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SHORT COMMUNICATION
Morphometrics of Graomys (Rodentia, Cricetidae) from
Central-Western Argentina
Juan Jose´ Martı
´nez
a,
, Jero´nimo Matı
´as Krapovickas
b
, Gerardo Rau´ l Theiler
c
a
Ca
´tedra de Gene
´tica de Poblaciones y Evolucio
´n, Facultad de Ciencias Exactas, Fı
´
sicas y Naturales,
Universidad Nacional de Co
´rdoba, Av. Ve
´lez Sarsfield 299 Co
´rdoba, Argentina
b
Ca
´tedra de Paleontologı
´
a, Seccio
´n Paleovertebrados, Facultad de Ciencias Exactas, Fı
´
sicas y Naturales,
Universidad Nacional de Co
´rdoba, Av. Ve
´lez Sarsfield 1611 Co
´rdoba, Argentina
c
Ca
´tedra de Introduccio
´n a la Fı
´
sica y Quı
´
mica Biolo
´gicas, Facultad de Odontologı
´
a, Universidad Nacional de Co
´rdoba,
Pabello
´n Argentina, Ciudad Universitaria, Co
´rdoba, Argentina
Received 18 July 2008; accepted 3 November 2008
Keywords: Graomys; Cytogenetics; Morphometrics; Multivariate analysis; Argentina
The taxonomy and systematics of the sigmodontine
rodents of the tribe Phyllotini are a matter of continuous
revision (Braun 1993;Steppan 1993, 1995;Steppan et al.
2007). In this sense, the species of the genus Graomys
(Thomas, 1916), with a wide geographical distribution
range in South America, lack a comprehensive systema-
tic revision.
Graomys centralis was originally described as a
subspecies of Eligmodontia (E. griseoflavus centralis)by
Thomas (1902), on the basis of five specimens from Cruz
del Eje (Co´ rdoba, Argentina). In this description,
Thomas pointed out the lower size of tympanic bullas
of centralis specimens in relation to the other subspecies
of the genus, especially when compared to cachinus and
chacoensis. However, Hershkovitz (1962) presented the
species cachinus,centralis,chacoensis,lockwoodi,and
medius, as synonyms of griseoflavus.Musser and
Carleton (1993), however, indicated the species homo-
geneity as ‘‘highly suspicious’’.
Several works have shown that G. griseoflavus
includes numerous cytotypes (2n¼34, 35, 36, 37, 38,
41, and 42) that are morphologically indistinguishable
(Wainberg and Fronza 1974;Zambelli et al. 1994). The
cytotypes 2n¼36, 37, and 38 are karyotypically mixed
populations and occur mainly in the Monte Desert and
Patagonic steppe, whereas cytotype 2n¼42 occurs in
the Espinal and in Western Chaco ecoregions (Theiler
et al. 1999).
Laboratory crossing tests demonstrated post-zygotic
isolation between animals with 2n¼42 and 2n¼36–38.
The reproductive isolation was clearly asymmetric; there
was no copula between males 2n¼36–38 and females
2n¼42, whereas the reciprocal crossings (females
2n¼36–38 males 2n¼42) produced viable sterile
hybrid offspring with 39 or 40 chromosomes (Theiler
and Blanco 1996a). Theiler and Blanco (1996b) also
found reinforcement of this post-zygotic isolation by
mechanisms involving olfactory discrimination during
female estrus. Females discriminated males of compa-
tible chromosome complement from those that would
produce non-viable offspring or sterile hybrids. On the
basis of these evidences, Theiler and Blanco (1996b)
concluded that 2n¼42 cytotype and 2n¼36–38 com-
plex are two sibling species.
Phylogenetic studies based on Cyt b and D-loop
fragments of the mtDNA showed that animals with
2n¼41 and 2n¼42 form a separate clade from
individuals with 2n¼34–38, the latter being included
in another well-supported group (Catanesi et al. 2002,
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1616-5047/$ - see front matter r2008 Deutsche Gesellschaft fu¨rSa¨ ugetierkunde. Published by Elsevier GmbH. All rights reserved.
doi:10.1016/j.mambio.2008.11.003 Mamm. biol. 75 (2010) 180–185
Corresponding author.
E-mail address: juan_jmart@yahoo.com.ar (J.J. Martı
´nez).
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2006). This result confirms the existence of at least two
sibling species.
Several authors (Theiler 1997;Tiranti 1998;Theiler
et al. 1999) described 2n¼42 cytotypes in individuals
found in localities near Cruz del Eje, the site where
the type specimens of Graomys centralis Thomas (1902)
was obtained.
Graomys centralis was validated on the basis of
concrete evidence (Theiler 1997;Musser and Carleton
2005;Dı
´az et al. 2006). Rodents from the Graomys
complex showing a 2n¼42 cytotypes were included in
this taxon. However, the morphometric variation of this
species from G. griseoflavus, has never been analyzed. In
this study, we present the first comparative morpho-
metric study of specimens of the species G. centralis and
G. griseoflavus. We also examine the diploid chromo-
some number of specimens from Cruz del Eje, type
locality for G. centralis.
Five individuals (two males and three females) were
live-trapped in a woody area located about 8 km from
Cruz del Eje (301430S, 641490W; Co´ rdoba province). The
karyotypes of these specimens were obtained according
to Theiler and Blanco (1996a).
Forty-three adult skulls (M3 erupted) belonging to
previously karyotyped G. centralis and G. griseoflavus
specimens (Theiler 1997) were examined; 23 additional
skulls of non-karyotyped specimens were included for
subsequent identification. All the examined specimens
are listed below, indicating locality and catalogue
number. The localities are shown in Fig. 1. The
karyotyped specimens have not been accessioned yet
and are currently identified with the collector’s initials
(GRT, Gerardo R Theiler). The non-karyotyped speci-
mens identified as G. griseoflavus are deposited in the
Universidad Nacional de Rı
´o Cuarto collection
(CUNRC), Grupo de Investigaciones en Ecologı
´ade
Poblaciones (GIEP), Universidad Nacional de Rı
´o
Cuarto, Rı
´o Cuarto, Argentina.
Specimens examined: Graomys centralis 2n¼42, (20).
Argentina: Chamical, La Rioja (GRT 024, 025, 026,
027, 028, 041, CUNRC h10, CUNRC m20); Villa de
Marı
´adeRı
´o Seco, Co´ rdoba (GRT 029. 030); Dea´n
Funes, Co´ rdoba (GRT 037, 038, 039); Santiago Temple,
Co´ rdoba (GRT 035, 036); Cruz del Eje, Co´ rdoba (GRT
031, 032, 033, 034, 040).
Graomys griseoflavus 2n¼36–38, (23). Argentina:
Papagayos, San Luis (GRT 001, 002, 003); Mendoza,
Mendoza (GRT 010, 011, 012, 013, 014, 015); N
˜acun˜a´n,
Mendoza (GRT 005, 006, 007, 008, 009); Me´ danos,
Buenos Aires (GRT 016, 017, 018, 019, 020, 021, 022,
023); Puerto Madryn, Chubut (GRT 004).
Non-karyotyped specimens (24). Argentina: Villa de
Marı
´adeRı
´o Seco, Co´ rdoba (CUNRC 1522, 1523,
1524, 1526, 4004, 4005, 4006, 4047, 4052, 4066, 4137);
San Vicente, Co´ rdoba (CUNRC, 2354), Yacanto,
Co´ rdoba (CUNRC 2387, 2816); Villa Dolores, Co´ rdoba
(CUNRC 50103); Cruz del Eje, Co´ rdoba (CUNRC
2178, 2180, 2195, 4264, 4283, 4952, 4953, 4954,
44781);Villa del Carmen, San Luis (CUNRC 43462).
We also made univariate and multivariate analyses
using 19 cranial measurements that were taken with a
caliper to the nearest 0.02 mm. The measurements are as
follows: Greatest length of skull (GLS), basal length
(BL), palatal length (PL), diastema length (DL),
zygomatic breadth (ZB), least interorbital breadth
(LIB), breadth of braincase (BB), rostral breadth
(RB), nasal length (NL), nasal width (NW), length of
incisive foramen (LIF), length of maxillary tooth row
(LM), length of mandibulary tooth row (Lm), mastoidal
breadth (MB), postpalatal length (PPL), length between
molars (LBM), condylo-first molar length (C1ML),
length of tympanic bulla (LTB), and width of tympanic
bulla (WTB).
At-test was performed to evaluate univariate mean
differences between the species across the variables. A
principal components analysis (PCA) was performed on
the correlation matrix to characterize the morphological
variation among the karyotyped and non-karyotyped
specimens. The first eight principal components (92% of
total variation) were used for a discriminant analysis to
obtain the rates of correct classification of previously
karyotyped animals; the values of discriminant function
were used to examine the classification of non-karyo-
typed animals. Statistical analyses were performed with
Infostat (2008) and PAST (Hammer et al. 2001).
The cytogenetic study showed that all individuals
examined from Cruz del Eje had similar karyotypes with
ARTICLE IN PRESS
Fig. 1. Location of Graomys specimens examined. The
localities were (1) Villa de Marı
´adeRı
´o Seco, (2) De´ an
Funes, (3) Cruz del Eje, (4) Chamical, (5) Santiago Temple, (6)
Villa Dolores, (7) San Vicente, (8) Yacanto, (9) Papagayos,
(10) Villa del Carmen, (11) Mendoza, (12) N
˜acun˜a´n, (13)
Me´ danos, and (14) Puerto Madryn.
J.J. Martı
´nez et al. / Mamm. biol. 75 (2010) 180–185 181
Author's personal copy
42 chromosomes (Fig. 2). Pairs 1–17 are acrocentric
decreasing in size. Pair 18 is medium-sized submeta-
centric chromosomes, and pairs 19 and 20 are composed
of small submetacentric chromosomes. The X chromo-
some is a large submetacentric and Y is a small
acrocentric. Starting from the cytotype 2n¼42 in
G. centralis, two centric fusions (15–17 and 16–18)
originated cytotype 2n¼38. A third fusion involving
chromosomes 1 and 6 produced cytotype 2n¼36. The
2n¼37 cytotype is the heterozygote for 1–6 Robertso-
nian fusion. Finally, a fourth centric fusion has
been described involving chromosomes 2 and 5, yield-
ing cytotypes 2n¼34 and 2n¼35 in heterozygotes
(Zambelli et al. 1994;Theiler 1997).
Fourteen of 19 measurements differed significantly
and were greater in G. griseoflavus than in G. centralis.
On the other hand, measurements from the type
G. centralis Thomas (1902) were more similar to those
of specimens with 2n¼42 (classified by us as
G. centralis) than to measurements of G. griseoflavus
specimens (2n¼36–38) (Table 1).
The first three principal components (PC) on 19
measurements (Fig. 3) explained 77.5% of the total
variation, 65% of the variation being explained by the
first PC. All the measurements are positively correlated
with the first PC, which is interpreted as a measure
of size. Almost all the non-karyotyped individuals
are more related to G. centralis specimens than to
G. griseoflavus ones.
The discriminant analysis correctly classified 95.35%
of the specimens previously classified on the basis
of their karyotypes. Two specimens (one of each
species) were misclassified: one from Chamical in La
Rioja province and the other from Papagayos in
San Luis province. Considering the high rate of
correct classification, the status of each non-karyotyped
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Fig. 2. Standard Giemsa-stained bone marrow karyotype of one male of Graomys from Cruz del Eje, Cordoba with 2n¼42; type
locality of Graomys centralis.
Table 1. Descriptive statistics (mean7S.D.) of cranial measurements (mm) of G. centralis,G. griseoflavus, and the type of G.
centralis (Thomas, 1902). Pof ttest of mean differences was estimated.
Measurement G. centralis (N¼20) G. griseoflavus (N ¼23) G. centralis (holotype) P
GLS 33.2771.71 35.1571.71 33.50 0.0009
BL 28.4271.76 32.8271.41 26.00 o0.0001
PL 6.1470.52 6.3370.48 – 0.2204
DL 8.6170.70 9.5170.69 8.50 0.0001
ZB 17.2471.21 17.8170.71 17.00 0.0750
LIB 5.5170.62 5.4970.38 5.40 0.8846
BB 14.0770.58 14.7570.64 13.50 0.0007
RB 5.5770.41 5.5970.41 – 0.9117
NL 13.7570.88 14.5271.11 14.00 0.0177
NW 3.9270.32 3.9970.33 – 0.4727
LIF 7.2170.43 7.9970.53 – o0.0001
LM 5.3570.25 5.5170.26 4.50 0.0409
Lm 5.2570.22 5.4370.30 – 0.0417
MB 12.4470.44 12.8870.43 – 0.0018
PPL 11.4070.81 12.7270.75 – o0.0001
LBM 6.5870.43 6.8370.27 – 0.0320
C1ML 19.7571.01 21.1870.74 – o0.0001
LTB 6.3570.33 7.2270.34 6.00 o0.0001
WTB 4.4870.44 5.2870.40 – o0.0001
J.J. Martı
´nez et al. / Mamm. biol. 75 (2010) 180–185182
Author's personal copy
individual was assigned based on a discrimination func-
tion analysis.
The centroids in the discriminant space are 2.17
(3.45–0.14) and 1.87 (0.45–3.95) for G. centralis
and G. griseoflavus, respectively. Almost all the non-
karyotyped specimens were classified as G. centralis,
except two individuals, CUNRC 43462 and CUNRC
50103, from Villa del Carmen and Villa Dolores,
respectively. The first specimen (CUNRC 43462) is
30 km away from Papagayos, San Luis Province, where
individuals of G. griseoflavus occur. The other specimen,
CUNRC 50103, was collected 80 km away from
Papagayos in San Luis Province, a site very close to
the localities of Yacanto (21 km) and San Vicente
(18 km), where the specimens were classified as
G. centralis. The coexistence of these two species in the
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Fig. 3. Principal component analysis (PCA) using all standardized cranial characters in Graomys specimens (N¼67): (A) Plot of
principal component 1 versus principal component 2. (B) Plot of principal component 1 versus principal component 3. m:G.
centralis specimens; J:G. griseoflavus specimens; : non-kayotyped specimens.
J.J. Martı
´nez et al. / Mamm. biol. 75 (2010) 180–185 183
Author's personal copy
same area might be due to a transitional physiognomy
between Chaco and Monte ecoregions. Further field
studies in the area are needed to elucidate this situation.
In a recent study, Lanzone et al. (2007) proposed a
new taxonomic status for individuals from Chumbicha,
Catamarca province, type locality of Graomys medius,
on the basis of cytogenetic and morphometric evidence.
They suggested that G. medius should be synonymized
with G. centralis. These authors also pointed out
the smaller size of individuals from Chumbicha than
that of G. griseoflavus specimens from N
˜acun˜a´n. In
addition, they remarked that specimens from Villa
Hayes, in Paraguay, have 2n¼42 and stated that ‘‘If
only one Graomys species inhabits the Chaco biome,
the name chacoensis Allen (1901) should be applied to
those specimens’’.
In this study, we analyzed the morphometric variation
of G. centralis from central-western Argentina, where
the main studies of the genus were conducted, and
distinguished that species from G. griseoflavus speci-
mens. This discrimination, however, was possible
mainly because of size differences; therefore, other
methods, such geometric morphometrics, should be
implemented to detect slight differences due to shape
changes. In addition, the karyotypes of animals from
Cruz del Eje, type locality of G. centralis, are provided
for the first time. A comprehensive morphometric
study of individuals representing the complete genus
and the range of distribution in South America may
clarify the species taxonomy.
Acknowledgements
We are grateful to Jose´ Priotto and Jaime Polop from
Universidad Nacional de Rı
´o Cuarto who kindly
permitted the access to animals in their care. We also
thank Teresa Sanchez and Veronica Bertero from
CIPAL, Universidad Nacional de Co´ rdoba. Guillermo
Albrieu assisted with the English version. Financial
support was provided by Consejo Nacional de Investi-
gaciones Cientı
´ficas y Te´cnicas (CONICET) to JJM.
JJM is a postgraduate student of the Doctorado en
Ciencias Biolo´ gicas, Universidad Nacional de Co´ rdoba.
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... centralis) from central western Argentina (Theiler et al., 1999;Catanesi et al., 2002Catanesi et al., , 2006Martínez et al., 2010b), the geographic distribution and variation in skull shape in G. chacoensis and G. griseoflavus have never been examined. Martínez et al. (2010a), using traditional morphometrics on specimens collected in central western Argentina, were able to distinguish the two species, but only on the basis of size variation. The main drawback of traditional morphometrics is that it measures size rather than shape and that it can be difficult to separate information about shape from that about size. ...
... The interspecific differences in centroid size in the dorsal and ventral views of the skulls are consistent in that G. domorum has a larger skull than the other two species, and that G. griseoflavus tends to have a larger skull than G. chacoensis. These results agree with those of traditional morphometrics by Martínez et al. (2010a), which find significant differences between G. griseoflavus and G. chacoensis in fourteen of the nineteen measurements used. These measurements were larger in G. griseoflavus than in G. chacoensis. ...
... In contrast, G. griseoflavus possesses well developed tympanic bullae, and smaller incisive foramina than G. chacoensis, which has a more rostrally positioned fossa mesopterygoidea than G. griseoflavus. Some of these results are very similar to and corroborate the ones found by Martínez et al. (2010a) using traditional morphometrics. These results can be used for the taxonomic identification of specimens and as a basis for future morphological analyses of the genus Graomys. ...
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