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Biological variation in a large sample of mouse lemurs from Amboasary, Madagascar: Implications for interpreting variation in primate biology and paleobiology

Authors:
Biological variation in a large sample of mouse lemurs from Amboasary,
Madagascar: Implications for interpreting variation in primate biology and
paleobiology
Frank P. Cuozzo
a
,
b
,
*
,
1
, Emilienne Rasoazanabary
c
, Laurie R. Godfrey
c
, Michelle L. Sauther
b
,
Ibrahim Antho Youssouf
d
, Marni M. LaFleur
b
a
Department of Anthropology, University of North Dakota, 236 Centennial Drive, Stop 8374, Grand Forks, ND 58202-8374, USA
b
Department of Anthropology, University of Colorado, Campus Box 233, Boulder, CO 80309-0233, USA
c
Department of Anthropology, University of Massachusetts, 240 Hicks Way, Amherst, MA 01003, USA
d
Département des Sciences Biologiques, Université de Toliara, BP 185, Toliara, Madagascar
article info
Article history:
Received 21 February 2012
Accepted 23 August 2012
Available online 11 December 2012
Keywords:
Microcebus griseorufus
Teeth
Pelage
Individual variants
Taxonomy
Paleobiology
Species
Beza Mahafaly
Lemur catta
abstract
A thorough knowledge of biological variation in extant primates is imperative for interpreting variation,
and for delineating species in primate biology and paleobiology. This is especially the case given the
recent, rapid taxonomic expansion in many primate groups, notably among small-bodied nocturnal
forms. Here we present data on dental, cranial, and pelage variation in a single-locality museum sample
of mouse lemurs from Amboasary, Madagascar. To interpret these data, we include comparative infor-
mation from other museum samples, and from a newly collected mouse lemur skeletal sample from the
Beza Mahafaly Special Reserve (BMSR), Madagascar. We scored forty dental traits (n¼126) and three
pelage variants (n¼19), and collected 21 cranial/dental measures. Most dental traits exhibit variable
frequencies, with some only rarely present. Individual dental variants include misshapen and super-
numerary teeth. All Amboasary pelage specimens display a reversed Von the cap, and a distinct dorsal
median stripe on the back. All but two displayed the dominant grayebrown pelage coloration typical of
Microcebus griseorufus. Cranial and dental metric variability are each quite low, and craniometric vari-
ation does not illustrate heteroscedasticity. To assess whether this sample represents a single species, we
compared dental and pelage variation to a documented, single-species M. griseorufus sample from BMSR.
As at Amboasary, BMSR mouse lemurs display limited odontometric variation and wide variation in non-
metric dental traits. In contrast, BMSR mouse lemurs display diverse pelage, despite reported genetic
homogeneity. Ranges of dental and pelage variation at BMSR and Amboasary overlap. Thus, we conclude
that the Amboasary mouse lemurs represent a single species emost likely (in the absence of genetic
data to the contrary) M. griseorufus, and we reject their previous allocation to Microcebus murinus.
Patterns of variation in the Amboasary sample provide a comparative template for recognizing the
degree of variation manifested in a single primate population, and by implication, they provide minimum
values for this speciesintraspecic variation. Finally, discordance between different biological systems in
our mouse lemur samples illustrates the need to examine multiple systems when conducting taxonomic
analyses among living or fossil primates.
Ó2012 Elsevier Ltd. All rights reserved.
Introduction
Mammalian teeth are diagnostic morphologically, often identi-
able to the level of species (e.g., Roth, 2005). As such, patterns of
dental variation provide important information for understanding
the taxonomy of living and extinct primates (e.g., Schwarz, 1931;
Schuman and Brace, 1954;Swindler et al., 1963;Greene, 1973;
Gingerich, 1974;Johanson, 1974;Swindler and Orlosky, 1974;
Gingerich and Schoeninger,1979;Cope, 1989,1993;Vitzhum, 1990;
Cope and Lacy, 1992,1995;Plavcan, 1993;Uchida, 1998a,b;Sauther
et al., 2001;Cuozzo, 2002,2008;Tornow et al., 2006;Scott et al.,
2009;Pilbrow, 2010). Plavcan and Cope (2001: 206) emphasized
that comparative analyses of biological variation should be based
on data from restricted geographic localities and time horizons.
*Corresponding author.
E-mail address: frank.cuozzo@email.und.edu (F.P. Cuozzo).
1
Current address: Department of Anthropology, University of Colorado-Boulder,
Campus Box 233,Boulder, CO 80309, USA. Tel.:þ1 303 492 1712;fax: þ1 303 492 1871.
Contents lists available at SciVerse ScienceDirect
Journal of Human Evolution
journal homepage: www.elsevier.com/locate/jhevol
0047-2484/$ esee front matter Ó2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.jhevol.2012.08.007
Journal of Human Evolution 64 (2013) 1e20
Kieser (1994) made a similar suggestion, addressing the impor-
tance of choosing an appropriate reference population. Tornow
et al. (2006) noted that there are few such samples of extant
primates available for comparison. To date, most studies of dental
variation within extant species have focused on anthropoid and/or
haplorhine primates, or even more narrowly, on hominoids, which
hold keys for ascribing hominin fossils to particular taxa (e.g.,
Schuman and Brace, 1954;Swindler et al., 1963;Greene, 1973;
Johanson, 1974;Swindler and Orlosky, 1974;Cope, 1989,1993;
Vitzhum, 1990;Rosenberger et al., 1991;Wood et al., 1991;Plavcan,
1993;Swindler et al., 1998;Uchida, 1998a,b;Pan and Oxnard, 2003;
Tornow et al., 2006;Hlusko and Mahaney, 2007;Scott et al., 2009;
Pilbrow, 2010).
By contrast, most previous studies of dental variation in strep-
sirrhine primates have focused on interspecic variation, with an
emphasis on species descriptions and phylogenetic relationships
(e.g., Schwarz, 1931;Hill, 1953;James, 1960;Swindler, 1976,2002;
Schwartz and Tattersall, 1985;Tattersall and Schwartz, 1991;
Tattersall, 1993;Groves and Helgen, 2007). Fewer studies have
addressed patterns of intraspecic dental variation in strepsir-
rhines (Eaglen, 1986;Kieser and Groeneveld, 1989;Schwartz and
Beutel, 1995;Sauther et al., 2001;Cuozzo, 2008). Given the
primary role of variation as the target of natural selection (e.g.,
Darwin, 1859;Simpson, 1944; see; Bowler, 2005), understanding
the ranges of variation in populations and/or species can provide
insights into the amount of variation available for selection and/or
drift. Assuming morphological variation correlates with reproduc-
tive isolation, the central component of the Biological Species
Concept (Mayr, 1940,1942,1988; see review in Tattersall, 2007),
individual variants can be important for assessing species bound-
aries in the mammalian fossil record (e.g., Goodwin, 1998). Yet, such
variation in strepsirrhine primates remains underexplored
(Sauther and Cuozzo, 2008; see summary data in Miles and
Grigson, 1990).
Mouse lemurs (Microcebus) have been the focus of increased
attention in recent years, but their intraspecic patterns of bio-
logical variation (i.e., dental, cranial, and pelage) remain poorly
documented, and taxonomic inferences are often drawn on the
basis of limited information and small samples (see critiques in
Tattersall, 2007;Godfrey, 2011). Mouse lemurs are the smallest
living primates (Rasoloarison et al., 2000), and traditionally, only
two mouse lemur species have been recognized ethe western
gray mouse lemur (Microcebus murinus) and the eastern reddish-
brown form (Microcebus rufus)(Hill, 1953;Tattersall, 1982;
Atsalis et al., 1996;Rasoloarison et al., 2000;Yoder et al., 2000a,b,
2002;Heckman et al., 2006;Gligor et al., 2009). However, the
taxonomy of mouse lemurs, as with many of the smaller nocturnal
strepsirrhine forms (e.g., the dwarf galagos of continental Africa
[Bearder et al., 1995;Honess, 1996;Wickings et al., 1998;Bearder,
1999;Nekaris and Bearder, 2007]), has recently undergone revi-
sion, with the two long-standing species now divided into as many
as 19 distinct species on the basis of morphological, biogeographic,
and/or genetic data (e.g., Yoder et al., 2000a,b;Rasoloarison et al.,
2000;Radespiel et al., 2003,2008,2012;Andriantompohavana
et al., 2006;Louis et al., 2006,2008;Olivieri et al., 2007;
Mittermeier et al., 2010;Weisrock et al., 2010; see Tab le 1),
although this dramatic increase in the number of described species
has been contested (e.g., Tattersall, 2007). Recent years have also
witnessed a growth in mouse lemur behavioral and/or ecological
studies (e.g., Atsalis, 1998,2007;Rasoazanabary, 2004,20 06;
Lahann et al., 2006;Eberle and Kappeler, 2008;Dammhahn
and Kappeler, 2008;Génin, 2008,2010; see review in Atsalis,
2007), as well as expanded genetic analyses capable of recog-
nizing instances of incomplete lineage sorting (Heckman et al.,
2007).
Heckman et al. (2006) concluded that, despite substantial
variation in pelage characters, individuals belonging to a sample of
mouse lemurs, collected across multiple habitats in and around
the Beza Mahafaly Special Reserve (BMSR) in southern
Madagascar exhibit identical mitochondrial haplotypes (cyto-
chrome b), and thus appear to represent a single species. These
observations contravened the hypothesis originally posited on the
basis of three distinct color variants (e.g., Rasoazanabary, 2004),
that at least two and perhaps three species are represented in the
sample. Thus, Heckman et al. (20 06) made a plea for a careful
consideration of the degree to which observed variation can be
contained in a single population or species. A parallel case can be
made for dental variation (see review of lemur dental variation in
Cuozzo and Yamashita, 2006), which becomes critical if dental
variants are to be used in diagnosing species boundaries within
the fossil record (e.g., Tattersall, 1992;Goodwin, 1998;Cuozzo,
2008). At the very least, we need to examine variation in
multiple biological systems when contemplating extant or fossil
taxonomic boundaries.
Research questions
The American Museum of Natural History (AMNH) (New York)
houses one of the largest single-locality skeletal and soft tissue
samples of mouse lemurs available for study (n¼181 [Buettner-
Janusch and Tattersall, 1985]). These specimens were collected in
October and November 1931 by Hans Bluntschli at Amboasary,
southern Madagascar. As noted above, at the time, most workers
viewed Microcebus as comprising two species, the western gray
mouse lemur (M. murinus) and the eastern reddish-brown form
(M. rufus), common to the more humid forests that mark the
eastern mountains of Madagascar. Amboasary is located in the far
southeastern part of Madagascar, below the Tropic of Capricorn,
and outside of the humid forest zones. Thus, this sample was
initially assigned to M. murinus (Buettner-Janusch and Tattersall,
1985). The AMNH collection represents only a portion of the
mouse lemur material amassed by Bluntschli at Amboasary, with
specimens distributed across institutions in the United States and
Europe, including Harvards Museum of Comparative Zoology, the
Museum für Naturkunde (Berlin) and the Muséum National
dHistoire Naturelle (Paris) (Buettner-Janusch and Tattersall, 1985).
Bluntschlis collection strategies, which included the collection of
Table 1
Currently recognized extant mouse lemur species.
a
Microcebus berthae (Madame Berthes mouse lemur)
Microcebus gerpi (Gerps mouse lemur)
Microcebus griseorufus (Reddish-gray mouse lemur)
Microcebus jollyae (Jollys mouse lemur)
Microcebus lehilahytsara (Goodmans mouse lemur)
Microcebus margotmarshae (Margot Marshes mouse lemur)
Microcebus mittermeieri (Mittermeiers mouse lemur)
Microcebus murinus (Gray mouse lemur)
Microcebus myoxinus (Pygmy mouse lemur)
Microcebus ravelobensis (Golden-brown mouse lemur)
Microcebus rufus (Brown mouse lemur)
Microcebus sambiranensis (Sambirano mouse lemur)
Microcebus simmonsi (Simmonsmouse lemur)
Microcebus tavaratra (Northern brown mouse lemur)
Microcebus mamiratra (Claires mouse lemur)
Microcebus lokobensis
b
(Lokoben mouse lemur)
Microcebus danfossi (Danfosss mouse lemur)
Microcebus bongolavensis (Bongolava mouse lemur)
Microcebus macarthurii (MacArthurs mouse lemur)
a
Data compiled from Yoder et al. (2000a,b),Rasoloarison et al. (2000),Louis et al.
(2006),Andriantompohavana et al. (2006),Mittermeier et al. (2008),Olivieri et al.
(2007), and Radespiel et al. (2008,2012).
b
M. lokobensis is apparently a synonym for M. mamiratra.
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e202
as many as 50 mouse lemurs in a single day (Bluntschli, 1933,1951),
would be anathema to contemporary conservation ideals. Thus, we
do not support further collection of such samples, but the collection
he assembled does provide a unique opportunity to examine bio-
logical variation in a single primate population, and makes use of
these sacriced lemurs. As noted by Yoder et al. (2005), such older
samples may be of critical importance for taxonomic analyses of
Malagasy vertebrates.
Recent study of mouse lemurs in the southeastern region of
Madagascar indicates the presence of both M. murinus and Micro-
cebus griseorufus (Yoder et al., 2002;Génin, 2008;Gligor et al.,
2009). For example, in and around the Berenty Private Reserve
(Yoder et al., 2002;Génin, 2008) less than 20 km from Amboasary,
M. murinus is described from the gallery forest and M. griseorufus in
the dry, spiny forest areas. Gligor et al. (2009) also note the pres-
ence of M. griseorufus in dry, spiny forests, as well as M. murinus in
the littoral and eastern humid forests, 25e30 km east of Amboa-
sary. They also recognize the presence of intermediatemorpho-
types of the two species in the small, remaining transitional forests
between the dry western and humid eastern forests. Hapke et al.
(2011) suggest that these intermediate morphotypes may repre-
sent true hybrids, a by-product of recent, short-term climatic
uctuations, a potentially important process in the diversication
of Madagascars lemurs.
The rst goal of our project was to assess 1) whether the AMNH
Amboasary mouse lemur sample represents a single species, and 2)
the taxonomic afnity of this sample, previously recognized as
M. murinus. To do this, we compared patterns of dental and pelage
variation with those from a known, single-species population of
M. griseorufus from Beza Mahafaly, including a newly collected
sample of dental remains from a cache of owl pellets recovered by
authors FPC, MLS, IAYJ, and MML in 2008. Our second goal was to
gain new insights into the biological variation within a single
primate species, and to explore the implications of such variation
for understanding primate biology and for diagnosing primate taxa,
particularly in paleobiology.
Materials and methods
Cranial and dental metric analyses
A total of 126 mouse lemur cranial and/or dental specimens at
the American Museum of Natural History AMNH were studied.
Only adult specimens were analyzed, with adult status deter-
mined by a fully erupted permanent dentition. Twenty-one cranial
and/or dental measures were collected (measure to the nearest
0.01 mm) using Fowler digital needle-point calipers, (see Table 2
for denition of each measure). All dental measurements were
taken using a Nikon SMZ-1 binocular scope, and were collected by
one person (FPC), thereby eliminating the potential for inter-
observer error. Measurements were collected from left tooth
positions when possible, and from right teeth only when
measurements of left teeth were not available due to damage or
pathology. A measurement reliability analysis was conducted by
taking measurements on a subset of the sample several months
after taking the original measurements. This analysis revealed
average measurement errors of 0.03 mm for M
1
length (n¼25),
0.04 mm for cranial length (n¼25), and 0.04 mm for M
1
width
(n¼25).
A comparable set of odontometric data was collected from
a sample of mouse lemurs from the Beza Mahafaly Special Reserve
(BMSR), southern Madagascar (also by FPC). This sample (n¼32)
includes nine cranial/dental specimens collected previously from
naturally deceased individuals at two separate locations, and
twenty-three new craniodental specimens recovered in July 2008
in a cache of owl pellets from the gallery forest area of BMSR. Owl
pellets and loose skeletal remains were collected at a large regur-
gitation site. The site encompassed an approximate 3 m radius
surrounding a large felled dead tree stump. Pellets were weighed,
measured and photographed before being immersed in water to
loosen compacted material (about two days). Loose bones were
soaked overnight in water if they had dirt, hair, chitin, or other
matter attached. After rinsing and drying for one day, bones were
separated and categorized, using the Beza Mahafaly Special Reserve
Museums comparative osteology collection (BMOC). Bones were
identied as bird, reptile, rodent or primate. The rodent genera
included both Rattus and Mus, while Microcebus was the sole
primate genus. As with the Amboasary sample, measurements
were collected from left tooth positions when possible, and from
right teeth only when measurements of left teeth were not avail-
able due to damage or pathology.
Quantitative assessment of cranial and dental metric variation
Summary statistics (mean, standard deviation, and coefcient
of variation) were calculated for each cranial and dental variable,
from both samples. All coefcients of variation (CVs) were cor-
rected for sample size following Sokal and Rohlf (1995) and
Plavcan and Cope (2001), as CVs are known to vary dramatically in
small samples (see discussion below). Odontometric data for the
two samples were compared using the Studentst-test, with
a signicance level of 0.05. All metric data were analyzed using
Statview statistical and data analysis software (Haycock et al.,
199 2).
The coefcient of variation has long been used as an analytical
tool in mammalian biology and paleobiology to assess specic
boundaries. The use of metric variation to assess taxonomic
boundaries in fossil forms, often based on odontometry, stems from
the expectation that, as noted by Cope and Lacy (1994), there is
little to suggest that patterns of dental variation would dramatically
differ between living and fossil mammals. The coefcient of vari-
ation is a numerical index dened as the standard deviation divided
by the mean, usually multiplied by 100 (e.g., Simpson et al., 1960;
Table 2
Denition of cranial and dental measurements.
1. Cranial length: Distance from the anterior border of the nasals to the
posterior boundary of the occiput.
2. Bizygomatic breadth: Distance between the outer margins of the zygomatic
arches, along the inferior border of the cranium.
3. Biorbital breadth: Maximum distance between the outer margins of the
orbits, measured horizontally across the orbits.
4. Palate breadth: Distance between the buccal edges of the third upper molars.
5. Maxillary toothrow length: Measured from the mesial edge of the canine to
the distal edge of the third upper molar, parallel to the toothrow.
6. Mandibular toothrow length: Measured from the mesial edge of the second
(caniniform) premolar to the distal edge of the third lower molar, parallel to
the toothrow.
7. First and second mandibular molar length: Measured parallel to the
toothrow, from the mesial edge of the paracristid to the distal border of the
postentocristid.
8. Third mandibular molar length: Measured parallel to the toothrow, from
the mesial border of the paracristid to the distal edge of the tooth.
9. Mandibular molar trigonid width: Measured as maximum width,
perpendicular to the toothrow.
10. Mandibular molar talonid width: Measured as maximum width,
perpendicular to the toothrow.
11. Maxillary molar length: Measured parallel to the toothrow, across the
paracone and metacone.
12. First and second maxillary molar width: Measured perpendicular to the
toothrow, across the metacone and hypocone.
13. Maxillary third molar width: Perpendicular to the toothrow, across the
paracone and protocone.
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e20 3
Carrasco, 1998;Plavcan and Cope, 2001;Van Valen, 2005). Use of
this statistic has received signicant attention over the years (e.g.,
Simpson, 1937;Simpson and Roe, 1939). Initially, a CV of greater
than 10 was interpreted as indicating a taxonomically diverse
sample (Simpson and Roe, 1939; Simpson et al., 1960; see review in
Plavcan and Cope, 2001). More recently, researchers have rened
this idea, noting that premolars generally exhibit more metric
variation than do molars (Gingerich, 1974;Gingerich and
Schoeninger, 1979), that third molars generally vary more than
rst and second molars (e.g., Gingerich, 1974;Sauther et al., 2001),
and that a contrast in metric variation between anterior and
posterior teeth (i.e., greater variability in canines vs. molars) indi-
cates sexual dimorphism rather than taxonomic diversity
(Gingerich, 1995).
The CV has remained an important measure with which to
assess taxonomic boundaries in primates and other mammals,
extant and extinct (e.g., Gingerich, 1974,1995;Cope, 1989,1993;
Cope and Lacy,1992,1995;Carrasco, 1998;Plavcan and Cope, 2001;
Cuozzo, 2002,2008;Tornow et al., 2006). Its use continues, despite
some limitations and critiques (e.g., Lande, 1977;Soulé, 1982;
Kelley and Plavcan, 1998;Polly, 1998;Plavcan and Cope, 2001; see
debate on the efcacy of CVs between; Kieser, 1994 and Cope and
Lacy, 1994). First, CVs are known to vary greatly in small samples
(e.g., Plavcan and Cope, 2001). Thus, use of the correction factor CV
[1 þ1/4(n)] is often required (e.g., Sokal and Rohlf, 1995;Plavcan
and Cope, 2001). Also, as noted by Lande (1977), CVs produced
from a set of correlated data, for example, measurement of a series
of cranial variables, or multiple measures from a single tooth, will
likely result in lower values than those collected from unrelated
variables. CVs can also only show the presence of multiple species
in an assemblage, but cannot generally illustrate that only one
species is present (Cope and Lacy, 1992;Carrasco,1998). In addition,
Polly (1998) noted that under certain circumstances CVs can be
size-dependent. For example, when comparing variables of
dissimilar size, CVs will vary according to size, with larger measures
displaying higher CVs. Because of these limitations, the CV is best
used as a rst approximationwhen assessing taxonomic
boundaries, especially in the fossil record, to eliminate the possi-
bility of multiple species (e.g., Carrasco, 1998;Cuozzo, 2008). Still,
when combined with analyses of dental morphology, and assessed
in the context of adequate data from appropriate comparative
samples, the CV can be a crucial rst approximation in assessing
taxonomic diversity among extinct forms (Kieser, 1994;Plavcan and
Cope, 2001;Tornow et al., 2006;Cuozzo, 2008). When identifying
species among living forms, additional measures and data analyses
(e.g., pelage and/or molecular information) are essential, as
described herein.
Dental morphology
A total of forty non-metric dental traits (Table 3) were scored for
both right and left dentitions (whenever possible) for all specimens
in both the Amboasary and Beza Mahafaly samples. Traits scored
came from prior studies of mouse lemur dentition (e.g., Forbes,
1894;Elliot, 1913;Hill, 1953;James, 1960;Swindler, 1976;
Schwartz and Tattersall,1985;Rasoloarison et al., 2000), as well as
initial, preliminary analyses of the AMNH sample by FPC. The
majority (28) of the forty scored traits have binary conditions: these
features were scored as presentwhenever they could be dis-
cerned, or absent. For these binary traits, the degreeof presence
was not scored (i.e., strong, weak, etc.), resulting in a very conser-
vative (i.e., condent) measure of trait presence. The remaining 12
traits represent tripartite conditions, with each trait appropriately
scored. Individual variants (i.e., supernumerary, abbreviated, and/
or connate teeth) were also recorded.
Pelage assessment
Pelage data from Amboasary were collected to aid our assess-
ment of the samples taxonomic afnity and to assess the single-
species diagnosis for this sample. Among the mouse lemurs at
Beza Mahafaly there exists a discordance between degrees of
variation in pelage and genetic traits. Specically, there is
substantial pelage variation but limited diversity in mitochondrial
DNA (cytochrome b) in this sample, taken by Heckman et al. (2006)
to represent a single species.
Most of the mouse lemur skulls and/or skeletons from Amboa-
sary in the AMNH Bluntschli collection lack skins. The population is
represented by 126 cranial specimens (most without associated
postcrania), and only 16 skins. These specimens were collected
during a 10 day period, in late October, 1931. No more than three
skins were kept during any given day during the collection period.
Thus, although derived from a small sample, these specimens
appear to have been randomly collected.Given the small number of
Amboasary Microcebus pelage specimens, we compiled a compar-
ative pelage database from a total of 72 dried skins scored at three
museums (Chicago Field Museum [FMNH], American Museum of
Natural History [AMNH], and the Museum of Comparative Zoology
at Harvard University [MCZ]). This database includes the 16 AMNH
Amboasary pelage specimens plus three specimens from Amboa-
sary housed at MCZ. In addition to the 72 museum pelage samples,
Table 3
Dental traits examined.
a
# Trait Conditions scored
1. C w/distal style Absent, present
2. P
2
paracone only Absent, present
3. P
3
w/protocone Absent, present
4. P
4
w/protocone Absent, present
5. M
1
pericone Absent, present
6. M
1
hypocone Absent, present
7. M
1
lingual extension/style Absent, present
8. M
1
parastyle Absent, present
9. M
1
metastyle Absent, present
10. M
1
shape Square, buccalelingual elongation
11. M
1
buccal cingulum Strong, weak, absent
12. M
2
pericone Absent, present
13. M
2
hypocone Absent, present
14. M
2
lingual extension/style Absent, present
15. M
2
parastyle Absent, present
16. M
2
metastyle Absent, present
17. M
2
shape Square, buccalelingual elongation
18. M
2
buccal cingulum Strong, weak, absent
19. M
3
pericone Absent, present
20. M
3
hypocone Absent, present
21. M
3
parastyle Absent, present
22. M
3
metastyle Absent, present
23. M
3
buccal cingulum Strong, weak, absent
24. P
2
caniniform Absent, present
25. P
2
buccal cingulum Strong, weak, absent
26. P
3
buccal cingulum Strong, weak, absent
27. P
4
thick buccal cingulum Absent, present
28. P
4
w/talonid Absent, present
29. P
4
entoconid position Central, lingual
30. M
1
shape Square, rectangular, parallelogram
31. M
1
buccal cingulum Strong, weak, absent
32. M
1
distal cingular shelf Strong, weak, absent
33. M
2
shape Square, rectangular, parallelogram
34. M
2
buccal cingulum Strong, weak, absent
35. M
2
distal cingular shelf Strong, weak, absent
36. M
3
buccal cingulum Strong, weak, absent
37. M
3
w/hypoconulid Absent, present
38. M
3
w/notch between
hypoconid/hypoconulid
Absent, present
39. M
3
w/cingulum in notch Absent, present
40. M
3
w/entoconid and hypoconulid Distinct, not distinct
a
See text for discussion of the identication of morphological traits examined.
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e204
ER collected eld data on pelage from a total of 196 live-caught
individuals at Beza Mahafaly between 2003 and 2004. Mouse
lemurs were captured using Sherman live animal traps (Sherman
Traps, Inc., Tallahassee, FL, USA), hand-sedated, and released in
their original capture area, with University of Massachusetts-
Amherst IACUC approval. All captured individuals at BMSR were
microchipped (Trovan, Identify UK, Ltd., East Yorkshire, HU13 0RD,
United Kingdom), so that recaptured individuals could be distin-
guished from rst captures, making it easy to eliminate any
duplication of individuals in the sample. Individuals were sampled
from three forests: the gallery and spiny forests within the Beza
Mahafaly Special Reserve, and a nearby mixed dry forest(Ihazoara).
Despite marked variation in coat coloration, these individuals have
been shown to belong to a single species; their DNA (cytochrome b)
matched reference samples of M. griseorufus from Berenty, while
diverging from reference samples of M. murinus from a variety of
locations (Heckman et al., 2006). In all, comparative pelage data
include samples from 19 sites (counting the three Beza locations as
a single site), and from individuals that have been attributed to
eight separate species (Table 4).
A Munsell (GretagMacbeth; New Windsor, New York) soil color
book was used as a reference in collecting the data on dried skins.
Colors in the Munsell book are coded by hue (i.e., specic color),
value (i.e., lightness or darkness), and chroma (i.e., color intensity),
and arranged on sheets of color chips that are perforated, so that
any sample can be matched easily to individual color chips. Similar
chips are assigned the same color names (e.g., strong brown,
yellowish brown). Although preservation of pelage specimens can
vary, thus possibly impacting their color, we assigned hue scores
allowing for a range of more and less faded shades of the same color
hues (i.e., not scoring obviously faded skins as a different hue), thus
controlling for some possible pelage degradation. ER used this
system to record the closest matching pelage colors for the
following regions on each specimen: interorbital, orbital ring,
nasals, cheeks, cap, shoulder and dorsal neck, middle back, rump,
throat, chest, middle belly, groin, proximal tail (dorsal and ventral),
distal tail (dorsal and ventral), dorsal thigh, dorsal leg, dorsal upper
arm, and dorsal forearm. Two additional pattern variables were
scored: the presence or absence of a distinct reversed Von the
cap, and the presence or absence of a distinct dorsal median stripe.
The reversed Vis a fork-like mark, which is darker (usually
browner or redder) than the surrounding fur; the lines begin just
above the eyes and converge to an apex at the back of the cap. For
any particular variable, not all individuals could be scored due to
damage on specimens.
For live-caught individuals, coat color was scored for the dorsal
region only, and the presence or absence of a reversed V and
a dorsal median stripe was also recorded. Dorsal fur color was
grouped into three categories: 1) gray (corresponding mainly to
Gray or Dark gray on the Munsell chart), 2) grayebrown (corre-
sponding mainly to Grayish brown, Dark grayish brown, or Dark
yellowish brown on the Munsell chart), and 3) redor dark brown
(corresponding mainly to Dark brown or Very dark brown on the
Munsell chart). Fur color varies on the dorsum of single individuals,
thus categoriesdesignate the dominant color of the dorsal pelage
(excluding the median stripe which, when distinct, is always darker
or browner than the surrounding fur).
We used StatXact (Cytel Studios) to test the null hypothesis of no
differences across taxa in the frequencies of the reversed V, dorsal
median stripe, and dorsal fur coloration (gray, grayebrown, or
red). This program allows one to calculate Fishers exact test for
the relationship between two variables in a row-by-column
frequency table of any size. We prefer this to the traditional Pear-
sons Chi-square or the maximum likelihood test for independence,
because the Chi-square estimates of the true probability value may
not be very accurate when the marginal values are strikingly
uneven or when one or more expected values are very small,
particularly when there are small expected values (less than ve) in
one or more of the cells. Fishers exact test provides the exact
probability of nding any given result (or more extreme differ-
ences) by chance alone (Agresti, 1990).
We rst tested the signicance of differences in frequency
distributions of coat characteristics for Amboasary and Beza
Mahafaly alone. We then used StatXact to assess the signicance of
frequency differences across the living and museum samples
studied herein. For these tests, the specimens from Amboasary
were treated as a distinct, unassigned population. For the purpose
of these broader statistical comparisons, we also omitted Micro-
cebus berthae and Microcebus sambiranensis, both of which were too
poorly sampled to capture meaningful patterns of variation.
Results
Cranial and dental metrics
Metric data for the 21 cranial and/or dental measures at
Amboasary are presented in Table 5a. Metric variation in the six
cranial measures is quite limited, with Coefcients of Variation
Table 4
Total comparative sample epelage analyses.
Comparative sample NSample eld locations Condition
M. griseorufus 196 Beza Mahafaly
(Gallery, Spiny
forest, Ihazoara)
Live
M. griseorufus 16 Beza Mahafaly, Tabiky Dried skins
M. griseorufus 19 Amboasary Dried skins
M. murinus 7 Andranomena
(Kirindy), Toliara,
Vohimena, Manamby
Dried skins
M. myoxinus 6 Aboalimena, Bemaraha,
Ambararatabe, Namoroka
Dried skins
M. ravelobensis 6 Ankarafantsika Dried skins
M. berthae 1 Kirindy Dried skins
M. rufus 9 Antsihanaka, Andampy,
Didy, Ivondro,
Tampina, Analamazaotra
Dried skins
M. tavaratra 5 Ankarana Dried skins
M. sambiranensis 3 Manongarivo Dried skins
Table 5a
Amboasary craniometric and odontometric summary statistics.
Measure NMean SD Range CV
Skull length 122 31.47 0.77 29.68e33.88 2.4
Biorbital breadth 120 19.90 0.61 18.56e21.70 3.1
Zygomatic breadth 117 20.12 0.67 18.60e21.59 3.3
Palate breadth at M
3
123 9.59 0.27 9.02e10.36 2.8
Maxillary toothrow 105 10.08 0.25 9.23e10.64 2.5
Mandibular toothrow 103 9.27 0.26 8.34e9.85 2.8
M
1
length 124 1.58 0.06 1.37e1.78 4.0
M
1
trigonid width 123 1.20 0.06 1.07e1.35 4.7
M
1
talonid width 123 1.27 0.06 1.17e1.40 4.3
M
2
length 124 1.59 0.06 1.40e1.82 4.0
M
2
trigonid width 124 1.32 0.06 1.16e1.49 4.9
M
2
talonid width 124 1.33 0.06 1.20e1.48 4.7
M
3
length 124 2.05 0.09 1.73e2.30 4.5
M
3
trigonid width 121 1.24 0.07 1.09e1.43 5.5
M
3
talonid width 122 1.16 0.07 1.00e1.32 5.7
M
1
length 123 1.59 0.06 1.42e1.77 3.7
M
1
width 123 2.08 0.10 1.80e2.35 4.6
M
2
length 123 1.59 0.06 1.40e1.75 3.6
M
2
width 123 2.10 0.10 1.84e2.39 4.9
M
3
length 123 1.48 0.05 1.35e1.66 3.7
M
3
width 123 1.95 0.11 1.70e2.26 5.5
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e20 5
(CVs) ranging from 2.4 for cranial length (n¼122) to 3.3 for bizy-
gomatic breadth (n¼117). We also examined the Amboasary
cranial sample for the presence of heteroscedasticity, as a trend
toward greater variation in smaller or larger individuals would be
informative for interpreting variation, and thus species boundaries,
in living and fossil primates. Fig. 1a, b and c, present bivariate
scatterplots and linear regressions of skull length compared with
each of the three cranial measures we collected (biorbital breadth,
bizygomatic breadth, and palate breadth). The linear relationship
between cranial length and each of these variables is signicant
(p<0.05), with cranial length and biorbital breadth (n¼119 ,
R
2
¼0.210, p¼<0.0001), cranial length and bizygomatic breadth
(n¼117, R
2
¼0.276, p¼<0.0001), and cranial length and palate
breadth (n¼122, R
2
¼0.204, p¼<0.0001), all exhibiting distinct
linear patterns. This illustrates that neither larger nor smaller
specimens exhibit greater variability, and provides a potential
framework for interpreting how an individual cranial specimen,
either extant or fossil, ts within a broader data set.
Dental measures also exhibit a limited range of variation
(Table 5a), with M
1
length being the least variable (CV ¼3.7,
n¼123), and M
3
talonid width being the most variable (CV ¼5.7,
n¼122). CVs for both tooth rows are also low, with the maxillary
toothrow having a CV of 2.5 (n¼105), and the mandibular tooth-
row having a CV of 2.8 (n¼103). Samples sizes for both toothrows
are somewhat smaller than for other measures due to damage of
the maxillary canines or caniniform P
2
, the mesial boundaries of
toothrow length (in mouse lemurs, as in most strepsirrhine
primates, the mandibular canine is incorporated into the tooth-
comb [see review in Cuozzo and Yamashita, 2006]).
Metric data for the Beza Mahafaly sample are presented in
Table 5b. Only dental data are available (maxillary and mandibular
rst molars), as the majority of the 32 BMSR specimens represent
partial remains recovered from owl pellets. Patterns of variation at
BMSR are similar to those for Amboasary, with all M
1
and M
1
CVs
less than 5.0. The two samples are also similar in having lower CVs
for M
1
and M
1
lengths than for corresponding widths at BMSR. In
addition, the overall ranges of dental measures at BMSR fall within
the range of variation at Amboasary (Table 5a and b).
Table 5c presents a statistical comparison of Amboasary and
BMSR samples for the ve rst molar measures. Measures for each
of the three mandibular molar measures are signicantly larger at
BMSR than at Amboasary (M
1
length, p¼0.0269; M
1
trigonid
width, p¼0.0018; M
1
talonid width, p¼0.0133). In contrast,
measures for the rst maxillary molar do not signicantly differ.
Table 5d provides comparative CV data for BMSR, Amboasary, two
subfossil mouse lemur assemblages (Andrahomona Cave and
Ankilitelo Cave), and the samples described by Rasoloarison et al.
(2000) of M. murinus and M. griseorufus, respectively, which
include the neotypes for both species. First maxillary and
mandibular molar variation at BMSR is lower than that seen at
Amboasary (M
1
length CV 2.90 and 3.70, respectively; M
1
length CV
3.20 and 4.00, respectively). Both BMSR and the Amboasary
samples display less rst molar variation than either of the two
subfossil cave samples, as well as both of the extant mouse lemur
samples reported by Rasoloarison et al. (2000). Of note,
Figure 1. Bivariate scatterplots and linear regressions of cranial measurements in the Amboasary mouse lemur sample. (a) Comparison of skull length and biorbital breadth;
(b) comparsion of skull length and zygomatic breadth; (c) comparison of skull length and palate breadth.
Table 5b
Beza Mahafaly odontometric summary statistics.
Measure NMean SD Range CV
M
1
length 15 1.62 0.05 1.55e1.73 3.2
M
1
trigonid width 15 1.25 0.04 1.18e1.32 3.4
M
1
talonid width 15 1.31 0.05 1.22e1.38 3.8
M
1
length 14 1.60 0.05 1.51e1.67 2.9
M
1
width 14 2.09 0.09 1.93e2.25 4.2
Table 5c
Amboasary and Beza Mahafaly odontometric comparisons.
Measure Amboasary mean BMSR mean P-Value
a
M
1
length 1.58 1.62 0.0269
M
1
trigonid width 1.20 1.25 0.0018
M
1
talonid width 1.27 1.31 0.0133
M
1
length 1.59 1.60 0.4188
M
1
width 2.08 2.09 0.4966
a
Bold values (studentst-test) represent signicant differences (p<0.05).
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e206
Rasoazanabary (unpublished data) has concluded that the Andra-
homana Cave sample may represent a single species assemblage,
based on patterns of metric and morphological variation, while
Muldoon et al. (2009) argue that the Ankilitelo sample contains
both M. murinus and M. griseorufus, based on two distinct dental
morphs. The M
1
and M
1
CVs for the fossil sites are approximately
twice as large as those of the samples at Amboasary and BMSR. The
M. murinus sample described by Rasoloarison et al. (2000) repre-
sents three localities, across a wide geographic range. On the other
hand, the Rasoloarison et al. (2000) sample for M. griseorufus near
BMSR includes only 6 individuals, which may account for its rela-
tively high CV (7.17).
Dental morphology
Frequencies for each condition of the 40 traits (Appendix A
[right teeth] and Appendix B [left teeth]) show that eight (20%)
exhibit 100% presence for both left and right teeth in the Amboa-
sary sample. Included among these are traits characteristic of all
mouse lemurs, such as a single cusped P
2
and P
2
, a distinct proto-
cone on P
4
, and P
4
with a thick buccal cingulid and centrally placed
entoconid. Other traits exhibiting 100% presence for both left and
right tooth positions are M
1
hypocones, and metastyles on M
1
and
M
2
. The remaining traits exhibit a wide range of variation, with
several exhibiting a nearly dichotomous distribution in the sample,
and others exhibiting low frequencies. Traits exhibiting a dichoto-
mous distribution include lower molar cingular development
(Appendices A and B, traits 11, 18, and 23: nearly equal frequencies
of individuals with weak and strong buccal cingula on left and right
M
1
,M
2
, and M
3
), and P
3
buccal cingulids (Appendices A and B, trait
26) with nearly equal frequencies of weak and strong rims on both
left and right teeth. Also of note is the low, but distinct, presence of
variable secondary cusps on the maxillary teeth: protocones on P
3
(Appendices A and B, trait 3; 4.0% in right teeth, 2.4% in left teeth),
an accessory ridge and/or cusp distolingual to the hypocone on M
1
(Appendices A and B, trait 7; 6.5% of right M
1
, 5.7% of left M
1
), and
M
3
hypocones. These traits are similar to ones often assigned
taxonomic signicance, particularly in cladistic analyses, among
both living and especially fossil primates and other mammals (see
discussions in Krishtalka and Stucky, 1985 and Simons, 2003).
One example of the range of dental morphology seen in this
sample is variation in the lingual morphology on M
1
, which results
in the existence of very dissimilar teeth within the sample. The
lingual portion of M
1
may or may not exhibit pericones, accessory
ridges, or a cusp distolingual to the hypocone. Furthermore, the
overall shape of M
1
can be squared, when a pericone equal in size to
the hypocone is present (Fig. 2a), squared with a distolingual
extension when the post-hypocone accessory ridge and/or cusp is
present, or triangular (i.e., tribosphenic) when the pericone is
absent, or greatly reduced. The latter triangular shape can also be
accentuated if the post-hypocone area is well-developed (Fig. 2b).
As a result of these traits, the morphology of M
1
varies tremen-
dously in this sample.
Patterns of variation at BMSR are similar to those described for
Amboasary. Of the 40 traits scored for right and left teeth
(Appendices C and D), approximately half display 100% presence or
absence of specic traits. This percentage is higher than that at
Amboasary, but is largely a product of the smaller sample sizes at
BMSR, as a number of the traits not present in 100% of the speci-
mens at Amboasary occur at low frequencies. Of those traits rep-
resenting dichotomous distributions at BMSR, many are also
dichotomous at Amboasary. This includes traits 25 and 26 (P
2
and
P
3
buccal cingulum strength), and trait 31 (M
1
buccal cingulum
strength). Certain traits show low frequencies of occurrence in both
samples; this includes trait 7, a lingual extension/style on M
1
, which
occurs in 6.5% of the Amboasary right teeth (Appendix A) and 5.6%
of the left (Appendix B). At BMSR (Appendices C and D) this trait is
seen in only one tooth, a left M
1
(Appendix D,n¼12). The one
specimen at BMSR displaying this feature is one of six from Iha-
zoara Canyon, approximately 5 km from the protected BMSR parcel
where the majority of the new mouse lemur specimens were
recovered in 2008. However, this specimen does not exhibit an M
2
pericone, similar to the majority of individuals in both the BMSR
and Amboasary samples. In contrast, a second BMSR specimen from
Ihazoara Canyon possesses an M
2
pericone, but does not exhibit the
M
1
lingual extension. This illustrates that even in a small subset of
a large sample, traits associated with lingual dental development
can vary widely, and are likely of limited taxonomic and/or
phylogenetic value among living or fossil primates.
Individual dental variants
In addition to the above patterns of intraspecic dental variation,
some interesting variantscharacterize single individuals in the AMNH
sample. For example, one specimen (AMNH 174496) displays a single
cusped, connate M
3
(Fig. 3a). This tooth differs substantially from the
regular M
3
pattern (Fig. 3b), and out of context, would be impossible
Table 5d
Microcebus cranial and odontometric variation comparisons.
Locality M
1
length CV
a
NM
1
length CV
a
NSkull
length CV
a
N
Amboasary
b
3.70 123 4.00 124 2.40 122
BMSR
b
2.90 14 3.20 15 ee
Andrahomana
Cave
c
5.33 45 6.83 47 ee
Ankilitelo
d
ee7.69 21 ee
Microcebus
murinus
e
4.82 11 ee1.89 11
Microcebus
griseorufus
e
7.17 6 ee2.53 6
a
All CVs corrected for sample size following Sokal and Rohlf (1995) and Plavcan
and Cope (2001).
b
Data from current study.
c
Data from Rasoazanabary (unpublished).
d
Data from Muldoon et al. (2009).
e
Data on M. murinus and M. griseorufus samples from Rasoloarison et al. (2000) e
M. murinus represents three localities; M. griseorufus represents a single locality.
Figure 2. Variation in AMNH mouse lemur (Microcebus griseorufus) maxillary molar
morphology. (a). Squaredleft M
1
with thick cingulum, equal pericone and hypocone,
and no distolingual extension (black arrow); (b). Triangularright M
1
with small
pericone, large hypocone, and distinct distolingual extension (black arrow). [Photos by
Frank Cuozzo].
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e20 7
to identify either as an M
3
, or as a mouse lemur tooth. Another indi-
vidual specimen has a signicantly shortened M
3
(AMNH 174523),
with the typically extended hypoconulid absent (Fig. 4aandb).These
variants are quite different from the standard mouse lemur pattern,
and again illustrate the possible range of variation that can exist in
a likely breeding population. Two specimens (AMNH 174499 and
AMNH 174515) exhibit supernumerary teeth. Individual AMNH
174499 has supernumerary lower molars on both the left and right
mandibles (Fig. 5), and AMNH 174515 has an extra left maxillary
incisor (Fig. 6). These individualvariants often resultfrom disruptions
during odontogenesis (Miles and Grigson, 1990;Swindler, 2002),
although supernumerary teeth may be polymorphisms in the lemur
genome ei.e., artifacts of the ancestral mammalian dental formula,
which included three incisors in each quadrant (see discussion in
Sauther and Cuozzo, 2008). Kangas et al. (2004) note that increase in
the expression of a single gene can lead to an increased number of
teeth in mice, thus supernumerary teeth may also reect a rapid
genetic change. These traits, as well as the traits discussed previously,
have implications for interpreting mammalian paleotaxonomic
diversity based on dental morphology (Goodwin, 1998).
Pelage variation
The pattern of pelage variation exhibited by the Amboasary
specimens and those of M. griseorufus from other sites is not shared
by most other mouse lemurs, including other recognized species
from the west (Table 6). This is conrmed by Fishers exact test of
signicance of differences in frequency distributions across taxa
(Tables 7 and 8); all are highly signicant. However, a comparison
of coat characteristics of individuals from Amboasary and from
Beza Mahafaly afrms their similarity, in which the limited varia-
tion in Amboasary pelage (all individuals display a reversed Von
the cap and a dorsal median stripe, and all but two exhibit a graye
brown coat), falls within the range of pelage variation at BMSR
(Table 6). When assessed quantitatively, frequency differences in
these traits are not signicant between Amboasary and BMSR,
suggesting that the populations at these two sites likely belong to
the same species (Tables 7 and 8). The match was poor for
Amboasary specimens with those belonging to M. murinus or to
M. rufus (Table 6).
Qualitative data also point to a good match between Amboasary
specimens and M. griseorufus at Beza Mahafaly. Individuals
captured at BMSR generally display what may be called the
typicalM. griseorufus pattern (Table 6), consisting of a redebrown
tail, shades of gray and brown on the back, a redebrown stripe of
varying intensity along the dorsal midline, that generally matches
the color of the tail, a white underside, a white stripe between the
eyes, and reddish-brown markings above the eyes converging in an
apex (the reversed V) on an otherwise gray or yellowish-brown
cap (Fig. 7a and b). However, variants included some that are
more similar to M. murinus at the Kirindy forest (a redebrown tail,
a gray back lacking a contrasting dorsal midline stripe, a cream
Figure 3. (a). Connate M
3
(white arrow) in AMNH 174496 (Microcebus griseorufus). (b) Regulartriangular M
3
shape in AMNH Microcebus griseorufus. [Photos by Frank Cuozzo].
Figure 4. Variation in AMNH mouse lemur (Microcebus griseorufus) mandibular third molars. (a). The typicalM
3
morphology, with distal extension and hypoconulid, marked by
a white arrow (buccal view); (b). M
3
without distal heeland hypoconulid (AMNH 174523), with white arrow marking the squareddistal border rather than the distal extension
seen in 3a (occlusal view). [Photos by Frank Cuozzo].
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e208
underside, and no reverse V on the cap) (Fig. 7c). Additional indi-
viduals are all red(a redebrown tail, a redebrown back lacking
a dorsal midline stripe, a cream underside, a redebrown face and
cap but with a creamy white stripe between the eyes). A dorsal
median stripe is most distinct in individuals with relatively light
coats; it becomes less distinct, or disappears entirely, as the coat
darkens. As seen in Fig. 7aec, and in Table 6, the BMSR mouse
lemurs display a wider range of pelage variation than at Amboasary,
where all individuals display at least two of the typical
M. griseorufus traits (two of the 19 Amboasary pelage specimens
display a red/dark brownoverall color, compared to the typical
grayebrown of M. griseorufus [Table 6]). This wide range of pelage
characteristics at BMSR is especially notable, as this population has
been shown to illustrate genetic homogeneity (Heckman et al.,
2006). Thus, the BMSR mouse lemurs exhibit clear discordance
between mitochondrial DNA and pelage.
Qualitatively, the coats of individuals from Amboasary in the
AMNH Bluntschli collection resemble the majority from Beza
Mahafaly in the tendency to have light fur between the eyes and on
the nasal region (white, pale yellow, or pale brownish gray), pale
cheeks, a yellowish brown cap with a dark reversed V, a white, pale
yellow, or pale yellowish brown throat and ventrum; dark
yellowish brown pelage on the dorsal surfaces of the arm and upper
arm, and a dorsal median stripe. The color of the tail and the dorsal
median stripe is more uniform across mouse lemurs; it tends to be
dark yellowish brown or dark brown. M. rufus from Antsihanaka,
Andampy, Didy, Ivondro, Tampina, and Analamazaotra have
consistently darker pelage, with brown, dark brown, or very dark
brown faces and dorsal pelage, and light yellowish brown fur or
yellowish brown fur on the throat and ventrum. Sometimes the tail
is very dark brown. M. murinus from Andranomena, Toliara, Vohi-
mena, and Manamby is characterized by more gray or yellowish
brown fur on the cheeks, more gray, brown, or dark brown fur on
the dorsum, and mostly yellowish brown fur on the throat and
ventrum.
Discussion
Taxonomic afnity of the AMNH Amboasary mouse lemur sample
The immediate goal of our project was to assess the single-
species status of the Amboasary mouse lemur sample housed at
AMNH. We were also interested in establishing the specicafnity
of this sample, given the dramatic recent changes in mouse lemur
taxonomy (see earlier references). We recognize that pelage can
vary signicantly among related, morphologically similar primate
species (e.g., African guenons, genus Cercopithecus [Enstam and
Isbell, 2007]). However, we are condent that the BMSR mouse
lemur population provides an accurate point of reference for
assessing specic variability in southern Madagascars mouse
lemurs. Specically, mitochondrial DNA and a consensus phylogeny
derived from a combination of mtDNA and nDNA markers supports
a single species designation for BMSR mouse lemurs (Heckman
et al., 2006,2007), despite notable variation in pelage characters
(Table 6,Fig. 7aec). Although occurring in a small area (all speci-
mens were collected within ve km of the reserve headquarters),
mouse lemur habitats at BMSR range from an open, dry, xerophytic
forest, to an area of closed-canopy tamarind-dominated gallery
forest along the Sakamena River, to the mixed dry forest at Ihazoara
Canyon. Heckman et al. (2006) suggested that the pelage variation
observed, which is independent of habitat, is inconsequential, and
likely plays no role in mate recognition in these nocturnal, solitary
animals, as mouse lemurs frequently depend on olfaction and
vocalizations in social encounters (e.g., Yoder et al., 2002).
However, this deserves further study, as recent, dramatic habitat
fragmentation in the Beza Mahafaly area, and southern Madagascar
as a whole, may also impact current patterns of pelage variation
within single lemur species. Of note, a previous sample of mouse
lemur jaws collected from owl pellets by Goodman in the early
1990s, across the Sakamena River from the eastern edge of the Beza
Mahafaly reserve near the village of Ambinda, has been identied
as being made up almost entirely (all but one specimen) of
M. griseorufus material (Rasoloarison et al., 2000). Furthermore,
when single nDNA markers are analyzed alone, they show patterns
of paraphyly consistent with incomplete lineage sorting (Heckman
et al., 2007; see also Hapke et al., 2011). However, genetic evidence
as a whole (with nDNA and mtDNA considered in combination)
rmly establishes M. griseorufus and M. murinus as sister taxa and
independent species despite the existence of pockets of
hybridization.
As we have seen, pelage characteristics (color and patterning) of
individual mouse lemurs from Amboasary in the Bluntschli
collection housed at the AMNH and MCZ generally match typical
M. griseorufus from Beza Mahafaly (Table 6), and there are no
signicant differences in trait frequencies when the two samples
are compared (Table 8). Furthermore, the distribution of trait
variants at Amboasary is not unlike that seen in living M. griseorufus
from Beza Mahafaly, albeit displaying far less variation than at
BMSR (Table 6). This limited variation in pelage characteristics at
Amboasary when compared to BMSR, in which each trait scored at
BMSR shows some variation, while those at Amboasary vary in only
two of the three traits, may be a product of the smaller sample sizes
at Amboasary. However, it is noteworthy to again emphasize that
pelage characteristics of individuals at Beza Mahafaly, a population
shown to be genetically homogenous (cytochrome b) and
Figure 5. Supernumerary molar in a right mandible of AMNH 174499 (Microcebus
griseorufus). Black arrows mark the three molars distal to M
1
. [Photo by Frank Cuozzo].
Figure 6. Supernumerary left incisor in AMNH 174499 (Microcebus griseorufus) [Photo
by Frank Cuozzo].
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e20 9
suggested to belong to M. griseorufus, are quite variable (Heckman
et al., 2006). Although we have not surveyed variation in coat
characteristics of living mouse lemurs from other sites, it is
apparent that similar variation may exist elsewhere. M. murinus is
one such variable species; for example, the skins (including the
neotype from Andranomena, south of Kirindy) of M. murinus at the
Field Museum of Natural History, Chicago (Rasoloarison et al.,
2000) differ strikingly from the grayer M. murinus skins that
occur in the Kirindy forest (ER, pers. obs.). Evidently, it is not pelage
coloration per se but the frequency distribution of pelage traits that
can be described as characterizing any particular species. This
implies that coat characteristics must be well sampled before
species can be properly described, and before pelage variation can
be assessed in relation to patterns of dental variation.
Patterns of dental variation in the Amboasary sample, similar to
pelage variants, are consistent with those seen in the BMSR mouse
lemurs, a known, single-species sample (Heckman et al., 2006).
This includes overlapping ranges of dental measurements, similar
degrees of odontometric variation, and low CVs for all dental
measures (Table 5aed). The Amboasary sample also exhibits a very
low degree of craniometric variation (Fig. 1aec; Table 5aed).
Although mandibular rst molar measures are signicantly larger
at BMSR than Amboasary, maxillary molar size does not differ
(Table 5c). Therefore, these metric data do not appear to indicate
a meaningful biological difference between the two samples. In
addition, patterns of dental morphology are also consistent across
the two mouse lemur samples, with the same dental features in
each sample displaying 100%, dichotomous, and infrequent occur-
rences. Given the limited metric variation in cranial and dental
measures, and the overlap of similar, variable, non-metric dental
traits, in the mouse lemurs at Amboasary and BMSR ecombined
with pelage patterns that overlap, and that match traits of estab-
lished M. griseorufus at BMSR, it seems to be highly unlikely that the
Amboasary sample comprises more than one species. We therefore
conclude that the AMNH Amboasary sample represents a single
species eM. griseorufus.
Interpreting primate biological variation
The presence of diverse pelage (BMSR) and substantial variation
in dental morphology (i.e., non-metric traits [BMSR and Amboa-
sary]), combined with limited cranial and/or dental metric varia-
tion in each of our two single-locality, single-species Microcebus
samples, provides a strong point of comparison for interpreting
variation, and thus species boundaries, in primate biology. Most
notably, our data indicate that different biological systems can be
discordant in a single species, thus drawing attention to the efcacy
of identifying primate species on the basis of single biological traits,
whether genetic markers, pelage variants, dental morphology, or
cranial/dental metric variation.
This point is further illustrated when we compare our mouse
lemur data to that of sympatric ring-tailed lemurs (Lemur catta).
The Beza Mahafaly ring-tailed lemurs comprise an important
comparative database for assessing biological variation among
primates, particularly because dental variation in this unequivocal,
single-species primate population has been so well documented
(Sauther et al., 2001;Cuozzo and Sauther, 2004,2006a,b; see
reviews in Cuozzo and Yamashita, 2006, and Cuozzo, 2008). As
noted by Plavcan and Cope (2001) and Tornow et al. (2006), such
samples for extant species are rare. In this population, a number of
dental traits vary (Table 6;Sauther et al., 2001;Cuozzo and
Yamashita, 2006;Cuozzo, 2008). Variable traits include P
4
meta-
conids and upper molar lingual cusps (Table 9), the absence of
which have been suggested as diagnostic of ring-tailed lemurs
(Tattersall and Schwartz, 1991;Tattersall, 1993). At Beza Mahafaly,
two individuals display pronounced lingual cusps on M
1
and M
2
,
and 24 individuals (45.3%, n¼53; Table 9) exhibit distinct meta-
conids on P
4
. The presence of upper molar lingual cusps (albeit at
a low frequency) is especially notable, as these distinct cusps are
viewed as diagnostic of Eulemur (i.e., Eulemur fulvus) in contrast to
Lemur catta (Tattersall and Schwartz, 1991;Tattersall, 1993;
Swindler, 2002; see discussion in Cuozzo and Yamashita, 2006).
The pattern of lingual dental morphological variability in L. catta at
the Beza Mahafaly Special Reserve thus parallels that in each of our
mouse lemur samples. This is an especially interesting point of
comparison, as ring-tailed lemurs have been reported to exhibit
Table 6
Frequency data, scores on dried and live-animal coats for three variables.
Taxon (N) Reversed V Dorsal median stripe Dominant color of the dorsal fur
Absent or indistinct Present Absent or indistinct Present Gray Grayebrown Red(dark brown)
M. berthae (1) 0 1 0 1 0 1 0
M. sambiranensis (3) 3 0 3 0 0 0 3
M. ravelobensis (6) 6 0 6 0 0 6 0
M. murinus (7) 7 0 7 0 1 0 6
M. myoxinus (6) 6 0 0 6 0 5 1
M. tavaratra (5) 5 0 5 0 0 2 3
M. rufus (9) 9 0 9 0 0 2 7
M. griseorufus (212) 39 173 37 175 16 170 26
Amboasary (19) 0 11 0 19 0 17 2
Table 7
Fishers exact test of signicance of differences in frequency distributions of coat
characteristics.
a
Trait tested NFishers
statistic
Signicance
(two-sided)
Reversed V (present or absent) 256 88.3 p<0.001
Dorsal median stripe
(present or absent)
264 82.8 p<0.001
Dorsal fur dominant color
(gray, grayebrown, or red)
264 241.6 p<0.001
a
Included taxa are: M. ravelobensis,M. murinus,M. myoxinus,M. tavaratra,
M. rufus,M. griseorufus, and Amboasary.
Table 8
Fishers exact test of signicance of differences in frequency distributions of coat
characteristics for Beza Mahafaly and Amboasary.
Trait tested NFishers
statistic
Signicance
(two-sided)
Reversed V (present or absent) 212 1.18 p¼0.37
Dorsal median stripe
(present or absent)
220 1.14 p¼0.56
Dorsal fur dominant color
(gray, grayebrown, or red)
220 2.6 p¼0.14
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e2010
pelage variation, with a higher altitude population in the north-
ernmost area of their natural range exhibiting differences in tail
ring number and overall darker pelage color (Goodman and
Langrand, 1996), yet are not genetically distinct from other pop-
ulations (e.g., cytochrome b[Yoder et al., 2000b]).
The recognition of substantial intraspecic dental morpholog-
ical variation in extant primates is not new (e.g., Schwarz, 1931;
Schuman and Brace, 1954;Swindler and Orlosky, 1974;Schwartz
and Beutel, 1995). However, many scholars have failed to fully
appreciate the degree to which such variation can exist in extant
species, or even within populations. This is especially true among
paleontologists, who sometimes assign taxonomic and/or phylo-
genetic signicance to even slight variations among the specimens
in a fossil assemblage and/or when conducting cladistic and other
taxonomic analyses (see discussions in Krishtalka and Stucky, 1985;
Jernvall, 2000;Cuozzo, 2002,2008;Simons, 2003;Kangas et al.,
2004; see also chapters in Kimbel and Martin, 2003).
One complicating factor in the use of nonmetric dental variation
to diagnose primate (and other mammalian) species, in either
living or fossil forms, is the apparent rapidity in which slight
developmental differences can generate surprising amounts of
variation in dental morphology (e.g., Jernvall, 2000;Kangas et al.,
2004). For example, Kangas et al. (2004) report that increased
expression in a single gene in mice leads to changes in the number,
shape, and position of cusps. Thus, in effect, failure to appreciate the
developmental component of the generation of variation can
obscure phylogenetic history(Kangas et al., 2004: 211). Also,
recent work illustrates differences in the degree of heritability for
different dental features, and that tooth size and discrete traits are
not necessarily linked (e.g., Hlusko and Mahaney, 2003,2007;
Hlusko et al., 2007). For instance, certain traits of the lingual
cingulum in a large sample of pedigreed baboons show high heri-
tability within the arcade (e.g., between left and right teeth of
either the maxilla or mandible), but less so between arcades
(Hlusko and Mahaney, 2003).
Our lemur data suggest that notable variation in nonmetric
dental traits can occur in populations exhibiting limited odonto-
metric variation. Most notably in our two extant mouse lemur
samples, the M
1
post-hypocone ridge and/or cusp (Fig. 2b) is vari-
able in appearance, ranging from a small ridge, to a ridge with an
accessory cusp, and it can also vary within the arcade, with either
left or right teeth, or sometimes both, displaying the trait. In
contrast, the lingual cingulum traits discussed by Hlusko and
Mahaney (2003) show a strong correspondence within an arcade.
This trait also appears in a single M
2
from Amboasary (Appendix B).
In addition, several Amboasary specimens displayed an ination of
the area of M
1
distolingual to the hypocone without any true
manifestation of a post-hypocone ridge or cusp. This trait, with its
various manifestations along a gradient ranging from a slight
lingual ination to a ridge with a distinct cusp, corresponds with
Jernvalls (2000) observation that various trait conditions are
present, albeit at low frequencies, within geographically-restricted
samples of a single mammal species. Under selective pressure (or
due to genetic drift), any of these variants could become more
Figure 7. Coat color variation within Microcebus griseorufus at Beza Mahafaly. (a). The typical griseorufusmorph; (b) The graymorph; (c) The redmorph. [Photo credits:
Emilienne Rasoazanabary]. (For interpretation of the references to colour in this gure legend, the reader is referred to the web version of this article.)
Table 9
Variation in dental traits among ring-tailed lemurs (Lemur catta) from Beza Mahafaly
Special Reserve, Madagascar.
Trait N# with trait % with trait
M
12
ledge-like cingulum 58 56 96.5
P
3
metaconid absent 57 57 100.0
P
4
metaconid absent 53 29 54.7
M
1
lingual notch: narrow/pinched 48 48 100.0
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e20 11
frequent in the population. The same applies to other dental vari-
ants we describe. For example, protocones on P
3
could hold
a selective advantage over time, given their potential for aiding in
the processing of certain, perhaps novel foods. Butler (2000),in
describing the evolution of primate teeth notes the potential
crushingbenet of the development of a protocone on P
3
, when
combined with corresponding changes in the mandibular molars.
Jernvall et al. (2008) also discuss the molarizationof premolars
(e.g., development of lingual cusps) in Hapalemur simus, as a benet
to processing more brous foods. Thus, the development of this
premolar feature in mouse lemurs could be benecial in a changing
environment, and could quite rapidly become frequent in a pop-
ulation. Kangas et al. (2004) suggest that the potential for changes
in a single gene to cause quite dramatic morphological variation,
could lead to such rapid changes in dental morphology in response
to environmental change. Thus, changes in the frequency of lingual
dental traits over time in the fossil record might prove useful in
delineating species (e.g., Rose and Bown, 1984;Cuozzo, 2008)if
viewed in the context of environmental change. Given the potential
for dramatic variation in nonmetric dental traits that we document,
it would be prudent, when conducting taxonomic analyses, to heed
the advice of Strauss (1954: 308) who, citing Schuman and Braces
(1954) seminal paper on chimpanzee dental variation, wrote that
the demonstration of high dental variation within a homogeneous
population of chimpanzees should serve as a rein upon unbridled
odontological speculation.
Similar caution should also be used when assessing species
diversity using biological systems other than teeth. For example,
many new species of living mouse lemur have been dened on the
basis of single systems, frequently molecular data (e.g., Yoder et al.,
2000a,b;Louis et al., 2006,2008;Weisrock et al., 2010). However,
the use of DNA characters in taxonomy has been critiqued by some
as having no more weight than other biological characters (see
comments by Lipscomb et al., 2003). Tattersall (2007) has argued
against what he perceives as a dramatic and unwarranted prolif-
eration of recognized extant lemur species, many of which have
been diagnosed from small samples, and with limited knowledge of
hard-tissue variation, and/or ecological and reproductive behavior.
Markolf et al. (2011) follow this theme, suggesting that genetic
markers from several loci should be combined with other biological
data, such as behavioral, ecological, and morphological informa-
tion, for interpreting species boundaries in lemurs. For the BMSR
mouse lemurs we document notable variation in pelage (Table 6)
and non-metric dental traits (Appendices C and D), yet limited
dental metric variation (Table 5b). Heckman et al. (2006) report
homogeneity in cytochrome bin a sample of 70 mouse lemurs at
BMSR, collected across multiple habitats, which refuted their
earlier hypothesis that multiple species were present at BMSR. The
distinction between M. griseorufus and M. murinus is also further
explored in their later work (Heckman et al., 2007), using both
nDNA and mNDA markers. In the Amboasary sample, we show that
limited cranial variation (Table 5a) and no evidence of hetero-
scedasticity (i.e., neither larger nor smaller values are more vari-
able, Fig. 1aec), corresponds to low levels of dental metric variation
(Table 5a), notable variation in non-metric dental traits
(Appendices A and B), and variation in one of three pelage char-
acters (Table 6). This parallels the ndings in the BMSR mouse
lemurs, where for the markers assessed, a single species designa-
tion is supported, across habitats and pelage variants (Heckman
et al., 2006). We thus argue that substantial variation in pelage
and non-metric dental traits can occur in a single primate species,
but that this species diagnosis rests upon tandem interpretations of
limited metric variation of hard-tissue traits (e.g., cranial and/or
dental measures) and molecular data showing distinct differences
between species for certain genetic markers. From our mouse
lemur example, it is clear that careful consideration of multiple
biological systems is needed when interpreting variation, and
subsequently, species boundaries in contemporary primate biology.
Implications for primate paleotaxonomy
Species diagnosis in paleobiology necessarily differs from the
diagnosis of extant taxa, as paleotaxonomy must depend to
a greater degree on morphological data (e.g. Tattersall, 1992).
However, in addition to qualitative analyses of teeth, patterns of
metric variation, when adequate samples are available, also provide
an important point of comparison for interpreting and identifying
species in the primate fossil record. Recall earlier comments by
Kieser (1994),Plavcan and Cope (2001), and Tornow et al. (2006) on
the importance, but rarity, of characterizing variation in
geographically restricted samples. Our data do just that eprovide
data on patterns of biological variation in a large, geographically
restricted primate sample. Thus, this work provides a useful
reference for assessing the degrees of similarity and/or difference in
other taxa, providing a template for condent assessment and
interpretation of biological variation in the primate fossil record.
Of all our results, discordance between different traits, notably,
consistent patterns of limited cranial and dental metric variation
corresponding to marked variation in non-metric dental traits, is
most relevant for questions of interpreting paleobiology. One
especially relevant aspect of our data for interpreting the fossil
record is the absence of heteroscedasticity in cranial variation in
the large (n¼126) Amboasary sample. One of the challenges in
interpreting fossil specimens, especially in the absence of large
samples (e.g., in many hominin taxa), centers on the ability to
accurately assess single specimens. For example, Trinkaus (2003)
notes the impact that a single largeNeandertal specimen has
had on descriptions of Neandertal biology, especially when
compared to modern humans. Dayan et al. (2002) note that there is
substantial heteroscedasticity in cranial and dental measures in
wolves (Canis lupus) and wild cats (Felis silvestris), which they
suggest as cautionary for interpreting the relationships between
dental and cranial variation, most specically in the context of
interpreting taxonomic diversity in the carnivoran fossil record.
They attribute this pattern, in part, to the derived dentition of
extant carnivores, not an issue for many early primates (e.g.,
Rasmussen, 2007), or many extant lemurs (e.g., Cuozzo and
Yamashita, 2006), given their retention of a number of ancestral
dental traits. As we illustrate in Fig. 1a, b and c, the relationships
between skull length and biorbital breadth, zygomatic breadth, and
palate breadth, respectively, there is a signicant linear relationship
between skull length and each of these other variables (p<0.0001),
thus indicating that this sample does not exhibit greater variation
in larger or smaller cranial measures. These data provide a template
for interpreting the taxonomic placement/identication of single
fossils, when cranial specimens are available, especially among
early primates, as extant mouse lemurs are among the analogs for
the small-bodied extinct primates of the Eocene Epoch (Covert,
1995,1997;Cuozzo, 2008).
As we briey note earlier, the patterns of morphological varia-
tion we describe in the dentition of our lemur samples also provide
a point of reference for interpreting variation in primate fossils. For
example, the importance of acknowledging the potential for
substantial variation in dental traits is seen in Szalays critiques
(1982,1993) of several Eocene omomyid species. In developing
these critiques, Szalay argued that species sharing similar, although
not identical, morphologies, as well as temporal congruence, may
not represent distinct species, but may instead represent a single,
highly variable species. Similarly, Albrecht and Miller (1993) argue
that the morphological variation seen in fossil primates may largely
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e2012
represent intraspecic geographic variation, rather than species
differences. Our data support these assertions; for example, the
absence of a distinct, extended hypoconulid in AMNH 174523 is
analogous to the Eocene adapid Smilodectes missing its talonid
heel, the shape of which is considered by manyas a diagnostic trait
of this genus (e.g., Covert, 1990). Also, the parallel patterns of
lingual dental cusp variation in each of our mouse lemur samples,
and in our comparative ring-tailed lemur sample, provide further
support that dental morphology varies in single-species samples.
Evaluating more subtle non-metric dental variation has even
greater importance than the above example for assessing fossil
assemblages and interpreting individual specimens. Maxillary
molar lingual traits, and premolar secondary cusps, vary widely
among the mouse lemurs at Amboasary and BMSR (recall these
traits also vary among the ring-tailed lemurs at BMSR), often
exhibiting dichotomous characters states. While these traits can
prove important in delineating species boundaries, when viewed
over time in the geologic record, as seen in several small-bodied
Eocene omomyid primates from North America (e.g., Rose and
Bown, 1984;Cuozzo, 2008), their signicance in single locality
assemblages are likely of limited taxonomic importance. Rose et al.
(2009) recognized the importance of such patterns of dental vari-
ation (e.g., premolar cusps) in their analysis of Eocene primates
from southern Asia. They argue that two forms previously identi-
ed from the same stratum on the basis of subtle premolar differ-
ences, Suratius robustus and Asiadapis cambayensis, should be
synonymized. Cuozzo (2002) made a similar argument for synon-
ymizing two small omomyids from the early Eocene of Wyoming
(see Tornow, 2008 for a contrasting view).
Conclusions
We encourage the integration of dental, cranial, pelage, and
ecological data, combined with information, when available, from
genetic samples, when diagnosing primate species among living,
and when appropriate, among fossil forms. We also strongly
discourage the sacrice of living, wild primates solely for taxo-
nomic purposes. Our collaborative, long-term work at the Beza
Mahafaly Special Reserve, Madagascar, illustrates the power of
sustained research on living individuals and populations, for
example, the collection of dental, linear, and pelage data during
exams of sedated, living primates, as well as the importance of
collecting data from those individuals who die natural deaths,
including from predation.
Knowledge of variation in multiple biological systems, as we
describe herein for established single-species samples, their
discordance, and their role in assigning specic status, also tran-
scends interpretation of the fossil record. For example, Stanford
(2001: 310) notes that taxonomic status often dictates conserva-
tion prioritiesamong primates, illustrating the need to understand
the range of variation within species. Hey et al. (2003: 600) note
that species living in nature must be part of evolving populations,
thus acknowledging the link between contemporary conservation
concerns and evolutionary biology. Among Madagascars lemurs,
the past three decades have witnessed a dramatic increase in the
number of recognized species, from 36 species (Tattersall, 1982)to
97e99 species (Mittermeier et al., 2008,2010). The new data that
we present provide an important reference for interpreting primate
intraspecic variability, which is directly relevant to the efcacy of
recent, rapid increases in named lemur species (e.g., Tattersall,
2007;Markolf et al., 2011), as well as other primate groups (e.g.,
Stanford, 2001).
Finally, as Tattersall (1992: 343) noted in reference to hominin
paleontology, species in the fossil record are, and will continue to
be, categorized and ranked.at least primarily on the basis of
morphological attributes.This is not to say that paleotaxonomy
should be trapped in a world of typology, but rather, that assessing
the fossil record will remain dominated by morphology, regardless
of how much we appreciate the importance of spatial, temporal,
and behavioral variables in addressing the theoretical question,
What is a species?Our new data provide a template to begin to
address this question in living and fossil primates.
Acknowledgments
We thank the curators and their support staffs at the American
Museum of Natural History, The Museum of Comparative Zoology
(Harvard University), and the Field Museum of Natural History for
access to, and assistance with, specimens in their care. Collection of
mouse lemur dental data at AMNH was supported by the University
of Colorado William H. Burt Fund, a University of Colorado
Department of Anthropology Pre-dissertation Grant, Las Positas
College, and an AMNH Collection Study Grant to FPC. Collection of
ring-tailed lemur dental data at Beza Mahafaly Special Reserve
(2003e2008), and the collection of new mouse lemur dental
specimens at Beza Mahafaly Special Reserve (2008), was supported
by funds awarded to FPC by the St. Louis Zoo (FRC 06-1), the
University of North Dakota (SSAC, Faculty Seed Grant Council, Arts,
Humanities, and Social Sciences Award), North Dakota EPSCoR,
Primate Conservation, Inc., the International Primatological Society,
and to MLS by Primate Conservation Inc., the American Society of
Primatologists, the Lindbergh Fund, the Saint Louis Zoo, the John
Ball Zoo Society, the National Geographic Society, and the Univer-
sity of Colorado, Boulder (CRCW, IGP). Collection of new mouse
lemur dental specimens at Beza Mahafaly Special Reserve (2008)
was also supported by funds awarded to MML by the University of
Colorado (Department of Anthropology, Pre-Dissertation Research
Grant, a Beverley Sears Award from the Graduate School, and the
CU Museum of Natural History), and the Denver Museum of Nature
and Science (Native American Resource Advisory Group and the
Department of Anthropology). Collection of mouse lemur pelage
data from living individuals at the Beza Mahafaly Special Reserve
and from museum specimens at AMNH, the Field Museum of
Natural History (Chicago), and the Museum of Comparative Zoology
(Harvard University) was supported by the Wenner Gren Founda-
tion for Anthropological Research (Professional Development
International Fellowship), the Margot Marsh Biodiversity Founda-
tion, Primate Conservation, Inc., and the American Society of
Primatologists to ER, and by the National Science Foundation BCS-
0237388 to LRG. FPC and MLS thank the numerous individuals
acknowledged in previous publications for their assistance with
data collection at Beza Mahafaly. ER thanks Elahavelo, Edidy, Enafa,
Rigobert, and Etsimandiso for their assistance with data collection
at Beza Mahafaly. This project was aided by assistance from Ruth
Steel and Roger Ramarokoto, student assistants. We also thank the
Département des Eaux et Forêts, Ecole Supérieure des Sciences
Agronomiques (ESSA), Université dAntananarivo and the Associa-
tion Nationale pour la Gestion des Aires Protégées (ANGAP) for
their permission to work at Beza Mahafaly (2003e2008). Data
collected from the ring-tailed lemurs at the Beza Mahafaly Special
Reserve from 2003 to 2008 described herein received IACUC
approval from the University of North Dakota and the University of
Colorado-Boulder. Data collection on the mouse lemur population
at Beza Mahafaly in 2003e2004 received IACUC approval from the
University of Massachusetts-Amherst. We thank Mark Teaford, the
JHE editorial staff, previous JHE editors and Associate Editors, and
three anonymous reviewers for their helpful comments and
suggestions on this and earlier versions of our manuscript, which
have greatly improved our paper.
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e20 13
Appendix A. Variation in Amboasary dental traits: right teeth
# Trait nCondition % nCondition % nCondition % n
1 C w/distal style 118 Absent 11.9 14 Present 88.1 104
2P
2
paracone only 125 Absent 0.0 0 Present 100.0 125
3P
3
w/protocone 125 Absent 96.0 120 Present 04.0 5
4P
4
w/protocone 125 Absent 0.0 0 Present 100.0 125
5M
1
pericone 116 Absent 87.1 101 Present 12.9 15
6M
1
hypocone 123 Absent 0.0 0 Present 100.0 123
7M
1
lingual extension/style 124 Absent 93.5 116 Present 06.5 8
8M
1
parastyle 118 Absent 10.2 12 Present 89.8 106
9M
1
metastyle 121 Absent 0.0 0 Present 100.0 121
10 M
1
shape 125 Square 0.8 1 Elongated 99.2 124
11 M
1
buccal cingulum 125 Strong 49.6 62 Weak 50.4 63 Absent 0.0 0
12 M
2
pericone 115 Absent 89.6 103 Present 10.4 12
13 M
2
hypocone 120 Absent 03.3 4 Present 96.7 116
14 M
2
lingual extension/style 120 Absent 100.0 120 Present 0.0 0
15 M
2
parastyle 120 Absent 06.7 8 Present 93.3 112
16 M
2
metastyle 124 Absent 0.0 0 Present 100.0 124
17 M
2
shape 122 Square 0.0 0 Elongated 100.0 122
18 M
2
buccal cingulum 124 Strong 56.5 70 Weak 42.7 53 Absent 0.8 1
19 M
3
pericone 120 Absent 98.3 119 Present 0.8 1
20 M
3
hypocone 106 Absent 95.3 101 Present 04.7 5
21 M
3
parastyle 120 Absent 10.8 13 Present 89.2 107
22 M
3
metastyle 121 Absent 05.0 6 Present 95.0 115
23 M
3
buccal cingulum 125 Strong 62.4 78 Weak 37.6 47 Absent 0.0 0
24 P
2
caniniform 125 Absent 0.0 0 Present 100.0 125
25 P
2
buccal cingulum 124 Strong 26.6 33 Weak 72.6 90 Absent 0.8 1
26 P
3
buccal cingulum 126 Strong 48.4 61 Weak 51.6 65 Absent 0.0 0
27 P
4
thick buccal cingulum 125 Absent 0.0 0 Present 100.0 125
28 P
4
w/talonid 125 Absent 0.8 1 Present 99.2 124
29 P
4
entoconid position 125 Central 100.0 125 Lingual 0.0 0
30 M
1
shape 124 Square 0.0 0 Rectangular 01.6 2 Parrallelogram 98.4 122
31 M
1
buccal cingulum 126 Strong 27.0 34 Weak 72.2 91 Absent 0.8 1
32 M
1
distal cingular shelf 123 Strong 11.4 14 Weak 74.0 91 Absent 14.6 18
33 M
2
shape 123 Square 27.6 34 Rectangular 05.7 7 Parrallelogram 66.7 82
34 M
2
buccal cingulum 126 Strong 29.4 37 Weak 69.8 88 Absent 0.8 1
35 M
2
distal cingular shelf 124 Strong 32.3 40 Weak 60.5 75 Absent 07.3 9
36 M
3
buccal cingulum 125 Strong 31.2 39 Weak 68.0 85 Absent 0.8 1
37 M
3
w/hypoconulid 123 Absent 01.6 2 Present 98.4 121
38 M
3
w/notch between hypoconid/hypoconulid 124 Absent 01.6 2 Present 98.4 122
39 M
3
w/cingulum in notch 118 Absent 11.0 13 Present 89.0 105
40 M
3
w/entoconid and hypoconulid 108 Distinct 86.1 93 Not distinct 13.9 15
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e2014
Appendix B. Variation in Amboasary dental traits: left teeth
# Trait nCondition % nCondition % nCondition % n
1 C w/distal style 111 Absent 10.8 12 Present 89.2 99
2P
2
paracone only 125 Absent 0.0 0 Present 100.0 125
3P
3
w/protocone 124 Absent 97.6 121 Present 02.4 3
4P
4
w/protocone 125 Absent 0.0 0 Present 100.0 125
5M
1
pericone 115 Absent 87.8 101 Present 12.2 14
6M
1
hypocone 122 Absent 0.0 0 Present 100.0 122
7M
1
lingual extension/style 124 Absent 94.4 117 Present 05.6 7
8M
1
parastyle 115 Absent 08.7 10 Present 91.3 105
9M
1
metastyle 119 Absent 0.0 0 Present 100.0 119
10 M
1
shape 125 Square 0.8 1 Elongated 99.2 124
11 M
1
buccal cingulum 125 Strong 48.8 61 Weak 51.2 64 Absent 0.0 0
12 M
2
pericone 116 Absent 91.4 106 Present 08.6 10
13 M
2
hypocone 122 Absent 01.6 2 Present 98.4 120
14 M
2
lingual extension/style 120 Absent 99.2 119 Present 0.8 1
15 M
2
parastyle 120 Absent 05.8 7 Present 94.2 113
16 M
2
metastyle 124 Absent 0.0 0 Present 100.0 124
17 M
2
shape 122 Square 0.0 0 Elongated 100.0 122
18 M
2
buccal cingulum 125 Strong 56.8 71 Weak 42.4 53 Absent 0.8 1
19 M
3
pericone 121 Absent 98.4 119 Present 01.6 2
20 M
3
hypocone 111 Absent 96.4 107 Present 03.6 4
21 M
3
parastyle 118 Absent 09.3 11 Present 90.7 107
22 M
3
metastyle 117 Absent 04.3 5 Present 95.7 112
23 M
3
buccal cingulum 124 Strong 62.1 77 Weak 37.9 47 Absent 0.0 0
24 P
2
caniniform 126 Absent 0.0 0 Present 100.0 126
25 P
2
buccal cingulum 125 Strong 26.4 33 Weak 72.8 91 Absent 0.8 1
26 P
3
buccal cingulum 124 Strong 51.6 64 Weak 48.4 60 Absent 0.0 0
27 P
4
thick buccal cingulum 125 Absent 0.0 0 Present 100.0 125
28 P
4
w/talonid 125 Absent 0.0 0 Present 100.0 125
29 P
4
entoconid position 125 Central 100.0 125 Lingual 0.0 0
30 M
1
shape 124 Square 0.0 0 Rectangular 01.6 2 Parrallelogram 98.4 122
31 M
1
buccal cingulum 125 Strong 26.4 33 Weak 72.8 91 Absent 0.8 1
32 M
1
distal cingular shelf 123 Strong 11.4 14 Weak 71.5 88 Absent 17.1 21
33 M
2
shape 124 Square 23.4 29 Rectangular 05.6 7 Parrallelogram 71.0 88
34 M
2
buccal cingulum 125 Strong 28.8 36 Weak 70.4 88 Absent 0.8 1
35 M
2
distal cingular shelf 124 Strong 31.5 39 Weak 61.3 76 Absent 07.3 9
36 M
3
buccal cingulum 118 Strong 32.2 38 Weak 66.9 79 Absent 0.8 1
37 M
3
w/hypoconulid 122 Absent 0.8 1 Present 99.2 121
38 M
3
w/notch between hypoconid/hypoconulid 123 Absent 0.8 1 Present 99.2 122
39 M
3
w/cingulum in notch 115 Absent 12.2 14 Present 87.8 101
40 M
3
w/entoconid and hypoconulid 101 Distinct 85.1 86 Not distinct 14.9 15
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e20 15
Appendix C. Variation in Beza Mahafaly dental traits: right teeth
# Trait nCondition % nCondition % nCondition % n
1 C w/distal style 5 Absent 0.0 0 Present 100.0 5
2P
2
paracone only 5 Absent 0.0 0 Present 100.0 5
3P
3
w/protocone 10 Absent 0.0 0 Present 100.0 10
4P
4
w/protocone 13 Absent 0.0 0 Present 100.0 13
5M
1
pericone 10 Absent 90.0 9 Present 10.0 1
6M
1
hypocone 12 Absent 0.0 0 Present 100.0 12
7M
1
lingual extension/style 12 Absent 100.0 12 Present 0.0 0
8M
1
parastyle 11 Absent 0.0 0 Present 100.0 11
9M
1
metastyle 10 Absent 0.0 0 Present 100.0 10
10 M
1
shape 12 Square 0.0 0 Elongated 100.0 12
11 M
1
buccal cingulum 11 Strong 9.1 1 Weak 90.0 10 Absent 0.0 0
12 M
2
pericone 9 Absent 77.8 7 Present 22.2 2
13 M
2
hypocone 10 Absent 10.0 1 Present 90.0 9
14 M
2
lingual extension/style 10 Absent 100.0 10 Present 0.0 0
15 M
2
parastyle 10 Absent 20.0 2 Present 80.0 8
16 M
2
metastyle 10 Absent 0.0 0 Present 100.0 10
17 M
2
shape 11 Square 0.0 0 Elongated 100.0 11
18 M
2
buccal cingulum 11 Strong 18.2 2 Weak 81.8 9 Absent 0.0 0
19 M
3
pericone 11 Absent 100.0 10 Present 0.0 0
20 M
3
hypocone 10 Absent 100.0 10 Present 0.0 0
21 M
3
parastyle 12 Absent 9.1 1 Present 90.9 11
22 M
3
metastyle 11 Absent 27.3 3 Present 72.7 8
23 M
3
buccal cingulum 9 Strong 11.1 1 Weak 88.9 8 Absent 0.0 0
24 P
2
caniniform 6 Absent 0.0 0 Present 100.0 6
25 P
2
buccal cingulum 6 Strong 33.3 2 Weak 66.7 4 Absent 0.0 0
26 P
3
buccal cingulum 6 Strong 50.0 3 Weak 50.0 3 Absent 0.0 0
27 P
4
thick buccal cingulum 8 Absent 0.0 0 Present 100.0 8
28 P
4
w/talonid 8 Absent 0.0 0 Present 100.0 8
29 P
4
entoconid position 8 Central 37.5 3 Lingual 62.5 5
30 M
1
shape 11 Square 9.1 1 Rectangular 36.4 4 Parrallelogram 54.5 6
31 M
1
buccal cingulum 11 Strong 36.4 4 Weak 54.5 6 Absent 11.1 1
32 M
1
distal cingular shelf 10 Strong 20.0 2 Weak 40.0 4 Absent 40.0 4
33 M
2
shape 13 Square 100.0 13 Rectangular 0.0 0 Parrallelogram 0.0 0
34 M
2
buccal cingulum 12 Strong 25.0 3 Weak 75.0 9 Absent 0.0 0
35 M
2
distal cingular shelf 13 Strong 38.5 5 Weak 38.5 5 Absent 23.0 3
36 M
3
buccal cingulum 10 Strong 30.0 3 Weak 70.0 7 Absent 0.0 0
37 M
3
w/hypoconulid 10 Absent 0.0 0 Present 100.0 10
38 M
3
w/notch between hypoconid/hypoconulid 9 Absent 0.0 0 Present 100.0 9
39 M
3
w/cingulum in notch 9 Absent 11.1 1 Present 88.9 8
40 M
3
w/entoconid and hypoconulid 8 Distinct 100.0 8 Not distinct 0.0 0
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e2016
Appendix D. Variation in Beza Mahafaly dental traits: left teeth
# Trait nCondition % nCondition % nCondition % n
1 C w/distal style 5 Absent 0.0 0 Present 100.0 5
2P
2
paracone only 6 Absent 0.0 0 Present 100.0 6
3P
3
w/protocone 7 Absent 0.0 0 Present 100.0 7
4P
4
w/protocone 9 Absent 0.0 0 Present 100.0 9
5M
1
pericone 7 Absent 85.7 6 Present 14.3 1
6M
1
hypocone 9 Absent 0.0 0 Present 100.0 9
7M
1
lingual extension/stylid 9 Absent 88.9 8 Present 11.1 1
8M
1
parastyle 8 Absent 0.0 0 Present 100.0 8
9M
1
metastyle 8 Absent 0.0 0 Present 100.0 8
10 M
1
shape 9 Square 0.0 0 Elongated 100.0 9
11 M
1
buccal cingulum 9 Strong 11.1 1 Weak 88.9 8 Absent 0.0 0
12 M
2
pericone 7 Absent 71.4 5 Present 28.6 2
13 M
2
hypocone 9 Absent 0.0 0 Present 100.0 9
14 M
2
lingual extension/stylid 8 Absent 100.0 8 Present 0.0 0
15 M
2
parastyle 8 Absent 0.0 0 Present 100.0 8
16 M
2
metastyle 8 Absent 0.0 0 Present 100.0 8
17 M
2
shape 9 Square 0.0 0 Elongated 100.0 9
18 M
2
buccal cingulum 8 Strong 25.0 2 Weak 75.0 6 Absent 0.0 0
19 M
3
pericone 7 Absent 100.0 7 Present 0.0 0
20 M
3
hypocone 7 Absent 100.0 7 Present 0.0 0
21 M
3
parastyle 8 Absent 12.5 1 Present 87.5 7
22 M
3
metastyle 7 Absent 42.9 3 Present 57.1 4
23 M
3
buccal cingulum 6 Strong 16.7 1 Weak 83.3 5 Absent 0.0 0
24 P
2
caniniform 5 Absent 0.0 0 Present 100.0 5
25 P
2
buccal cingulum 5 Strong 40.0 2 Weak 60.0 3 Absent 0.0 0
26 P
3
buccal cingulum 6 Strong 50.0 3 Weak 50.0 3 Absent 0.0 0
27 P
4
thick buccal cingulum 8 Absent 0.0 0 Present 100.0 8
28 P
4
w/talonid 8 Absent 0.0 0 Present 100.0 8
29 P
4
entoconid position 8 Central 12.5 1 Lingual 87.5 7
30 M
1
shape 9 Square 11.1 1 Rectangular 33.3 3 Parrallelogram 55.6 5
31 M
1
buccal cingulum 8 Strong 37.5 3 Weak 62.5 5 Absent 0.0 0
32 M
1
distal cingular shelf 7 Strong 14.2 1 Weak 42.9 3 Absent 42.9 3
33 M
2
shape 8 Square 75.0 6 Rectangular 0.0 0 Parrallelogram 25.0 2
34 M
2
buccal cingulum 8 Strong 25.0 2 Weak 75.0 6 Absent 0.0 0
35 M
2
distal cingular shelf 8 Strong 50.0 4 Weak 25.0 2 Absent 25.0 2
36 M
3
buccal cingulum 7 Strong 14.3 1 Weak 85.7 6 Absent 0.0 0
37 M
3
w/hypoconulid 8 Absent 0.0 0 Present 100.0 8
38 M
3
w/notch between hypoconid/hypoconulid 8 Absent 0.0 0 Present 100.0 8
39 M
3
w/cingulum in notch 6 Absent 33.3 2 Present 66.74
40 M
3
w/entoconid and hypoconulid 6 Distinct 83.3 5 Not distinct 16.7 1
F.P. Cuozzo et al. / Journal of Human Evolution 64 (2013) 1e20 17
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