. Although variation
was closely correlated with taxonomically important
dentition differences, phylogenetic relatedness could
not be used to account for variation between all genera.
For example, differences in horizontal ramus shape
between Urotrichus and Neurotrichus (not closely
related) are very similar to those that separate Scalopus from the closely related Scapanus and Parascalops. Variation in the ascending ramus shapes are
more strongly influenced by functional controls than
taxonomic or phylogenetic relatedness, particularly in
coronoid process shape where allometric effects may
also be responsible for differences among closely
related genera (e.g. Galemys and Desmana). We found
the influence of these various factors even more apparent when variation was examined among the two fully
fossorial clades. The horizontal ramus shape provided
the clearest distinction between the two clades, reflecting their phylogenetic separation. We documented
shared patterns of variation in ascending ramus
shapes between the two clades, corresponding to their
similar functional roles. Within each clade the results
revealed distinctions between genera in coronoid
process (and to a lesser degree angular process)
shapes, including between subspecies. One explanation for discrimination at this level concerns the time
since these taxa diverged (it is possible they have not
had time to converge) and, as implied by variation in
Scalopus, may also be associated with size differences.
Dentaries are among the most common elements in
the talpid fossil record. Therefore, results of this
study could be useful in providing interpretations of
fossil as well as modern talpid biology. The present
study could be expanded to include fossil taxa and the
patterns of morphological variation might help identify evolutionary guilds (for an example, see MacLeod
& Rose, 1993). Additionally, measuring discrete sections of bone structure might be well suited to studying fossil records where structures are all too often
incomplete. Closely related genera within this study
share similar lifestyles and diets. It is therefore difficult to determine the effects of function (feeding
habits and the effects on masticatory muscles) over
phylogeny on dentary morphology. This will require
additional study.
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
SHAPE VARIATION IN THE MOLE DENTARY
Insight into intrageneric and intraspecific shape
variation among Talpidae, for example in diverse
genera such as Mogera (Abe, 1999), may also provide
a potential avenue for future study. This study may
also aid in the discovery of new phylogenetic characters as well as help define character states and
features of potential phylogenetic value (as recommended by MacLeod, 2002 and Sánchez-Villagra
et al., 2006). Larger sample sizes are required to
clarify boundaries between genera and variation at
the species level, in the hope of discovering characters
that would be useful in phylogenetic studies. Examining the pattern of morphological integration could
be particularly interesting in understanding the evolution of this structure and could be studied at developmental as well as evolutionary levels. Integrated
traits are selected for together and therefore their use
as cladistic characters is questioned (Strait, 2001;
Ackermann, 2005). Characters that are not independent might bias the results of such analyses.
ACKNOWLEDGEMENTS
We thank Daphne Hills, Louise Tomsett and Paula
Jenkins (Natural History Museum, London) and
Robert Asher and Willi Willborn (Museum für
Naturkunde, Berlin) for providing access to the material examined in this study. A research visit to Berlin
was funded by SYNTHESYS whose support is gratefully acknowledged. All eigenshape analyses were
carried out using programs written by N.M. (available
from http://www.nhm.ac.uk/hosted_sites/paleonet/ftp/
ftp.html). We also thank two anonymous reviewers for
their useful comments and especially thank Marcelo
Sánchez-Villagra (Natural History Museum, London)
for his help and advice throughout this study and his
comments on previous versions of the manuscript.
REFERENCES
Abe H. 1999. Nation-wide investigation of moles in Japan –
geographic and interspecific variations of an insectivore.
In: Yokohata Y, Nakamura S, eds. Recent Advances in the
Biology of Japanese Insectivora. Proceedings of the symposium on the biology of insectivores in Japan and on the
wildlife conservation. Hiba: Hiba Society of Natural History,
Shobara, 15–19.
Ackermann RR. 2005. Ontogenetic integration of the hominoid face. Journal of Human Evolution 48: 175–197.
Allen GM. 1938. The mammals of China and Mongolia.
Natural history of Central Asia, vol. XI, part 1. New York:
American Museum of Natural History.
Arnqvist G, Martensson T. 1998. Measurement error in
geometric morphometrics: empirical strategies to assess and
reduce its impact on measures of shape. Acta Zoologica
Academiae Scentiarum Hungarica 44: 73–96.
209
Asher RJ, Novacek MJ, Geisler JH. 2003. Relationships of
endemic African mammals and their fossil relatives based
on morphological and molecular evidence. Journal of Mammalian Evolution 10: 131–194.
Atchley WR. 1993. Genetic and developmental aspects of
variability in the Mammalian Mandible. In: Hanken J,
Hall BK, eds. The vertebrate skull. Chicago: University of
Chicago Press, 207–247.
Atchley WR, Cowley DE, Vogl C, McLellan T. 1992. Evolutionary divergence, shape change, and genetic correlation
structure in the rodent mandible. Systematic Biology 41:
196–221.
Atchley WR, Hall BK. 1991. A model for development and
evolution of complex morphological structures. Biological
Review 66: 101–157.
Badyaev AV, Foresman KR. 2004. Evolution of morphological integration. I. Functional units channel stress-induced
variation in shrew mandibles. American Naturalist 163:
868–879.
Badyaev AV, Foresman KR, Young RL. 2005. Evolution of
morphological integration: developmental accommodation of
stress-induced variation. American Naturalist 166: 382–395.
Björklund M, Merilä J. 1993. Morphological differentiation
in Carduelis finches: adaptive vs. constraint models.
Journal of Evolutionary Biology 6: 359–373.
Bolker JA. 2000. Modularity in development and why it
matters to evo-devo. American Zoologist 40: 770–776.
Bookstein FL. 1991. Morphometric tools for landmarks data:
geometry and biology. Cambridge: Cambridge University
Press.
Cabria MT, Rubines R, Gómez-Moliner B, Zardoya R.
2006. On the phylogenetic position of a rare Iberian
endemic mammal, the Pyrenean desman (Galemys pyrenaicus). Gene 375: 1–13.
Catania KC. 2002. The nose takes a starring role. Scientific
American 2002: 54–59.
Catania KC, Remple FE. 2005. Asymptotic prey profitability
drives star-nosed moles to the foraging speed limit. Nature
433: 519–522.
Cheverud JM. 1996. Developmental integration and the
evolution of pleiotropy. American Zoologist 36: 44–50.
Costa LF, Cesar RM. 2000. Shape analysis and classification: theory and practice. New York: CRC Press.
Dayan T, Simberloff D. 1994. Character displacement,
sexual dimorphism, and morphological variation among
British and Irish mustelids. Ecology 75: 1063–1073.
Duarte LC, Monteiro LR, von Zuben FJ, dos Reis SF.
2000. Variation in mandible shape in Trichomys apereoides
(Mammalia: Rodentia): geometric analysis of a complex
morphological structure. Systematic Biology 49: 563–578.
Gaughran GRL. 1954. A comparative study of the osteology
and myology of the cranial and cervical regions of the shrew,
Blarina brevicauda, and the mole, Scalopus aquaticus.
Miscellaneous Publications Museum of Zoology University of
Michigan 80: 1–82.
Grand T, Gould E, Montali R. 1998. Structure of the
proboscis and rays of the star-nosed mole, Condylura
cristata. Journal of Mammology 79: 492–501.
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
210
E. BARROW and N. MACLEOD
Greenacre MJ. 1984. Theory and applications of correspondence analysis. London: Academic Press.
Grüneberg H. 1952. The genetics of the mouse. Hague:
Martinus-Nijhoff.
Hall BK. 2003. Unlocking the black box between genotype
and phenotype. Biology and Philosophy 18: 219–247.
Hall BK. 2005. Bones and cartilage: developmental and evolutionary skeletal biology. Amsterdam: Elsevier Academic
Press.
Hallgrímsson B, Yardley Brown JJ, Hall KH. 2005.
The study of phenotypic variability: an emerging research
agenda for understanding the developmental-genetic architecture underlying phenotypic variation. In: Hallgrímsson
B, Hall BK, eds. Variation: a central concept in biology.
Amsterdam: Elsevier Academic Press, 525–551.
Hildebrand M. 1982. Analysis of vertebrate structure, 2nd
edn. New York: John Wiley and Sons, Inc.
Humphrey LT, Dean MC, Stringer CB. 1999. Morphological variation in great ape and modern human mandibles.
Journal of Anatomy 195: 491–513.
Hutchison JH. 1968. Fossil Talpidae (Insectivora, Mammalia) from the later Tertiary of Oregon. Bulletin of the
Museum of Natural History of the University of Oregon 11:
1–117.
Hutchison JH. 1974. Notes on type specimens of European
Miocene Talpidae and a tentative classification of Old World
Tertiary Talpidae (Insectivora: Mammalia). Geobios 7: 211–
256.
Hutchison JH. 1976. The Talpidae (Insectivora, Mammalia):
evolution, phylogeny, and classification. PhD Thesis,
University of California, Berkeley.
Hutterer R. 2005. Soricomorpha. In: Wilson DE, Reeder DM,
eds. Species of the world: a taxonomic and geographic reference. Baltimore: Johns Hopkins University Press, 220–311.
Hylander WL. 2005. The functional significance of primate
mandibular form. Journal of Morphology 160: 223–239.
Klingenberg CP. 2005. Developmental constraints, modules
and evolvability. In: Hallgrímsson B, Hall BK, eds. Variation: a central concept in biology. Amsterdam: Elsevier
Academic Press, 219–247.
Klingenberg CP, Leamy LJ, Cheverud JM. 2004. Integration and modularity of quantitative trait locus effects on
geometric shape in the mouse mandible. Genetics 166:
1909–1921.
Klingenberg CP, Mebus K, Auffray JC. 2003. Developmental integration in a complex morphological structure: how
distinct are the modules in the mouse mandible? Evolution
and Development 5: 522–531.
MacLeod N. 1999. Generalizing and extending the eigenshape method of shape space visualization and analysis.
Paleobiology 25: 107–138.
MacLeod N. 2002. Phylogenetic signals in morphometric
data. In: MacLeod N, Forey PL, eds. Morphology, shape and
phylogeny. Systematics Association Special Volume. London:
Taylor & Francis, 100–138.
MacLeod N. 2006. Rs and Qs II: correspondence analysis.
Palaeontological Association Newsletter 62: 60–74.
MacLeod N, Rose KD. 1993. Inferring locomotor behaviour
in Paleogene mammals via eigenshape analysis. American
Journal of Science 293: 300–355.
Monteiro LR, Bonato V, dos Reis SF. 2005. Evolutionary
integration and morphological diversification in complex
morphological structures: mandible shape divergence in
spiny rats (Rodentia, Echimyidae). Evolution and Development 7: 429–439.
Monteiro LR, dos Reis SF. 2005. Morphological evolution in
the mandible of spiny rats, genus Trinomys (Rodentia:
Echimyidae). Journal of Zoological Systematics and Evolutionary Research 43: 332–338.
Moore DW. 1986. Systematic and biogeographic relationships
among the Talpinae (Insectivora: Talpidae). PhD Dissertation, University of New Mexico.
Motokawa M. 2004. Phylogenetic relationships within
the family Talpidae (Mammalia: Insectivora). Journal of
Zoology (London) 263: 147–157.
Motokawa M, Lin LK, Cheng HC, Harada M. 2001. Taxonomic status of the Senkaku mole, Nesoscaptor uchidai,
with special reference to variation in Mogera insularis from
Taiwan (Mammalia: Insectivora). Zoological Science 18:
733–740.
Nowak RN. 1999. Walker’s mammals of the world, Vol. 1, 6th
edn. Baltimore: The John Hopkins University Press.
Okamoto M. 1997. Phylogeny of Japanese moles inferred from
mitochondrial CO1 gene sequences. In: Recent advances in
the biology of Japanese insectivora. Proceedings of the symposium on the biology of insectivores in Japan and on the
wildlife conservation. Hiba: Hiba Society of Natural History.
Olson EC, Miller RL. 1958. Morphological integration.
Chicago: University of Chicago Press.
Polly PD. 2008. Adaptive zones and the pinniped ankle: a 3D
quantitative analysis of carnivoran tarsal evolution. In:
Sargis E, Dagosto M, eds. Mammalian evolutionary morphology: a tribute to Frederick S. Szalay. Dordrecht:
Springer, 165–194.
Raw F. 1966. The soil fauna as a food source for moles.
Journal of Zoology (London) 149: 50–54.
Rees RW. 2005. Morphologic variation in the mandible of the
white-tailed deer (Odocoileus virginianus): a study of populational skeletal variation by principal component and
canonical analyses. Journal of Morphology 128: 113–130.
Reyment RA. 1991. Multidimensional paleobiology. Oxford:
Pergamon Press.
Reyment RA, Jöreskog KG. 1993. Applied factor analysis
in the natural sciences. Cambridge: Cambridge University
Press.
Rohlf FJ. 1990. Fitting curves to outlines. In: Rohlf FJ,
Bookstein FL, eds. Proceedings of the Michigan Morphometrics Workshop. The University of Michigan Museum of
Zoology, Special Publication No. 2, 167–177.
Rohlf FJ. 2003. tpsDig, relative warps analysis, Version 1.36.
Stony Brook: Department of Ecology and Evolution, State
University of New York at Stony Brook.
Rohlf FJ. 2004. tpsDig, digitize landmarks and outlines,
Version 2.0. Stony Brook: Department of Ecology and
Evolution, State University of New York at Stony Brook.
Rohlf FJ, Loy A, Corti M. 1996. Morphometric analysis of
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211
SHAPE VARIATION IN THE MOLE DENTARY
Old World Talpidae (Mammalia, Insectivora) using partialwarp scores. Systematic Biology 45: 344–362.
Sánchez-Villagra MR, Horovitz I, Motokawa M. 2006. A
comprehensive morpholgical analysis of talpid moles (Mammalia) phylogenetic relationships. Cladistics 22: 59–88.
Schlosser G, Wagner GP. 2004. Modularity in development
and evolution. Chicago: University of Chicago Press.
Schluter D. 1996. Adaptive radiation along genetic lines of
least resistance. Evolution 50: 1766–1774.
Shinohara A, Campbell KL, Suzuki H. 2003. Molecular
phylogenetic relationships of moles, shrew moles, and
desmans from the new and old worlds. Molecular
Phylogenetics and Evolution 27: 247–258.
Shinohara A, Suzuki H, Tsuchiya K, Zhang Y-P, Luo J,
Jiang X-L, Wang Y-X, Campbell KL. 2004. Evolution
and biogeography of talpid moles and continental East Asia
and the Japanese islands inferred from mitochondrial and
nuclear gene sequences. Zoological Science 21: 1177–1185.
Silcox MT, Teaford MF. 2002. The diet of worms: an analysis of mole dental microwear. Journal of Mammology 83:
804–814.
Slijper EJ. 1946. Comparative biologic–anatomical investigations on the vertebral column and spinal musculature of
mammals. Amsterdam: North-Holland Publishing Co.
Strait DS. 2001. Integration, phylogeny, and the hominid
cranial base. American Journal of Physical Anthropology
114: 273–297.
Tomo S, Ogita M, Tomo I. 1997. Development of mandibular
cartilages in the rat. Anatomical Record 249: 233–239.
True FW. 1896. A revision of the American moles. Proceedings of the US National Museum 29: 1–115.
Van Valen L. 1967. New Paleocene insectivores and insectivore classification. Bulletin of the American Museum of
Natural History 135: 217–284.
Waddell PJ, Okada N, Hasegawa M. 1999. Towards resolving the interordinal relationships of placental mammals.
Systematic Biology 48: 1–5.
Whidden HP. 2000. Comparative myology of moles and
the phylogeny of the Talpidae (Mammalia, Lipotyphla).
American Museum Noviates 3294: 1–53.
Yates TL, Moore DW. 1990. Speciation and evolution in the
family Talpidae (Mammalia: Insectivora). In: Nevo E, Reig
OA, eds. Evolution of subterranean mammals at the organismal and molecular levels. New York: Wiley-Liss, 1–22.
Yates TL, Schmidly DJ. 1978. Mammalian species. Scalopus
aquaticus. American Society of Mammalogists 105: 1–4.
Young R, Badyaev AV. 2006. Evolutionary persistence of
phenotypic integration: influence of developmental and
functional relationships on complex trait evolution.
Evolution 60: 1291–1299.
Zahn CT, Roskies RZ. 1972. Fourier shape descriptors
for closed plane curves: IEEE Transactions on Computers
v. C-21: 269–281.
Zelditch ML, Swiderski DL, Sheets HD, Fink WL.
2004. Geometric morphometrics for biologists: a primer.
Amsterdam: Elsevier Academic Press.
Ziegler AC. 1971. Dental homologies and possible relationships of recent Talpidae. Journal of Mammology 52: 50–68.
211
Ziegler R. 2003. Moles (Talpidae) from the late Middle
Miocene of South Germany. Acta Palaeontologica Polonica
48: 617–648.
APPENDIX 1
Estimates of repeatability of shape variables explaining up to 90% of the variation in each region of the
dentary. R1 is calculated from repeated measures
taken from the same images of each individual and R2
included repeated measures taken from separate
images of the same individual.
Variable
Coronoid process
ES-1
ES-2
ES-3
ES-4
ES-5
ES-6
ES-7
ES-8
ES-9
ES-10
ES-11
Condylar process
ES-1
ES-2
ES-3
ES-4
ES-5
ES-6
ES-7
ES-8
ES-9
ES-10
Angular process
ES-1
ES-2
ES-3
ES-4
ES-5
ES-6
ES-7
ES-8
ES-9
ES-10
ES-11
ES-12
Horizontal ramus
RW-1
RW-2
RW-3
RW-4
%
Cumulative
%
R1
R2
37.5
19.0
11.2
7.9
4.1
3.5
2.2
1.4
1.2
1.2
1.1
37.5
56.5
67.7
75.6
79.8
83.3
85.5
86.9
88.2
89.4
90.4
0.98
0.90
0.99
0.79
0.98
0.98
0.82
0.85
0.36
0.33
0.60
0.98
0.92
0.99
0.83
0.96
0.96
0.73
0.86
0.38
0.22
0.60
65.4
10.3
5.6
2.2
2.0
1.6
1.1
1.0
0.7
0.7
65.4
75.7
81.3
83.5
85.5
87.1
88.1
89.2
89.9
90.6
0.95
0.83
0.96
0.77
0.64
0.65
0.45
0.49
0.20
0.29
0.97
0.87
0.95
0.83
0.72
0.75
0.49
0.47
0.12
0.16
41.6
14.6
11.8
7.4
5.6
2.0
1.6
1.6
1.4
1.2
0.8
0.7
41.6
56.2
68.0
75.4
81.0
83.0
84.7
86.2
87.6
88.8
89.6
90.3
0.99
0.99
0.95
0.99
0.96
0.66
0.84
0.83
0.82
0.89
0.69
0.65
0.98
0.98
0.96
0.98
0.96
0.46
0.71
0.82
0.82
0.87
0.73
0.65
45.6
28.4
15.0
5.4
45.6
73.9
88.9
94.3
0.95
0.99
0.99
0.94
0.95
0.98
0.98
0.93
© 2008 Trustees of the Natural History Museum (London)
Journal compilation © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 153, 187–211