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Geometric Morphometric Investigation of Molar Shape Diversity in Modern Lemurs and Lorises.

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THE ANATOMICAL RECORD 292:701–719 (2009)
Geometric Morphometric Investigation
of Molar Shape Diversity in Modern
Lemurs and Lorises
JESS WHITE*
Department of Sociology and Anthropology, Western Illinois University, Macomb, Illinois
ABSTRACT
In the study of mammalian adaptation to the environment, teeth are
of primary importance due to their role as one of the direct interaction
points between an individual and its ecological surroundings. Here, molar
shape and function are investigated through traditional multivariate statistics and Thin-Plate Splines deformations to compare the relative location of lower first molar occlusal structures (protoconid, metaconid,
hypoconid, entoconid, cristid obliqua, and protolophid) in modern lemurs,
lorises, tarsiers, and a non-primate outgroup taxon (Tupaia). Results suggest that shape is based both on tooth size and dietary patterns. Small
teeth tend to be short (anteroposteriorally) with wide talonids, whereas
larger teeth are generally characterized as being long and narrow. In considering non-size related shape trends, frugivorous and graminivorous
taxa generally exhibit a relatively buccal intersection of the cristid obliqua with the base of the protolophid, and a relatively ‘‘perpendicular’’
position of the protolophid in relation to the anteroposterior axis of the
tooth (defined as the axis connecting the protolophid and hypoconid).
Morphological trends of folivores include a central (midline) position of
the cristid obliqua-protolophid base intersection and an oblique angle of
the protolophid. Insectivorous taxa (primate and non-primate) generally
exhibit a central placement of the cristid obliqua-protolophid base intersection (as in folivores), along with a relatively perpendicular angle of the
protolophid (as in frugivores). Omnivorous taxa exhibit shape patterns
that are intermediate between these three former groups. This study provides a comparative baseline for the interpretation of morphological
trends in fossil primate groups, particularly the Adapiformes. Anat Rec,
C 2009 Wiley-Liss, Inc.
292:701–719, 2009. V
Key words: functional morphology; thin-plate splines analysis;
strepsirrhine dental variation
Paleoecological and paleobiological interpretation of
the primate fossil record continues to rely upon the
quantification of morphological features and comparison
with extant primate groups (Witmer, 1995; Ungar, 1998).
Central to the present study is the exploration of biodiversity among adapiforms, fossil primates suggested to
be most closely related to modern ‘‘tooth-combed’’ primates (lemurs and lorises). The diversity and evolutionary
history of adapiform taxa is of interest in terms of their
role in community ecology, as well as their evolutionary
relationships to modern lemurs and lorises (Godinot,
1988, 2006; Masters et al., 2006). To explore these ecoC 2009 WILEY-LISS, INC.
V
Grant sponsors: University of Iowa Presidential Graduate
Fellowship; T. Anne Cleary International Dissertation Research
Fellowship; Travel assistance from the Department of
Anthropology at the University of Iowa.
*Correspondence to: Jess White, Department of Sociology and
Anthropology, Western Illinois University, 404 Morgan Hall,
Macomb, IL 61455. E-mail: JL-White@wiu.edu
Received 28 January 2008; Accepted 13 January 2009
DOI 10.1002/ar.20900
Published online in Wiley InterScience (www.interscience.wiley.
com).
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WHITE
logical roles, previous studies have utilized extant
lemurs and lorises as baselines in the analysis of patterns observed in adapiform material (for illustrative
examples, refer to Dagosto, 1983; Gebo, 1985; Lanèque,
1993; Viguier and Tort, 2000; Viguier, 2002; White and
Gebo, 2004; Gilbert, 2005; White, 2005, 2006). To provide
further insight into the analysis of fossil adapiform taxa,
this project aims to establish a comparative base-line for
analyzing molar shape using occlusal structures in modern lemurs and lorises by asking:
1. What is the degree of allometric influence (as discussed by Gould, 1966; Mosiman, 1970; Klingenberg,
1998) on the relative position of lower molar landmarks in a sample of recent primates and outgroup
taxa, and what shape trends are predicted by molar
size change?
2. Can components of molar size and shape be separated
in the current sample so that morphological trends
which are size-related, as well as those that are not,
can be investigated to construct and infer form-function associations?
3. Can differences in the relative location of lower molar
landmarks be related to various dietary patterns?
How might these trends be applied in exploration of
extinct primate adaptation and ecology?
4. How do the results obtained here compare to those
commonly used methods where a separate measure of
body size is required?
Living ‘‘tooth-combed’’ lemurs and lorises are primates
distributed throughout sub-Saharan Africa and southern
Asia. Lemurs (members of the families Lemuridae,
Indriidae, Lepilemuridae, Cheirogaligidae, and Daubentoniidae) are restricted to Madagascar, whereas lorises
and galagos (Lorisidae and Galagonidae) are distributed
throughout the tropical regions of Africa and southern
Asia. Lemurs and lorises are commonly referred to as
‘‘prosimians’’ or ‘‘strepsirrhines,’’ depending on the perspective authors take in reference to the relative placement of extinct and extant tarsiiform taxa within
primates, as well as to the evaluation of soft-tissue and
hard-tissue characteristics of the crania and postcrania
(Pocock, 1918; Rosenberger and Szalay, 1980; Schwartz
and Tattersall, 1987; Yoder, 1997; Fleagle, 1999; Gebo
et al., 2000). Here, the term ‘‘strepsirrhine’’ is used to distinguish the living lemur and loris taxa from tarsiiforms
and ‘‘higher primates’’ (haplorhines) (Martin, 2003). Modern strepsirrhines are incredibly diverse in their body
size [between 30 g and 6840 g (0.3–6.84 kg)], ecological
habitat, and dietary patterning (Fleagle, 1999). Whereas
lemurs and lorises are generally considered the most
basal of the extant primates, particular systematic issues
continue to be debated in the literature (Crovella et al.,
1993; Purvis, 1995; Yoder and Irwin, 1999; Wyner et al.,
2000; Yoder et al., 2001; Pastorini et al., 2003; Roos
et al., 2004; Karanth et al., 2005; Masters et al., 2005).
Discussion also continues regarding the relationships
between primates and non-primate outgroup taxa. Several recent molecular analyses have scrutinized the relationships between primates, bats, modern colugos
(Dermoptera), and tree shrews (Scandentia) (Adkins and
Honeycutt, 1991; Murphy et al., 2001; Springer et al.,
2003; Nishihara et al., 2006). Accordingly, this study also
Fig. 1. Summary of current phylogenetic hypotheses concerning
the relationships between lemuriforms, lorisiforms, and outgroup nonprimate taxa (Tupaia) (Crovella et al., 1993; Purvis, 1995; Yoder and
Irwin, 1999; Wyner et al., 2000; Yoder et al., 2001; Pastorini et al.,
2003; Roos et al., 2004; Karanth et al., 2005; Masters et al., 2005,
2006). Branch lengths are not intended to indicate evolutionary time or
distance.
considers primate and non-primate groups that ‘‘bracket’’
strepsirrhines in recent phylogenetic hypotheses to
explore shape trends in dental morphology (Fig. 1).
It is anticipated that an examination of form-function
relationships as designed here will provide a comparative framework for interpreting adapiform behavior.
Teeth are particularly relevant in the study of environmental adaptation because they serve as one point of
direct interaction between an organism and its ecology,
specifically dietary adaptation. The benefit of examining
dental morphology of extant groups is that form-function
relationships between morphology and ecological adaptation can be hypothesized and explored using a variety of
methods. Previously, research into molar morphology
and adaptation at several different analytical levels has
provided a host of methods to apply to extant groups
and the fossil record (refer to Ungar, 1998; Teaford, 2000
for comprehensive reviews). Each of these methods
address different aspects of function, be it an individual’s dietary behavior during life as measured by microwear methods (for example refer to Ungar et al., 2003;
Godfrey et al., 2004; Semprebon et al., 2004), shearing
and/or crushing capabilities as investigated through
comparative and quantitative studies of dental and mandibular morphology (for example refer to Kay and Hiiemae, 1974; Kay, 1975; Seligsohn and Szalay, 1974, 1978;
Hiiemae, 1978; Kay and Covert, 1984; Ungar and Kay,
1995; Ungar, 1998; Yamashita, 1998a; Strait, 2001; Kirk
and Simons, 2001; Ungar et al., 2003, 2004 and references therein), or the development of functional dental
models (Spears and Crompton, 1996; Evans and Sanson,
2003; Polly, 2004; Evans, 2005 and references therein).
Molar function has also been included in larger analyses
of mastication dynamics and patterns (refer to Hiiemae,
1984 and references therein). For example, one of the
most popular methods of dietary interpretation utilized
by paleoprimatologists is that developed by Kay (1975).
In this classic study, an association was drawn between
703
MOLAR DIVERSITY IN LEMURS AND LORISES
poorly developed shearing and crushing features and
frugivory in primates. Folivorous and insectivorous primates, on the other hand, share increased shearing,
crushing, and grinding capabilities facilitated by sharp
shearing blades and molar cusps.
The present analysis adds to the quantification of
shearing capabilities by examining the spatial pattern of
shearing and crushing components of the lower molar
and their relationship to dietary behavior in modern prosimians and mammalian outgroups. Specifically, I test
the hypothesis that lower molar shape is associated with
broad dietary categories among extant prosimians using
geometric morphometrics. I predicted that if shape differences are associated with different broad dietary categories in closely related groups of mammals, convergent
evolution of lower molar shape among prosimians with
similar diets may be observed.
TABLE 1. Summary of the genera and species
included in the present study, including sample sizes
(N) and dietary classification
Genus
Avahi
Eulemur
Galago
Hapalemur
Lepilemur
Lemur
Loris
Nycticebus
Otolemur
Perodicticus
Propithecus
Species
N
Diet
laniger
fulvus
macaco
moholi
senegalensis
griseus
sp.
mustelinus
catta
tardigradus
coucang
crassicaudatus
garnetti
potto
verreauxi
diadema
bancanus
syrichta
glis
palawanensis
6
8
5
5
4
9
1
8
7
6
7
5
1
6
5
3
5
3
7
6
FOL
FRG
FRG
INS
INS
GRM
GRM
FOL
FOL/ FRG
OMN
OMN
OMN
OMN
OMN
FOL/ FRG
FOL/ FRG
INS
INS
INS
INS
MATERIALS AND METHODS
Assumptions and Caveats Regarding the Study
of Dental Form and Dietary Behavior
Tarsius
The morphology of any structure of an organism is a
result of a combination of genetic, evolutionary, and
adaptive processes. Teeth are no exclusion to this pattern, and are commonly used to explore functional, evolutionary, or ecological hypotheses concerning living and
fossil taxa. Primates generally exhibit between four and
six cusps on mandibular molars (the paraconid, protoconid, metaconid, hypoconid, entoconid, and hypoconulid).
In primates, the primary structures of the upper and
lower molars are the paracone and protoconid, respectively. The acquisition of the protocone of the upper
molar in early therian mammals was coincident with the
appearance of a posterior talonid basin in the mandibular molars, resulting in a dental relationship that in
addition to puncturing and shearing, also enhanced
crushing and grinding capabilities (Patterson, 1956;
Crompton and Kielan-Jaworowska, 1978; Butler, 2000).
This additional functional complex likely offered early
mammals a system that could adapt to a variety of dietary patterns and adaptive niches (Clemens, 1971).
Ontogenetically, the pattern of cusp development closely
mirrors the evolutionary pattern of development as the
paracone and protoconid are the first to develop during
embryonic growth (Hershkovitz, 1971). Most recently,
several key studies and literature summaries have
established the embryonic patterns of growth and regulatory mechanisms responsible for molar morphogenesis
(Vaahtokare et al., 1996; Jernvall and Jung, 2000; Jernvall and Thesloff, 2000; Jernvall et al., 2000; Cobourne
and Sharpe, 2003; Kangas et al., 2004; Salazar-Ciudad
and Jernvall, 2004; Kassai et al., 2005; Polly, 2006). The
implications of this for the functional analysis of tooth
morphology are that the form and location of molar landmarks are determined early in embryonic development,
and appear to be less susceptible to the effects of later
development or of occlusion during fetal life. Therefore,
the analysis of molar relative landmark position is
appropriate for questions regarding initial functional adaptation and evolutionary change within mammalian
lineages. These data, combined with other morphological
information, can be used to refine the interpretation of
adaptive change in the dentition of mammalian groups.
FOL, folivorous; FRG, frugivorous; INS, insectivorous;
GRM, gramnivorous; OMN, omnivorous.
Tupaia
Sample and Categorization of Dietary Behavior
The taxa included for analysis here represent 12 primate genera (Galago, Otolemur, Loris, Perodicticus,
Nycticebus, Lepilemur, Hapalemur, Lemur, Eulemur,
Avahi, Propithecus, Tarsius), and one non-primate outgroup genus, Tupaia (Table 1). The sample was analyzed
at the generic level to maximize sample size and provide
an overall picture of shape variation to apply to the fossil record. Figure 1 illustrates the hypothesized relationships between the taxa included here. In total, 115
individuals were analyzed, housed in the following collections: Department of Mammalogy, Field Museum of
Natural History (Chicago); the Department of Vertebrate
Zoology, American Museum of Natural History (New
York); and the Division of Mammals, Smithsonian
National Museum of Natural History (Washington, DC).
As field projects documenting the diversity of dietary
behavior among lemurs and lorises continue to accumulate new data, it has become increasingly difficult to
assign organisms to distinct dietary groups. Overlap in
the use of food items, different field methods of observation, and seasonal use of resources by primate taxa are
just a few of the notable explanations for the increasing
complexity of dietary interpretation. However, as the use
of shape analysis has great implications for paleoecology
and interpreting dietary behavior in extinct organisms,
the categorization of gross dietary patterns and the association of morphological patterns to dietary behavior
remain useful. Given the incredible amount of information available, dietary groups used here were gleaned
largely from composite summaries of regional primate
behavior and ecology (Chapman et al., 1999; Gupta and
Chivers, 1999; Ganzhorn et al., 1999) (Table 1).
Although individual field studies may differ slightly
from the data presented in these studies, these dietary
group assignments were chosen for the convenience of
use in subsequent or comparative studies of dental
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WHITE
morphology. In only one case, Hapalemur, was the published assignment of ‘‘folivorous’’ not used (Ganzhorn
et al., 1999); instead, Hapalemur was assigned to a ‘‘graminivorous’’ category to acknowledge the overall differences between bamboo-feeding and the mastication of
leaf material. Dietary classification of the non-primate
genus, Tupaia, was based on Emmons (1991).
Geometric Morphometric Investigation
of Shape
The methods used by this study fall under the rubric
of ‘‘geometric morphometrics.’’ Geometric methods, based
on the identification of relative landmark locations in
either two- or three-dimensional space, are utilized
because they provide both quantitative variables appropriate for multivariate statistical methods as well as representations of shape variation within a sample. The
theory and practical application of geometric morphometrics have been thoroughly discussed in the biological
and morphometric literature (refer to Rohlf and Marcus,
1993; Roth and Mercer, 2000; Adams et al., 2004;
Zelditch et al., 2004; Slice, 2007 for literature reviews
and summary and Cardini and O’Higgens, 2004; Monteiro et al., 2003; Monteiro and Dos Reis, 2005; Maerz
et al., 2006 for recent examples of two-dimensional studies). The geometric morphometric approaches used here
to analyze shape variation within a sample of primate
dental material are as detailed below:
1. Landmark Identification: In this study, five dental
landmarks were identified on the first lower molar,
each representing either the location in two dimensional space of a cusp tip (protoconid, metaconid,
entoconid, hypoconid) or the intersection of major
shearing structures (the intersection of the cristid
obliqua with the base of the protolophid). For simplicity, the latter landmark will be referred to as the
‘‘CO-PRLPHD’’ point. The first lower molar of each
specimen was aligned and photographed under standardized conditions so that the occlusal surface was
parallel with the lens of a digital microscope (Digital
Blue, QX3). Important considerations regarding photography of three-dimensional material has been
raised in the literature (Mullin and Taylor, 2002;
Gharaibeh, 2005). Although three-dimensional capture may not be the most practical in field situations
and in situations requiring travel with 3-D scanners,
care was taken to address the possibility of error
introduction in using two-dimensional methods. Here,
each individual specimen was centered under the lens
of the digital microscope at the same magnification
using molding clay. After each specimen was photographed, the position of the movable microscope platform, as well as the shape of the molding clay, was
‘‘reset’’ so that the next specimen would be treated in
the same manner as previous material. With this
standardized process, it is assumed here that any
error that may have been introduced by the procedure
is either negligible or consistent over the sample
(Mullin and Taylor, 2002). The landmarks were subsequently digitized into a coordinate system using the
tpsDIG (v 2.0) (Rohlf, 2004) software package. The
lower first molar was chosen because it is the least
Fig. 2. Illustration of the landmarks included in the present study.
Landmarks are labeled as: 1) protoconid, 2) metaconid, 3) intersection
of the cristid obliqua with the protolophid base, 4) entoconid, and 5)
hypoconid. Crushing areas are labeled as: TGB, trigonid basin; TLB,
talonid basin; HF, hypoflexid region. Generalized lower molar based on
Hershkovitz (1971).
variable along the molar tooth row in most primate
and non-primate taxa and likely represents the single
best tooth to study size distribution and variability in
the fossil record (Gingerich, 1974, 1979).
The relative location of molar cusps (protoconid,
metaconid, hypoconid, and entoconid), along with the
intersection of the anterior extension of the cristid
obliqua with the protolophid base, were chosen as
landmarks to capture either the gross dimensions of
major crushing areas (the talonid basin of the lower
molar) or the relative position of shearing structures
(Fig. 2). The anterior landmarks (protoconid and
metaconid) serve to represent the location of the protolophid, an anterior shearing crest and the anterior
border of the talonid basin. The posterior landmarks
(entoconid and hypoconid) function as the posterior
corners of the talonid basin of the lower molar.
Finally, the point of intersection between the anterior
extension of the cristid obliqua (the primary talonid
shearing crest) and the base of protolophid was also
identified to assess the relative location of cristid
MOLAR DIVERSITY IN LEMURS AND LORISES
obliqua (Landmarks 3 and 5) (Fig. 2). Since, in many
cases, the anterior extension of the cristid obliqua is
located at the base of the protoconid or metaconid
(and does not continue to a cusp tip), the intersection
of the crest with the protolophid base was identified
as a uniform point within the sample. Among taxa,
the breadth of the protolophid varies; therefore, the
CO-PRLPHD point does not necessarily fall in line
with the segment formed by the protoconid (Landmark 1) and the metaconid (Landmark 2). This point,
which marks the buccal border of the talonid basin, is
designed to provide not only an approximate measure
of talonid basin size and dimensions, but also a
marker of the direction and location of shearing
capabilities.
2. Procrustes Superimposition and Geometric Morphometrics: Superimposition methods, such as those
based on Procrustes distances, serve to register landmarks in a given sample to one common coordinate
system through translation, scale, and rotation (Slice,
2005). A generalized Procrustes analysis (GPA) was
performed so that all individuals within the sample
could be compared to an iteratively computed sample
mean (Slice, 2005). The transformed landmark data
were then included in two-dimensional Thin-Plate
Splines (TPS) analysis, designed to illustrate morphological trends in shape difference (Thompson, 1917;
Rohlf and Marcus, 1993; Bookstein, 1991, 1996a,b;
Birch, 1997; Slice, 2005). The geometric morphometric
analyses were performed here using tpsRELW (version 1.42) software package (Rohlf, 2005).
3. Statistical Analyses: The relationship between size
and shape variables is necessary to investigate in any
biometric study because size is one of the most important determinants of biological form in mammals
(refer the discussions in Gingerich and Smith, 1984).
In this sample, log-transformed values of the centroid
size (the square root of the summed squared differences between each landmark from the center of the
form) was used as a proxy for tooth size and was
derived only through the process of Procrustes analysis. Centroid size (and transformations thereof) is
commonly used in geometric morphometric analyses
as it is a size variable that is independent of random,
isometric shape variation and can be used in regression analyses to test null hypotheses of isometry
within a sample (as described below) and to explore
how shape is correlated with size (allometric patterns)
once scale is removed from a landmark dataset
through superimposition methods (Zelditch et al.,
2004). Thus, interpretation of size-shape relationships
in the sample was not dependent on a separate proxy
variable representing size (such as body mass, tooth
length or width, or length of a cranial or postcranial
element). Using a variable such as centroid size to
examine the influence of allometry in a dataset is key,
as shape patterns correlated with allometric scaling
are important components in comparisons of biomechanic function, both at an ontological level (within
one taxonomic group), as well as between species of
difference sizes (Zelditch et al., 2004). Whereas a
regression of centroid size on body mass within this
sample would potentially provide further size-related
information, an important goal of this study was to
provide a framework in which to interpret fossil pri-
705
mate dietary behavior based on shape. Thus centroid
size is a quantifiable metric in any landmark-based
dataset that does not rely on other methods of estimating body mass, which can be difficult in the case
of fossil taxa, particularly if other dental or postcranial remains are not available.
In the present study, a multivariate regression analysis (using statistical definitions established by Slice
et al., 1998; Monteiro, 1999) performed by the tpsREGR
(Rohlf, 2007) software package was utilized to: 1) attain
an r2 value (square of correlation coefficient), a statistic
used to assess the predictive relationship between one
independent variable (in this case, molar size as represented by log centroid size) and multiple dependent variables (the partial warps, which collectively describe
shape, i.e., the relative distances between molar landmarks), and 2) examine whether the relationship
between size and shape indicates a significant deviation
from the null model of isometry as measured using a
Wilks’ K statistic. Instances in which r2 values approximating 1.0 suggest a strong predictive relationship
between size and shape (i.e., a particular shape can be
reliably predicted with a given measure of size). In the
latter test, the Wilks’ K value that is generated can be
used to detect a significant difference against a model of
isometry (P < 0.05 ¼ allometry; P > 0.05 ¼ isometry)
(Rohlf, 2007). The tpsREGR (Rohlf, 2007) software package also produces a measure of what percentage [R2 of
the shape variation in a given sample is not explained
by a measure of size (centroid size); Goodall’s F-test].
The partial warp scores, being multiple dependent
variables that collectively describe shape, can additionally be analyzed using one-way multivariate analysis of
variance (MANOVA). A MANOVA of the partial warps
tests for collective, multivariate statistical differences in
the partial warp scores (shape) among the genera, which
yields traditional multivariate statistics (Wilks’ K). If
there is shown to be a significant multivariate difference
in shape among the genera, subsequent post hoc oneway ANOVA comparisons tests (for each individual partial warp) are run following a traditional Bonferroni procedure with appropriately adjusted significance levels
(a ¼ 0.5/78 comparisons ¼ 0.000064 for each comparison).
Finally, a principal components analysis of shape (also often referred to ‘‘Relative Warps analysis’’) is performed to
consider the distribution of the sample in shape space.
MANOVA analyses, principal components analysis, and
relative warp analysis were performed using the
tpsRELW (version 1.42) software package (Rohlf, 2005)
and SPSS 14.0 (using the exported data from tpsRELW).
RESULTS
Allometry and Statistical Analyses
To gain a measure of the overall effect of tooth size
(log centroid size) on the pattern of shape variation
within the sample, a multivariate regression analysis
was performed. Results for the total sample (combined
primate and non-primate taxa, N ¼ 115) using uniform
and non-uniform variables shows a moderate relationship between tooth size and molar shape (with an overall multiple r2 ¼ 0.61) and significant shape allometry
(the null hypothesis of isometry is rejected) (Table 2). In
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TABLE 2. Summary of the results obtained through multivariate regression of the partial warp scores
against log centroid size in the present sample
Total uniform and non-uniform shape components
r2
Wilks’s K
df
P value
R2 (%)
0.6122
0.3877
6 (108)
P < 0.01
26.02%
Fig. 3. Bivariate plot illustrating the relationship of log centroid size
(X-axis) with the first principal component. Shape deformation grids
along the X-axis represent predicted shape change in the total sample
(smallest specimen to largest); shape deformation grids along the Y-
axis represent the shape change along the first principal component.
Taxonomic groups are as follows: !, Avahi; *, Propithecus; l, Eulemur; þ, Hapalemur; ~, Lepilemur; $, Nycticebus; n, Galago; ^,
Loris; h, Otolemur; |, Perodicticus; 3, Tarsius; , Tupaia; 3, Lemur.
this sample, 73.98% (R2 ¼ 26.02%) of the shape variation
remains unexplained by the size-shape relationship, suggesting tooth size, while important, is not the sole factor
determining molar shape variation.
Given that there was found to be a moderate relationship between tooth size (log centroid size) and molar
shape, bivariate plots of the first principal component
(generally representative of the greatest amount of variation in the sample) against log centroid size were produced to illustrate patterns of size-related shape change
using both by generic and dietary classification (Figs. 3
and 4). Here, using PC1 values, shape changes are predicted to be associated with a transformation from short,
wide molars at smaller tooth sizes to long, narrow
molars at larger tooth sizes. At smaller tooth sizes, the
distance between the entoconid and hypoconid is relatively larger, and the talonid basin is shortened with the
decrease in the distance between the intersection of the
cristid obliqua and the protolophid base (CO-PRLPHD)
and the posterior landmarks (entoconid and hypoconid).
MOLAR DIVERSITY IN LEMURS AND LORISES
707
Fig. 4. Bivariate plot illustrating the relationship of log centroid size
(X-axis) with the first principal component. Shape deformation grids
along the X-axis represent predicted shape change in the total sample
(smallest specimen to largest); shape deformation grids along the Y-
axis represent the shape change along the first principal component.
Dietary groups are as follows: *, graminivorous; l, insectivorous; þ,
frugivorous; ~, folivorous; h, omnivorous.
At larger tooth sizes, the relative distance between the
entoconid and the hypoconid decreases, whereas the
talonid basin lengthens with an anterior shift of the COPRLPHD position (Figs. 3 and 4).
One-way MANOVA comparisons were performed to
determine if differences in the mean configurations of
the five molar landmarks for each genus were statistically significant in the sample. At the generic level, significant differences were detected in the sample, Wilks’K
¼ 0.003, F(72, 533.541) ¼ 13.599, P <0.001. Subsequent
ANOVA of the partial warps generated post hoc Bonferroni comparisons that showed several significant differences at a 0.0000643 a-value (summarized in Table 3).
Among lemuriform taxa, significant differences were
noted between most other lemuriform and lorisiform
genera, with the exception of between 1) Lepilemur and
Avahi, Otolemur, Perodicticus, and Nycticebus, 2) Propithecus and Avahi and, 3) Eulemur and Lemur. Fewer
significant differences were noted between lorisiform
taxa; in fact, the only difference at the 0.000064 a-level
was noted between Loris and Otolemur. In addition, no
significant differences were observed between either Otolemur, Loris, Nycticebus with Tarsius, or between Loris
and Tupaia. In comparing the sample using five dietary
categories (frugivory, omnivory, folivory, insectivory, and
graminivory), significant differences were detected in the
sample, Wilks’ K ¼ 0.050, F(24, 367.511) ¼ 20.892, P <
0.001. Subsequent ANOVA-derived post hoc Bonferroni
comparisons for individual partial warps reveal statistical differences among all dietary groups.
Principal Components Analysis
A PCA of the partial warps for the lower first molar
indicates that the first two principal components (PCs)
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WHITE
TABLE 3. Summary of post hoc Bonferroni comparisons between taxonomic groups
TARS
TARS
GAL
OTO
PERO
LOR
NYCT
LEP
LEM
HAP
EULM
PROP
AVH
TUP
SD
N/A
SD
N/A
N/A
SD
SD
SD
SD
SD
SD
SD
GAL
OTO
PERO
LOR
NYCT
LEP
LEM
HAP
EULM
PROP
AVH
TUP
SD
N/A
N/A
SD
N/A
N/A
N/A
N/A
SD
N/A
N/A
N/A
N/A
N/A
N/A
SD
SD
N/A
N/A
SD
N/A
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
N/A
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
N/A
SD
SD
SD
N/A
SD
SD
SD
SD
N/A
SD
SD
SD
SD
SD
SD
SD
N/A
N/A
N/A
N/A
SD
SD
SD
SD
SD
SD
SD
N/A
SD
N/A
N/A
SD
SD
SD
SD
SD
SD
N/A
N/A
N/A
SD
SD
SD
SD
SD
SD
N/A
SD
SD
SD
SD
SD
SD
N/A
N/A
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
N/A
SD
SD
N/A
SD
SD
SD
SD
SD
SD
SD
SD
SD
SD
N/A
SD
SD
‘‘SD’’ notates the presence of a significant difference at the 0.000064 a-level. ‘‘N/A’’ denotes no significant difference.
TARS, Tarsius; GAL, Galago; OTO, Otolemur; PERO, Perodicticus; LOR, Loris; NYCT, Nycticebus; LEP, Lepilemur; LEM,
Lemur; HAP, Hapalemur; EULM, Eulemur; PROP, Propithecus; AVH, Avahi; TUP, Tupaia.
account for 70.53% of the total variation within the sample; 48.59% and 20.94% are explained by the first and
second axes, respectively (Table 4). The third PC
accounted for an additional 14.62%. The dispersion of
genera and dietary groups along the first three PCs is
illustrated in Figs. 5 through 8. Along the first axis, primate and non-primate insectivores are found at the minimum
values,
whereas
lemurid
graminivores
(Hapalemur) and frugivores are located at the maximum
values. As illustrated in Figs. 5 and 6, shape variation
along the first axis appears to correlate with the dimensions of the talonid basin, represented by the relative
positions of the entoconid, hypoconid, and the COPRLPHD point. At the minimum range of PC1 values,
the relative position of the five molar landmarks results
in a short, wide tooth characterized by a relatively short,
wide talonid basin. At maximum values, the overall
dimensions of the tooth indicate a combination of a long,
narrow molar with a long, narrow talonid basin. Additionally, the CO-PRLPHD occupies a relatively central
location (toward the midline of the tooth) at minimum
values, whereas it shifts in a relatively more buccal
direction at maximum values (Figs. 5 and 6). These
results suggest that the cristid obliqua, a major shearing
structure of the lower molar, provides midline shearing
capabilities at minimum values along the first axis. At
maximum values, the cristid obliqua runs along the buccal border of the tooth, serving as an external shearing
structure (Figs. 5 and 6).
Along the second axis (representing 20.94% of the
total variation), shape differences appear to correlate
with the relative location of the CO-PRLPHD point, and
the position of the protolophid relative to the long axis
(anteroposterior axis defined by the line between the
protoconid and hypoconid) of the tooth (Figs. 5 and 6).
At maximum values, the CO-PRLPHD is positioned centrally, while the protolophid lies at a more acute angle
relative to the anteroposterior (AP) axis of the tooth. At
minimum values along the second principal axis, the
protolophid lies at a relatively more perpendicular angle
to the long axis of the tooth. In addition, along the minimum range of values, the CO-PRLPHD occupies a postero-buccal position. In comparing PC1 and PC3, further
patterns emerge, although the third PC accounts for
TABLE 4. Summary of the relative warps
analysis (principal components analysis of shape)
and the percentage of variation explained by
individual components
Component
1
2
3
4
5
6
Percentage of
variance explained
Cumulative percentage
of variance explained
49.581
20.948
14.627
6.953
5.143
2.748
49.581
70.529
85.156
92.109
97.252
100
only 14.62% of the total shape variation (Figs. 7 and 8).
Shape deformations along PC3 suggest variation in the
length of the cristid obliqua and the position of the COPRLPHD intersection. Along PC3 (Y-axis), frugivorous
prosimians (e.g., Eulemur and Hapalemur) overlap with
some insectivorous taxa (e.g., Galago and Tarsius) exhibiting a shortened cristid obliqua and a buccal placement
of the CO-PRLPHD point, whereas prosimians which
incorporate a significant proportion of leafy matter in
their diet (e.g., Propithecus, Avahi, and Lemur) are distinct. This latter group does overlap, however, with the
spread of Tupaia, an insectivorous non-primate and
exhibits a lengthened cristid obliqua and a midline position of the CO-PRLPHD point. This is a surprising
result, given that Tupaia does not appear to overlap
along PC3 with insectivorous primate taxa, suggesting a
somewhat differing pattern of relative landmark position
in insectivorous mammalian taxa. Additionally, in certain generic groups (such as Eulemur and Propithecus)
in which several specific and sub-specific groups are recognized, a large spread is observed (Fig. 7); this may further suggest differentiation within generic groups and
would warrant a future investigation of shape difference
within these genera.
DISCUSSION
Geometric morphometric analyses facilitate linkages
between raw data and biological patterns, and can be
MOLAR DIVERSITY IN LEMURS AND LORISES
709
Fig. 5. Principal components analysis of shape scatter plot (PC1 and PC2) and associated shape
change (N ¼ 115). Shape deformation along is illustrated at the extreme values for each axis. The ‘‘consensus’’ form is included in the lower left corner of the figure. Taxonomic symbols follow Fig. 3.
used to explore morphological shape. Here, it was
hypothesized that tooth shape should vary significantly
with broad dietary categories among the primate taxa
examined here. My results suggest that my hypothesis
is supported. Certainly, there is a level of phylogenetic
influence in that lemuriform and lorisiform taxa separate along relative warp axes. Thus, phylogenetic relationships should not be discounted in any morphological
interpretation (Yamashita, 1998a). It would certainly be
preferable to additionally investigate the correlation
between taxonomic classification, size, and dietary
behavior in a multi-factorial interaction model. Unfortunately, given that some of the generic groups are also
the only representative of a dietary category (for example, Hapalemur is the only graminivore in the sample),
such analyses are not possible statistically due to the
limited sample size. Overall, however, the results of the
analyses performed here document particular shape
trends that are associated with dietary behavior.
Effect of Allometry on Molar Shape Trends
As indicated above, a moderate allometric relationship
was demonstrated between tooth size and shape (multiple r2 ¼ 0.61), with only 27% of the shape variation in
the sample predicted by size. Thus, the following sizeshape relationships can be summarized (Figs. 3 and 4).
1. Smaller teeth generally exhibit relative landmark
locations indicating a short, wide tooth (dietary association with insectivory and omnivory).
2. Larger teeth generally exhibit a pattern of landmarks
indicating a long, narrow tooth (dietary association
with frugivory and graminivory).
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Fig. 6. Principal components analysis of shape scatter plot (PC1 and PC2) and associated shape
change (N ¼ 115). Shape deformation along is illustrated at the extreme values for each axis. The ‘‘consensus’’ form is included in the lower left corner of the figure. Dietary symbols follow Fig. 4.
Non-Allometric Shape Trends
Although size appears to be a factor in shape variation, 74% of the shape variation in the sample did not
correlate with size. We can further summarize shape
trends along the first three principal components that
appear to distinguish between dietary behavioral patterns, rather than body size, as (Fig. 9):
1. Frugivorous Taxa: Larger talonid crushing areas, produced by the ‘‘perpendicular’’ position of the protolophid and the buccal position of the cristid obliqua.
Talonid shearing structures are positioned buccally. It
is important to note that Hapalemur (not a frugivorous prosimian) also exhibits a similar morphology,
possibly reflecting several phylogenetic or functional
factors (as discussed further below).
2. Folivorous Taxa: More midline shearing structures
with an oblique position of the protolophid and the
midline position of the cristid obliqua. Hypoflexid
crushing areas are generally larger than in
frugivores.
3. Insectivores: A relatively ‘‘perpendicular’’ position of
the protolophid (as in frugivores), paired with a more
midline position of the cristid obliqua (as in folivores),
result in midline shearing structures, albeit broader
talonid crushing areas than in folivores.
Variation between taxonomic and dietary groups
appears to be driven by the relative positions of the cristid obliqua, the protolophid, and the relative dimensions
of the talonid basin. The relative location of shearing
and crushing structures has direct implications for functional morphology. Occlusal wear patterns in primates
MOLAR DIVERSITY IN LEMURS AND LORISES
711
Fig. 7. Principal components analysis of shape plot (N ¼ 115) illustrating PC1 and PC3. Taxonomic
groups are as follows: !, Avahi; *, Propithecus; l, Eulemur; þ, Hapalemur; ~, Lepilemur; $, Nycticebus; n, Galago; ^, Loris; h, Otolemur; |, Perodicticus; 3, Tarsius; , Tupaia; 3, Lemur.
have been discussed at length in the relevant literature
(Kay and Hiiemae, 1974; Hiiemae, 1984) and suggest
that during initial stages of Phase I occlusion, the cristid
obliqua of the lower molar opposes the postparacrista on
the upper molar (Fig. 10). As Phase I occlusion continues, the protolophid of the lower molar also contacts the
preprotocrista of the upper molar, ending with the
crushing action accomplished through the non-parallel
position of the cristid obliqua with the preprotocrista.
The function of the cristid obliqua is further constrained
by the presence and size of the paraconule on the upper
molar.
In individuals with a relatively buccal location of the
CO-PRLPHD, the grinding surface of the anterior talonid basin is increased. In addition, as the talonid area
increases, the basin area available for retention of food
items also increases. On the other hand, a relatively
midline location of the CO-PRLPHD may provide
increased available crushing surface in the hypoflexid
region (buccal to the cristid obliqua) (Fig. 2). Thus, the
variation in the location of central shearing, crushing,
and grinding complexes (represented by the relative
positions of the landmarks examined here) may correlate
with differing food properties.
The results provide evidence of additional morphological differences between extant folivorous, frugivorous,
and omnivorous prosimians. Establishing morphological
differences between insectivores and folivores has been
difficult because the physical properties of leaf-structures and exoskeletal structures may demand similar
tooth adaptations (tall cusps, expanded shearing surfaces). In many cases, the discernment of folivorous and
insectivorous taxa using molar morphology often necessitates the inclusion of body size data (Kay, 1975; Kay and
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Fig. 8. Principal components analysis of shape plot (N ¼ 115) illustrating PC1 and PC3. Dietary groups
are as follows: *, graminivorous; l, insectivorous; þ, frugivorous; ~, folivorous; h, omnivorous.
Covert, 1984). Interpretation of shape, as represented
here by the relative location of occlusal landmarks, is
not dependent on a known estimate of body size. Future
analyses incorporating smaller-sized primate insectivores will further test the shape associations discussed
here. In addition, it is necessary to model these patterns
against physical properties of food (such as hardness or
chemical properties) to explore correlations with shape
variation.
Although not mutually exclusive (Lockwood, 2007),
these results highlight the simultaneous influence of
both function and/or phylogeny in morphology. For
example, Propithecus is generally classified as ‘‘folivorous’’ while including a large proportion of fruit items
(and seeds) in its diet (Meyers and Wright, 1993; Hemingway, 1995; Dew and Wright, 1998; Overdorff and
Strait, 1998; Simmen et al., 2003; Powzyk and Mowry,
2003). Here, Propithecus did not group exclusively with
other folivorous taxa (Avahi and Lepilemur) or frugivo-
rous lemurs in the comparison of the first two Principal
Components (Fig. 5). Rather, of the two indriids included
in the sample, Propithecus did exhibit a tooth with a relatively more buccal CO-PRLPHD and a less oblique protolophid, as in frugivores. Propithecus may exhibit tooth
morphology somewhat similar to Avahi as a result of
phylogenetic relationships, but this may also reflect a
functional convergence to similar shearing requirements
(as measured, for example, by shearing quotients). Upon
closer inspection, characteristics of an ‘‘indriid-type’’
tooth can vary in some details that may be related to dietary function (particularly the size of crushing areas).
These results for indriids (i.e., the presence of a phylogenetic shape signal overlaid on tooth morphology)
would seem to bolster current understanding of evolutionary diversification in indriids, particularly in light of
genetic data that suggests folivorous Avahi represents
the sister-group of Propithecus and Indri (tooth data not
presented here) (Rumpler et al., 1988; Razafindraibe
MOLAR DIVERSITY IN LEMURS AND LORISES
Fig. 9. Summary of shape patterns in dietary groups, (a) frugivory (Eulemur, FMNH 129378); (b) insectivory (Tarsius, FMNH 76860); (c) folivory (Lepilemur, FMNH 5658). Landmark designations follow Fig. 2.
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Fig. 10. Illustration of occlusal relationships between the protolophid, cristid obliqua, preprotocristia,
and postparacrista in primates (as figured for adapiform Leptadapis magnus) (adapted from Gingerich,
1972): (a) positions of the protolophid, cristid oblique, and postparacrista, (b) positions of the protolophid,
cristid oblique, and the preprotocrista.
et al., 1997; Roos et al., 2004). Moreover, it should be
noted that the folivorous Lepilemur, a lepilemurid, is
also characterized by morphology most similar to that of
Avahi. This result potentially strengthens the inferred
linkage between dietary adaptation and the landmark
patterns reported here. Certainly, these inferences must
MOLAR DIVERSITY IN LEMURS AND LORISES
Fig. 11. Summary of shape trends observed in the current study.
Symbols indicate: ~, short, wide tooth, midline CO-PRLPHD, perpendicular protolophid, and large crushing areas (Insectivores); , long,
narrow tooth with oblique protolophid and small crushing areas
(Folivores); *, short, wide tooth, buccal CO-PRLPHD, perpendicular
protolophid, and large crushing areas (Frugivores/Graminivores);
, intermediate shape. Branch lengths are not intended to indicate evolutionary time or distance.
*
be further explored using material from the Malagasy
lemur fossil record (sub-fossil material, for example)
before firmer statements regarding the dietary diversification of indriids may be proposed.
Likewise, the shape of the talonid basin observed in
Hapalemur may also be a result of both phylogenetic
and functional ‘‘co-opting’’ and compromise (Yamashita,
1996, 1998a,b) in which a feature originally efficient at
processing hard seeds and fruit may have also been suitable for efficient mastication of bamboo stems and
shoots. Similar functional demands related to ‘‘puncturecrushing’’ for processing both bamboo shoots and fruits/
seeds, rather than shearing and grinding (as in folivorous primates) (Seligsohn and Szalay, 1978), may be
influencing the molar shape patterns reported here.
Thus, these data are not incompatible with a phylogenetic hypothesis in which the ancestral lemurid was frugivorous (or graminivorous). Both Hapalemur and
Propithecus serve as illustrative cases that suggest phylogeny and function play important, integrated roles in
understanding the morphological adaptation, which
should not necessarily be considered independently
when inferring diet.
Lorisiforms (lorises and galagos), which tend to exhibit
a more variable or omnivorous dietary pattern (in particular Perodicticus, Otolemur, and Nycticebus) (CharlesDominique, 1977; Fleagle, 1999; Wiens, 2002), lie in an
intermediate position at the intersection between the
ranges of primarily frugivorous, folivorous, and insectivorous taxa. With the exception of Loris, the lorisiform
taxa included here overlap in shape trends with one
another, which may reflect common phylogenetic patterns or a relative lack of morphological specialization.
Although Loris is characterized here as ‘‘omnivorous,’’ it
is notable that field observations have documented a
high degree of insectivory (Nekaris and Rasmussen,
2003). In this analysis, of the omnivorous lorisids, Loris
715
groups most closely with other insectivorous taxa (particularly Tupaia). Otolemur and Nycticebus lie in positions along PC1 and PC2 intermediate between
insectivorous taxa and folivorous Lepilemur and indriids
(Fig. 5).
Thus, shape patterns in relative cusp and crest positions that overlap taxonomic groups serve to strengthen
confidence in the proposed functional correlations suggested here. For example, the overall similarity in insectivore tooth shape (both primate and non-primate)
suggests insectivory may be associated with a particular
cusp and crest pattern. In addition, functional relationships can also be used to evaluate fossil taxa when utilized
in an appropriate phylogenetic
context.
Morphological data should not be conceived of as static,
but rather as a component of ecological data that provides a dynamic picture of adaptation and ecological
change. Accordingly, examination of fossil material can
result in the development of innovative views of change
in community ecology and ecogeography through time
(Albrecht et al., 1990; DiMichele, 1994; Fleagle and
Reed, 1996; Lehman et al., 2005). For example, food
resource quality, food availability, ecological variability
(e.g., wet vs. dry forests), and diminishing soil quality
are all continual pressures facing modern lemurs, particularly those dependent on fruits (Ganzhorn et al., 1999).
Recent studies have suggested that certain folivorous
Lemur species may be more capable of adapting to the
change in forest ecology on Madagascar than other more
‘‘specialized’’ taxa (Lehman et al., 2006a,b).
Implications and Summary
The present analysis adds to extensive previous
groundwork by investigating patterns of molar shape
through exploration of cusp and shearing crest morphology, both components of molar morphology shown to develop early in embryonic development. The benefit of
having several methods to pursue is obvious: with different strategies, we are provided the opportunity to test
dietary hypotheses from several angles. Several different
methods have been previously introduced to address the
association between body size and dietary adaptation.
For example, measurements of shearing, grinding, and
crushing, combined with a measure of body size, appear
to be indicative of dietary patterns. Although insectivores and folivores each exhibit parallel patterns of welldeveloped shearing capacities, only with a measure of
body size they are distinguishable (Kay, 1975). In general, insectivores also exhibit larger molars in relation to
either frugivorous or folivorous primates of similar size.
Crown area alone, however, may not sufficiently explain
functional differences between primate taxa (Gingerich
and Smith, 1984).
As the goal of this work was to provide a comparative
sample from which to infer dietary behavior in fossil primates, a method that did not require body size was preferable. By employing techniques analyzing the relative
location of landmarks as described in the present study,
insectivores, folivores, and frugivores were shown to exhibit distinctive shapes without the necessity of body
size comparison. Thus, documenting how the relative
location of occlusal features of the tooth is effected by
size augments the results of Kay (1975) and others, adding a new dimension to the previous investigation of size
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and molar shape in primates ideally suited to interpreting diet from incomplete fossil remains.
Certainly, it would be short-sighted to suggest that the
method presented here for inferring dietary specialization provides a complete picture. Since dietary specialization can be defined at the evolutionary, functional, and
behavioral level (Ferry-Graham et al., 2002), various
approaches will yield different but complimentary
results. For example, information concerning an individual’s dietary behavior gained through microwear analysis provides a valuable amount of information regarding
the environment and food items available to that individual during a discreet slice of time. However, that
individual may exhibit a ‘‘specialist’’ or ‘‘generalist’’
microwear pattern due to ecological constraints, competitive populations, or food availability at a specific point in
time, and may not fully reflect its evolutionary background and the adaptive pattern of an ancestral population (Ferry-Graham et al., 2002). Thus, data concerning
an individual’s lifetime paired with data that reflect
upon evolutionary ancestry and adaptation provide a
broad picture of ecological change, population behavioral
patterns, and morphological adaptation that has been
canalized through genetic processes (Polly, 2006). Furthermore, although a match in interpretation from all
sides may be convenient, we must not overlook the value
that these methods provide when they offer counterinterpretations, prodding us to search our functional
questions more deeply.
To summarize, it was hypothesized and supported
here that primate and non-primate taxa would differ in
the relative shape and position of dental structures, and
that these differences could be discussed in terms of
functional demands placed on the organism as an adaptation to a particular dietary regime.
Using a geometric morphometric approach to investigating the relative position of major occlusal structures
in the first lower molar of strepsirrhine primates, the
shape trends observed are illustrated in Figs. 9 and 11,
and can be summarized as:
1. Frugivorous Taxa: ‘‘Perpendicular’’ position of the protolophid; buccal position of the cristid obliqua; larger
talonid crushing areas.
2. Folivorous Taxa: Oblique position of the protolophid;
midline position of the cristid obliqua; smaller talonid
crushing areas; expanded hypoflexid.
3. Insectivores: ‘‘Perpendicular’’ position of the protolophid; midline cristid obliqua; enlarged talonid and
hypoflexid regions.
Considering the phylogenetic closeness of extant lemur
and lorisiforms to fossil adapiforms, these data provide a
broad base from which to compare molar shape and
draw conclusions regarding dietary trends. This is not to
suggest, however, that adapiforms will be expected to
replicate this pattern, or that they are directly ancestral
to either living lemurs or lorises. What these data do
provide is a comparative baseline from which to propose
hypotheses of dietary adaptation and allometric molarshape scaling trends in adapiforms. The body size of
adapiforms has been suggested to be fairly broad [100–
6900 g (Fleagle, 1999)], and future comparisons will
bear out whether adapiforms exhibit similar relation-
ships between size and molar shape. This analysis also
suggests that certain features of the molar, such as the
position of the protolophid and the cristid obliqua, and
the breadth of the anterior talonid basin, may be related
to functional demands for shearing and/or crushing.
Thus, if differentiation in these features is also documented among adapiforms, further functional hypotheses may be posited regarding this diverse fossil group.
These results and the approach used here strongly encourage the collaborative use of several lines of morphological data to reveal the most complete picture of
dietary adaptation among fossil primates. Moreover, this
approach, in combination with other previously successful methods, suggests that understanding behavioral
and ecological diversity is always enhanced by the combination and comparison of different methods.
ACKNOWLEDGMENTS
The author thanks the members of the University of
Iowa dissertation committee for their valuable assistance: Dr. Russell Ciochon (UI–chair), Dr. Robert Franciscus (UI), Dr. James Enloe (UI), Dr. Christopher
Brochu (UI), and Dr. Gregg Gunnell (University of Michigan). She is further indebted Dr. Matthew Bonnan
(WIU) and Dr. Gregg Gunnell (UM) for their comments
and lengthy discussions in regard to this project since
the completion of her dissertation. Her gratitude is
extended, as well, to the following for their valuable assistance in accessing mammal collections at their institutions: Dr. Gregg Gunnell (UM Museum of
Paleontology), William Stanley (Field Museum, Chicago),
Minh-Tho Schulenberg (Field Museum, Chicago), Eileen
Westwig (American Museum Natural History, New
York), Linda Gordon (National Museum of Natural History, Smithsonian Institution, Washington, DC). She also
wants to recognize the conveners and participants of the
2006 Vienna MORPHOFEST for their invaluable advice
and assistance. Finally, she owes thanks to the following
for their continuing support: Steven Miller, Lindsay
Eaves-Johnson, Sara Filseth, Susan Meiers, and Matthew Bonnan.
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