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Species groups and the evolutionary diversification of tuco-tucos, genus Ctenomys (Rodentia: Ctenomyidae)

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Abstract We present the most comprehensive study to date of species groups in Ctenomys (tuco-tucos), a species-rich genus of Neotropical rodents. To explore phylogenetic relationships among 38 species and 12 undescribed forms we sequenced the complete mitochondrial cytochrome-b genes of 34 specimens and incorporated 50 previously published sequences. Parsimony, likelihood, and Bayesian phylogenetic analyses were performed using additional hystricognath rodents as outgroup taxa. The basal dichotomy of Ctenomys splits C. sociabilis from the remaining tuco-tucos, within which 8 main species groups were identified: boliviensis, frater, mendocinus, opimus, magellanicus, talarum, torquatus, and tucumanus. Whereas most of these groups refer to previous clades proposed on the basis of chromosomes or morphology, the torquatus and magellanicus species groups are novel taxonomic hypotheses. However, relationships among species groups are poorly resolved. Furthmore, the positions of C. leucodon, C. maulinus, and C. t...
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Species groups and the evolutionary diversification of tuco-tucos, genus
Ctenomys (Rodentia: Ctenomyidae)
ANDRE
´SPARADA,* GUILLERMO D’ELI
´A,CLAUDIO J. BIDAU,AND ENRIQUE P. LESSA
Laboratorio de Evolucio´n, Facultad de Ciencias, Universidad de la Repu´blica, Montevideo, Uruguay (AP, EPL)
Departamento de Ecologı
´a & Center for Advanced Studies in Ecology & Biodiversity, Pontificia Universidad Cato´lica,
Santiago, Chile (AP)
Instituto de Ecologı
´a y Evolucio´n, Universidad Austral de Chile, Valdivia, Chile (GD)
Lavorato´rio de Biologia e Parasitologia de Mamı
´feros Silvestres Reservato´rios, Instituto Oswaldo Cruz, FIOCRUZ, Rio
de Janeiro, Brazil (CJB)
* Correspondent: andrespara@gmail.com
We present the most comprehensive study to date of species groups in Ctenomys (tuco-tucos), a species-rich
genus of Neotropical rodents. To explore phylogenetic relationships among 38 species and 12 undescribed
forms we sequenced the complete mitochondrial cytochrome-bgenes of 34 specimens and incorporated 50
previously published sequences. Parsimony, likelihood, and Bayesian phylogenetic analyses were performed
using additional hystricognath rodents as outgroup taxa. The basal dichotomy of Ctenomys splits C. sociabilis
from the remaining tuco-tucos, within which 8 main species groups were identified: boliviensis,frater,
mendocinus,opimus,magellanicus,talarum,torquatus, and tucumanus. Whereas most of these groups refer to
previous clades proposed on the basis of chromosomes or morphology, the torquatus and magellanicus species
groups are novel taxonomic hypotheses. However, relationships among species groups are poorly resolved.
Furthmore, the positions of C. leucodon,C. maulinus, and C. tuconax are conflicting or unresolved, and they
might represent additional independent lineages. On the basis of molecular dating, we estimate that most
species groups originated approximately 3 million years ago.
Key words: Ctenomys, cytochrome b, molecular dating, species groups, subterranean rodents, systematics, tuco-tucos
E2011 American Society of Mammalogists
DOI: 10.1644/10-MAMM-A-121.1
The Neotropical region hosts a diverse, yet incompletely
characterized, variety of mammals. During the last few
decades field surveys, coupled with collection-based studies
and molecular analyses, have helped characterize this complex
mammalian fauna. Echimyids (spiny rats) and ctenomyids
(tuco-tucos) are the 2 most diverse families of South American
hystricognaths. Ctenomys, the sole living genus of the family
Ctenomyidae, is poorly known because of the partial
characterization of its alpha diversity and the unknown
processes behind its diversification. Despite a moderate degree
of morphological and ecological diversity, Ctenomys is
characterized by high species richness (approximately 60
recognized living species—Woods and Kilpatrick 2005).
Speciation is considered to be rapid for the genus to have
reached its current diversity since its appearance in the late
Pliocene (Reguero et al. 2007; Verzi et al. 2010).
Species of Ctenomys are distributed from southern Peru and
southern Brazil to Tierra del Fuego through parts of Chile and
most of Argentina, Bolivia, Paraguay, and Uruguay (Reig et
al. 1990; Fig. 1). Tuco-tucos occur in a wide variety of
habitats, from the Andean Puna above 4,000 m to the coastal
dunes of the Atlantic, and from the mesic and humid Pampas
to the dry Chaco and Monte desert. They have the largest
known range of chromosomal variation of any mammal genus,
with diploid numbers ranging from 2n 510 to 2n 570 (Cook
et al. 1990; Novello and Lessa 1986). Reig (1989) suggested
that tuco-tucos underwent a process of explosive radiation (see
also Castillo et al., 2005; Cook and Lessa 1998). Efforts
directed at revealing the macroevolutionary pattern of
diversification of Ctenomys have been hampered by a lack
of understanding of species limits and of phylogenetic
relationships among them. For example, Sage et al. (1986)
indicated that the genus was in a state of ‘‘taxonomic chaos.’’
Early efforts of establishing subgenera (Osgood 1946) or
www.mammalogy.org
Journal of Mammalogy, 92(3):671–682, 2011
671
sections (Ellerman 1940) for Ctenomys were later refuted
(D’Elı
´a et al. 1999). Other authors (Cabrera 1961) reduced
many forms to synonyms or subspecies that were considered
to be unfounded (Reig and Kiblisky 1969). In addition, many
forms are known only from their original descriptions on the
basis of one or a few specimens. Until the late 1960s
classification of tuco-tucos was based primarily on pelage color,
cranial morphology, and body size. More recent attempts were
based on allozyme frequencies (Sage et al. 1986), karyotypes
(Reig and Kiblisky 1969), penial morphology (Altuna and Lessa
1985; Balbontin et al. 1996), and sperm morphology (Feito and
Gallardo 1982). Vitullo et al. (1988) proposed that different
sperm variants appeared early in the radiation, possibly
indicating a natural subdivision of the genus. D’Elı
´aetal.
(1999) noted that the group of species with asymmetric sperm is
diphyletic in a phylogeny based on mitochondrial (mt)DNA
sequences. Massarini et al. (1991) and Ortells and Barrantes
(1994) delimited the C. mendocinus and Corrientes species
groups, respectively, on the basis of chromosomal variation.
Another proposal of classification was based on copy number of
a major satellite DNA sequence (Rossi et al. 1993).
Taking into account the geographical distribution of species
as an historical framework for the radiation, Contreras and
Bidau (1999) proposed 8 species groups (Table 1); however,
not all known species were considered. The first study with an
explicit phylogenetic approach included only Argentinean and
Bolivian species and was based on morphologic and
karyotypic characters (Gardner 1990). Subsequently, Cook
and Yates (1994) studied allozymic variation for Bolivian
species, and Ortells (1995) examined the variation of
karyotype G-band patterns in Argentinean species. More
recently, Lessa and Cook (1998), D’Elı
´a et al. (1999),
Mascheretti et al. (2000), and Slamovits et al. (2001) analyzed
sequences of the mitochondrial cytochrome-bgene of some
Argentinian, Brazilian, Bolivian, Chilean, and Uruguayan
species (Table 1). Most of these arrangements were given
additional support by phylogenetic reconstructions on the basis
of sequences of 2 nuclear introns (Castillo et al. 2005).
These studies during the last 2 decades have provided
evidence for the identification of some species groups,
whereas relationships among the groups remain poorly
resolved. In addition, the taxonomic coverage of these studies
has been limited to about one-half or less of the known species
FIG.1.—Map of collecting localities of Ctenomys used in the
present study. Locality numbers refer to those of Appendix I.
TABLE 1.—Species groups of Ctenomys recognized in the present
study compared with those suggested by Contreras and Bidau (1999).
Species Contreras and Bidau (1999) This study
boliviensis Bolivian–Matogrossense boliviensis
goodfellowi Bolivian–Matogrossense boliviensis
nattereri Bolivian–Matogrossense boliviensis
steinbachi Bolivian–Matogrossense boliviensis
conoveri Bolivian–Paraguayan frater
frater Bolivian–Paraguayan frater
lewisi Bolivian–Paraguayan frater
sp. Llathu Not considered frater
fodax Patagonian magellanicus
colburni Patagonian magellanicus
coyhaiquensis Chilean spp. magellanicus
haigi Allied to C. mendocinus magellanicus
magellanicus Patagonian magellanicus
sericeus Patagonian magellanicus
australis C. mendocinus complex mendocinus
flamarioni Allied to C. mendocinus mendocinus
mendocinus Allied to C. mendocinus mendocinus
porteousi Allied to C. mendocinus mendocinus
rionegrensis Eastern mendocinus
opimus Chaco opimus
fulvus Not considered opimus
saltarius Not considered opimus
scagliai Chaco opimus
pundti Ancestral talarum
talarum Ancestral talarum
minutus Eastern torquatus
lami Not considered torquatus
pearsoni Allied to Corrientes torquatus
perrensi Corrientes torquatus
roigi Corrientes torquatus
torquatus Eastern torquatus
argentinus Chaco tucumanus
latro Chaco tucumanus
ocultus Chaco tucumanus
tucumanus Chaco tucumanus
leucodon Uncertain position No species group
maulinus Chilean spp. No species group
sociabilis Not considered No species group
tuconax Uncertain position No species group
672 JOURNAL OF MAMMALOGY Vol. 92, No. 3
of the genus. Similarly, geographic coverage is incomplete,
with large geographic areas (e.g., Patagonia) remaining
underrepresented. In molecular studies most species were
represented by 1 specimen and very few came from type
localities, which cast doubts on the application of several
taxonomic names. Given this scenario, the present work is the
most comprehensive taxonomic and geographic coverage in a
phylogenetic analysis, with representatives of 38 species and 12
undetermined forms. Some species are represented by haplo-
types gathered from more than 1 specimen, including from type
localities. Our goals were to investigate species relationships and
the timing of the main cladogenetic events within Ctenomys.
MATERIALS AND METHODS
Taxonomic sampling.The analysis was based on 71
complete sequences of the mitochondrial gene that encodes for
the cytochrome-bprotein. These sequences were from speci-
mens of 38 nominal species (including 22 topotypes) and 12
undetermined forms. The outgroup consisted of 11 sequences
from representatives of other families of Caviomorpha and of
Thryonomys and Bathyergus, 2 African hystricognath genera.
Sequences of 34 specimens were newly acquired in the
present study. The sequence of C. sociabilis was kindly
provided by Ivanna Tomasco (Universidad de la Repu´blica,
Montevideo, Uruguay, pers. comm.). Details of the specimens
studied are provided in Appendix 1 and Fig. 1. All parts of the
study involving live animals followed guidelines of the
American Society of Mammalogists (Gannon et al. 2007).
DNA extraction, amplification, and sequencing.—The
complete mitochondrial cytochrome-bgene was amplified in
two partially overlapping fragments obtained with primers
MVZ05-tuco06 and tuco07-tuco14a (Smith and Patton 1999;
Wlasiuk et al. 2003). Polymerase chain reaction (PCR)
amplifications were carried out in a reaction volume of 40 ml
containing 1.8 units of Taq polymerase (Biotools ByM Labs,
Madrid, Spain), 20 ml of 3:100 total DNA dilution, 1.6 mlof
each primer (10 mM), 1.6 ml of deoxynucleotide triphosphates
(10 mM), and 4 ml of standard 10 mM buffer provided with the
enzyme (including MgCl
2
2 mM). The PCR amplification
conditions were 3 min of initial denaturation, 31–35 cycles of
30 s of denaturation at 95uC, 30 s of annealing at 45–47uC,
and 45 s of extension at 72uC followed by 10 min of final
extension at 72uC. Negative controls were included in all PCR
experiments. Amplicons were purified and sequenced at
Macrogen Inc. (Seoul, South Korea) using the amplification
primers. Partial sequences were assembled and edited with
Sequence Navigator version 1.01 (Applied Biosystems, Inc.,
Foster City, California) and deposited in GenBank (accession
numbers HM777474 to HM777506).
Phylogenetic analysis.—Alignment was done with MUS-
CLE (Edgar 2004) using 16 iterations and running in full
mode with no manual adjustment required. Uncorrected
genetic distances (p-distance) with pairwise deletion were
computed for all pairs of sequences, and for within and
between species, using MEGA 4.1 (Kumar et al. 2008).
Maximum parsimony (MP) analysis was done with TNT
(Goloboff et al. 2008). The consensus was stabilized 10 times
according to a factor of 100 collapses with tree bisection–
reconnection (TBR). The relative support for each clade was
obtained with 1,000 jackknife replicates (Farris et al. 1996),
33%character deletion, and searching 9 times for the best tree
for each replicate. These results are shown as frequency
differences (GC values, the difference in frequency between a
group and the most contradictory group—Goloboff et al.
2003). Relative Bremer support (Bs—Goloboff and Farris
2001) values were obtained with TBR over the best trees
found with TNT, taking into account relative amounts of
favorable and contradictory evidence (0 5entirely unsup-
ported, 1 5entirely uncontradicted).
Model-based analyses were done using the HKY85 model
of sequence evolution (Hasegawa et al. 1985) selected among
56 nested models by ModelGenerator (Keane et al. 2006)
through likelihood ratio tests using the Bayesian information
criterion. Maximum-likelihood (ML) searches were carried
out with PhyML (Guindon and Gascuel 2003) using 10
random starting trees optimized through subtree pruning and
regrafting and nearest-neighbor interchange, 4 substitution
categories with an estimated gamma distribution parameter
(0.76), an estimated proportion of invariable sites (0.42), and
the estimated transition/transversion ratio. Clade support was
assessed by bootstrapping (B) with 100 replicates.
Bayesian inference was done with BEAST 1.5.2 (Drum-
mond and Rambaut 2007) as a means to recover a
phylogenetic hypothesis and simultaneously obtain an esti-
mate of the divergence time for the main lineages of tuco-
tucos. The same model of nucleotide substitution for ML was
used with empirical base frequencies, 4 gamma categories,
and partitioning into ‘‘(1+2)+3’’ (first and second codon
positions in one partition and the third position in a separate
partition). As indicated by previous analyses (not shown), the
data are not clock-like; therefore, a relaxed uncorrelated
lognormal clock was used together with no fixed mean
substitution rate. This method incorporates the time-dependent
nature of the evolutionary process without assuming a strict
molecular clock. We used a Yule prior on branching rates
because our analysis deals with a species-level phylogeny.
Additionally, one prior was specified in the form of a
calibration point as the time of the most recent common
ancestor (tMRCA) for Caviomorpha (28.5–37 million years
ago [mya]—Wyss et al. 1993). Four independent runs of 8
million generations were implemented, with the first 500,000
generations of each run discarded as burn-in. Posterior
probabilities (P) were used as an estimate of branch support.
The 95%highest posterior density intervals for the divergence
time estimates were obtained for each node.
RESULTS
Patterns and levels of variation.—Complete sequences
(1,140 base pairs) of cytochrome bfrom 84 individuals (71
tuco-tucos and 13 other Hystricognathi) were analyzed and
June 2011 PARADA ET AL.—DIVERSIFICATION OF TUCO-TUCOS 673
resulted in 597 (52.4%) variable sites, of which 490 were
potentially parsimony informative and 68.2%of the variable
changes were at third codon positions (Table 2). The
estimated transition/transversion rate ratios is k
1
53.19
(purines) and k
2
57.28 (pyrimidines). The transition/
transversion bias is R52.256.
The range of intraspecific divergence is 0.2–3.5%(C. haigi
and C. magellanicus, respectively), whereas the average (n5
14) is 1.5%. Two species pairs are the most divergent (12.8%),
C. sociabilisC. frater and C. sociabilisC. leucodon.C.
sociabilis is the most divergent species (11.0%on average)
from other tuco-tucos. The least divergent species pairs are
comparable with those of some intraspecific comparisons. For
example, C. saltarius and C. scagliai, and C. coyhaiquensis
and C. sericeus differ by only 0.6%(see also Table 3).
Higher-level relationships.—Topologies obtained from the
different methods are congruent, with the exception of
discrepancies at weakly supported relationships within species
groups. Therefore, only the ML topology is presented (lnL 5
215458.521279), with the branch support values obtained
from all three of the inference methods (Fig. 2). The
parsimony analysis produced 12 shortest trees of 3,447 steps
and a consistency index of 0.308 and a retention index of
0.568.
Ctenomys is monophyletic with strong support. The
dichotomy at the base of Ctenomys splits into C. sociabilis
and a clade of all other tuco-tucos, followed by subsequent
divergence of C. tuconax, but these relationships are poorly
supported. Within the remaining tuco-tuco clade, 8 relatively
well-supported species groups are recovered (Fig. 2). The
branching pattern and the relationships among these 8 clades
and several other poorly supported clades are unstable.
The opimus group (A) is a relatively well-supported clade
composed of the altiplano species (C. opimus and C. fulvus)
and 2 species from the nearby Argentinean Chaco and the
open highlands of Tucuman (C. saltarius and C. scagliai) that
are sister to each other but with low sequence divergence
(0.6%). C. opimus is recovered as paraphyletic relative to C.
fulvus but poorly supported. The recovered divergence within
the group is, on average, 3.94%, whereas C. opimus has the
most divergent intraspecific haplotypes (1.8%). C. maulinus, a
species of uncertain affinities in previous studies, is recovered
as sister to the opimus group under MP and ML, although
without strong support.
The mendocinus group (B), including C. australis,C.
mendocinus, and C. porteousi (sensu Massarini et al. 1991),
are closely allied with C. flamarioni and C. rionegrensis.
However, the 3 haplotypes recovered from specimens assigned
to C. mendocinus do not form a monophyletic group. One
haplotype from Tupungato, an Andean locality in Mendoza,
Argentina, is not sister to a clade formed by the other
haplotypes of C. mendocinus, including one recovered from a
specimen collected at the species type locality. The genetic
divergences among members of the group are, on average,
2.4%.
The talarum group (C), which was referred to as the C.
pundti complex by Tiranti et al. (2005), is formed by C. pundti
TABLE 2.—Composition bias (%) and parsimony informative sites
(PI) for the cytochrome bdata set analyzed.
Base Total
Codon position
123
T 30.5 27 41 24
C 25.8 21.6 25.2 30.7
A 31.4 30.5 20.3 43.3
G 12.3 20.8 13.7 2.5
PI 490.0 30.3 10.8 87.9
TABLE 3.—Divergence among pairs of species within species
groups of Ctenomys for uncorrected p distance shown as percentage.
opimus group
fulvus
1.6 opimus
5.4 5.5 scagliai
5.7 5.8 0.6 saltarius
mendocinus group
porteousi
1.2 australis
1.7 1.9 mendocinus
2.6 2.8 3.1 flamarioni
2.5 2.9 2.8 3.4 rionegrensis
talarum group
pundti
2.9 talarum
torquatus group
pearsoni
2.3 perrensi
3.1 1.9 roigi
4.4 3.7 4.3 torquatus
3.9 3.3 3.8 3.4 lami
3.9 3.4 4.0 3.5 1.3 minutus
magellanicus group
sericeus
4.8 colburni
3.5 5.4 haigi
0.7 4.8 3.4 coyhaiquensis
1.4 5.6 4.3 1.2 fodax
5.0 0.5 5.6 5.0 5.7 magellanicus
tucumanus group
latro
2.0 occultus
1.5 1.5 argentinus
6.9 7.1 6.8 tucumanus
boliviensis group
nattereri
2.2 robo
5.4 5.7 boliviensis
5.4 5.6 1.2 goodfellowi
6.9 6.5 6.2 6.6 steinbachi
frater group
lewisi
5.2 frater
8.2 9.1 conoveri
8.3 8.9 6.8 C. sp. (from
Llathu)
674 JOURNAL OF MAMMALOGY Vol. 92, No. 3
and C. talarum (node C) in a well-supported monophyletic
clade. However, C. talarum is paraphyletic in relation to C.
pundti. The intraspecific divergence among C. talarum ranges
from 0.4%to 2.1%. The C. talarum group is the sister taxon to
the C. mendocinus group.
The torquatus group (D) has C. torquatus (from Brazil and
Uruguay) as a poorly supported sister to the remaining species
of the group, which are grouped into 2 clades. One of them is
well supported and is formed by C. perrensi,C. roigi
(Argentina), and C. pearsoni (Uruguay). However, the 3
haplotypes of C. perrensi are not reciprocally monophyletic.
The other clade is poorly supported and formed by 2 Brazilian
species, C. lami and C. minutus.C. minutus is paraphyletic in
relation to C. lami, and specimens of C. minutus from Osorio
and C. lami from Chico Loma share a haplotype. Observed
divergence within the torquatus group was, on average, 2.0%.
The magellanicus group (E) is well supported and
composed entirely of Patagonian–Fueguian species (C.
coyhaiquensis,C. colburni,C. fodax,C. haigi,C. magellani-
cus, and C. sericeus). The other Patagonian–Fueguian species
(C. maulinus and C. sociabilis) are in divergent lineages. The
haplotype from a specimen collected at the type locality (El
Maiten, Chubut, Argentina) of C. haigi diverges substantially
(.3.5%) from a clade that is composed of species assigned to
C. haigi and samples from 2 additional localities in the
northern Patagonian steppe (Somuncura and Talagapa,
Chubut, Argentina). Haplotypes recovered from specimens
of an undescribed form collected at Pichin˜an and Quichaura
(Chubut, Argentina) form a well-supported clade that is sister
to the clade composed of C. fodax,C. coyhaiquensis, and C.
sericeus. A haplotype from the type locality of C. colburni
was closely related to the Fueguian C. magellanicus, and their
divergence is minimal (0.5%). The recovered divergence
within the group was, on average, 3.5%.
The tucumanus group (F) is relatively well supported and
formed by species of northern distribution, including C.
argentinus,C. occultus,C. latro, and C. tucumanus as
successively basal lineages. The most divergent species is C.
tucumanus (6.9%). Within the group, observed divergence
was, on average, 4.3%.
The boliviensis group (G) is a well-supported monophyletic
clade that includes species identified as the ‘‘Boliviano–
Matogrossense’’ group (C. boliviensis,C. goodfellowi, and C.
nattereri) by Contreras and Bidau (1999), and C. sp. from
Robore, Bolivia (Lessa and Cook 1998), with interspecific
genetic divergence averaging 4.8%.C. steinbachi is a poorly
supported sister to this group. In addition, 3 undetermined
Bolivian forms (‘‘ita,’’ ‘‘monte,’’ and ‘‘minut’’) form a clade
that might be sister to the boliviensis group.
The frater group (H) is well supported and includes a
Chaco and intermediate Andean elevation species, which was
referred to as the Bolivian–Paraguayan group by Contreras
and Bidau (1999). It includes C. frater,C. lewisi,C. conoveri,
and C. sp. (from Llathu) and is sister to the clade formed by
the other species groups and C. leucodon. The frater group
has the highest observed divergence among species (up to
7.7%), with an average of 3.94%. The highest genetic
distance among groups was found between species of the C.
frater and the C. tucumanus groups (11.3%), with an average
distance of 7.6%.
Estimates of divergence dates have broad confidence
intervals (Fig. 3, Table 4). The tMRCA of Ctenomys was
dated at 9.22 (6.4–12.6) mya. Most of the tMRCA for species
groups were dated around 3 mya, and species groups from the
eastern distribution of the genus were of more recent origin.
DISCUSSION
Ctenomys is the most diverse genus of hystricognath
rodents, but our current understanding of this diversity, both
in terms of its alpha taxonomy and phylogenetic relationships,
is inadequate. The present study, based on mtDNA sequences,
has the broadest taxonomic and geographic coverage to date.
We focus mainly on relationships among species, although
some comments on species limits also are discussed.
Previous molecular phylogenetic studies (Castillo et al.
2005; Cook and Lessa 1998 D’Elı
´a et al. 1999; Lessa and
Cook 1998) found a polytomy at the base of the tuco-tucos
clade, possibly reflecting the rapid, early diversification of the
genus or saturation and loss of phylogenetic signal in the
cytochrome-bgene. In our study the node at the base of
Ctenomys leads to 2 lineages, C. sociabilis and a clade
forming the remaining tuco-tucos. The sequence provided by
Lara et al. (1996), and subsequently used by Lessa and Cook
(1998), does not correspond to C. sociabilis, but probably to C.
haigi. The identification of C. sociabilis, a social species
whose behavioral ecology has been studied intensively (Lacey
et al. 1997; Lacey and Wieczorek 2003), as sister to the
remaining species of the genus was well supported by only MP
bootstrapping. Therefore, this topology should be tested
further by the analysis of nuclear DNA sequences due to the
direct implications it has toward the understanding of the
biogeographic history of the genus. For example, C. sociabilis
is an austral species inhabiting the Argentinean province of
Neuqeuen in northern Patagonia, and the oldest known fossil
record assigned to Ctenomys,C. uquiensis, comes from Late
Pliocene sediments of the northwestern Argentinean province of
Jujuy (Verzi et al. 2010). This information needs to be integrated
into a historical biogeographic hypothesis for Ctenomys.
The phylogeny has most species of Ctenomys in 8 relatively
well-supported species groups. We did not associate names on
the basis of their geographic distribution as done by Contreras
and Bidau (1999). Instead, we refer to them using the names of
the oldest species in each group. Eight main species groups
were identified: boliviensis,frater,mendocinus,opimus,
talarum,magellanicus,torquatus, and tucumanus. The
magellanicus and torquatus groups are newly proposed in
this study, although the torquatus group was not well
supported. The other species groups were previously indenti-
fied, with some modifications, in earlier analyses.
Relationships among species groups are poorly supported,
with the exception of the mendocinus and talarum groups,
June 2011 PARADA ET AL.—DIVERSIFICATION OF TUCO-TUCOS 675
676 JOURNAL OF MAMMALOGY Vol. 92, No. 3
which are sister. The torquatus group is a poorly supported
sister to this clade, and these 3 species groups comprise the
eastern distribution of the genus. More effort is needed,
however, to clarify the position of the undetermined forms
referred to as ita, monte, and minut, which are recovered as a
poorly supported clade, phylogenetically close to the boliv-
iensis group.
The close relationship of C. mendocinus,C. porteousi,C.
australis, and C. azarae (not included here), originally
referred to as the mendocinus group, has been noted since
their karyotypes were first described (Massarini et al. 1991).
Subsequent explicit phylogenetic efforts (D’Elı
´a et al. 1999)
corroborated the grouping of these species and suggested that
C. flamarioni and C. rionegrensis are also part of it. Our
FIG.3.—Bayesian tree with divergence dates from the relaxed uncorrelated lognormal clock analysis. The bars represent the 95%highest
posterior density (HPD) interval for the divergence time estimates. Numbers indicate million years before present.
r
FIG.2.The phylogenetic tree resulting from maximum-likelihood analysis of cytochrome-bgene sequences recovered from 71 specimens of
Ctenomys. Haplotype labels follow specimen labels, as presented in Appendix I. Letters designate species groups as referred to in the text.
Numbers indicate support from parsimony jackknife (%), relative Bremer support, likelihood bootstrap (%), and posterior probability (J/Bs/B/P).
A node without numbers implies that the node has ,60%of J and B and/or ,0.7 P. * is a shared haplotype with C. lami from Chico Loma.
June 2011 PARADA ET AL.—DIVERSIFICATION OF TUCO-TUCOS 677
analysis corroborates this grouping, which inhabits lowlands
and mountainous regions across different ecoregions in the
center of the distributional range of the genus. As noted by
Massarini et al. (1991), the mendocinus group has a
conservative diploid number (2n 547–48) and morphology
for the genus. However, the limited genetic divergence that is
found among C. australis,C. porteousi, and C. mendocinus
needs further taxonomic assessment. In addition, the phylo-
genetic position of the haplotype recovered from a specimen
collected at Tupungato and currently assigned to C. mendo-
cinus indicates that it might represent a species distinct from
C. mendocinus. Furthermore, some nominal forms (e.g., C.
pontifex and C. coludo) that might belong to this group have
not been included in any phylogenetic study.
Ctenomys fulvus and C. opimus might be considered as
conspecific because of their high sequence (Lessa and Cook
1998) and chromosomal (Gallardo 1991) similarity. We
expand the opimus group to include C. saltarius and C.
scagliai, which has only 0.6%sequence divergence. In the
case of the ML and MP trees, C. maulinus is a poorly
supported sister species to the opimus group, whereas in the
Bayesian tree it is sister to the clade formed by the C.
mendocinus,C. talarum, and C. torquatus groups.
Mascheretti et al. (2000) identified a group of Chacoan
species formed by C. argentinus,C. latro,C. occultus, and C.
pilarensis, which with C. tucumanus form our tucumanus
group. C. opimus and C. scagliai were grouped under the
Chaco group by Contreras and Bidau (1999), but these 2
species are recovered in our study as part of the opimus group.
To investigate further the relationships of the species from
northern Argentina a broader phylogeographic analysis
including more representatives is needed.
Ctenomys talarum and C. pundti form a species group,
which Tiranti et al. (2005) identified as the C. pundti complex.
However, we refer to it as the talarum group because this is an
older name than pundti. In addition, haplotypes of C. talarum
form a paraphyletic group with respect to those of C. pundti,
casting doubts on the taxonomic status of both taxa. As is the
case with most taxa of Ctenomys, species limits within this
group need to be evaluated further with the integration of more
specimens, morphological characters, and nuclear DNA
sequences.
The topology recovered within the C. torquatus group
indicates the need for further assessment of the taxonomic
status of C. perrensi,C. pearsoni, and C. roigi. Each of these
nominal species has impressive chromosomal variation
(Ortells and Barrantes 1994), but some of these species are
not monophyletic. Similarly, pairwise distances between C.
minutus and C. lami (0.4–2.7%) indicate low divergence
among some haplotypes, and an analysis of cranial morphol-
ogy did not find any substantial difference between them
(Freitas 2005). Although the torquatus group lacks strong
support, it was recovered by all methods. In addition, previous
studies (Freitas 2005; Lessa and Langguth 1983) have
commented on the morphological similarities among members
of this group.
The magellanicus group comprises species from the
Patagonian–Fueguian open areas and represents the only extant
group to range into the southern end of South America. All
individuals collected on the mainland south of the Senger River
(,54uS), including those labeled as sp. 1, sp. 2, sp. 3, C.
sericeus,C. coyhaiquensis, and C. fodax, might represent a
single biological species, given the low observed genetic
distances among the haplotypes examined. Similarly, the
genetic distance between the haplotypes of C. colburni and C.
magellanicus is minimal. In addition, C. haigi was not
recovered as monophyletic, and the specimen labeled as haigi
3 is a topotype of C. haigi. The specimens labeled as haigi 1,
haigi 2, sp. 6, and sp. 7 form a subclade within the magellanicus
group. Whether the entire subclade represents 1 or more species
is unclear. Several named forms of Patagonian taxa not included
here (e.g., C. emilianus,C. magellanicus osgoodi) would have
to be considered in future analyses.
Asymmetric sperm morphotype is found in southern species
(mendocinus group, magellanicus group, C. maulinus, and C.
sociabilis), which do not form a monophyletic group. This
supports the suggestion of D’Elı
´a et al. (1999) and Slamovits
et al. (2001) that the asymmetric morph appeared more than
once in the evolutionary history of Ctenomys. The uncertain
position of C. maulinus, a species with the asymmetric sperm,
and the lack of sequence data for C. yolandae, which has a
third sperm morphology (Vitullo et al. 1988), hinders the
recovery of the evolutionary history of this variable trait.
Similarly, additional work is needed to understand the
chromosomal evolution of the genus and the general pattern
of diversification.
Divergence time estimates for the splitting of the lineages
leading to the families Ctenomyidae and Octodontidae and
TABLE 4.—Estimates of divergence times recovered as mean
estimates between different caviomorph lineages. Each value
represents the estimated divergence time (mya) and 95%confidence
interval. As in the text, Ctenomys species groups are referred to by the
specific term.
Lineage Divergence time
tMRCA Caviomorpha 32.03 (28.6–37.2)
tMRCA Cavioidea 21.89 (14.6–29.5)
(Ctenomys+Octodontidae/
Echimyidae) +Erethizontoidea 28.98 (23.4–34.5)
Ctenomys+Octodontidae/Echimyidae 23.18 (18.2–28.6)
Ctenomys+Octodontidae 17.97 (13.5–23.0)
tMRCA Octodontidae 12.34 (8.4–16.7)
tMRCA Ctenomys 9.22 (6.4–12.6)
All Ctenomys minus sociabilis 7.74 (5.7–10.2)
frater 4.97 (3.3–7.0)
All spp. groups minus frater 5.02 (3.7–6.7)
boliviensis 3.77 (2.6–5.1)
tucumanus 3.44 (2.4–4.8)
magellanicus 3.30 (2.6–4.6)
opimus 3.29 (2.1–4.8)
torquatus 2.46 (1.6–3.4)
talarum 1.44 (0.9–2.1)
mendocinus 1.85 (1.2–2.7)
talarum/mendocinus 2.78 (1.9–3.9)
678 JOURNAL OF MAMMALOGY Vol. 92, No. 3
that of the tMRCA of Octodontidae (estimated around 17.97
and 12.34 mya, respectively) are older than previous estimates
on the basis of 12S rRNA and growth hormone receptor
sequences (Opazo 2005). Similarly, the tMRCA of Ctenomys
was estimated at 9.22 mya, a value much older than previous
estimates (3.7 mya—Castillo et al. 2005) or the evidence from
the fossil record, which suggests that the split between
Ctenomyidae and Octodontidae occurred not more than 9 mya
(Verzi 2002). It should be taken into account that our analysis
differs from previous ones on methods and sampling. More
recently, Verzi et al. (2010) reported and described the oldest
known tuco-tuco species, implying a minimum age for the
genus of about 3.5 million years. Verzi et al. (2010)
considered that the uncertainty of the age of Praectenomys
(which is regarded as sister to Ctenomys) hampers a more
definitive estimation of a maximum age for Ctenomys. Our
estimations are based on a single locus, with large confidence
intervals associated with them (Table 4).
The northern species groups occurring in Argentina and
Bolivia (boliviensis,frater,tucumanus, and opimus) and the
southern magellanicus group seem to be older (,3.5 million
years) than those inhabiting central Argentina, eastern Brazil,
and Uruguay, such as the talarum and torquatus groups that
diverged around 2.0 mya. The inclusion of taxa missing in our
analysis could change this date, and these estimates refer only
to living members of species groups.
Our results are similar to those found by Cook and Lessa
(1998) in identifying an increase in the diversification rate at
the base of the tuco-tucos clade. After the basal split our
results suggested an increase in diversification ,3 mya after
some main lineages already had diverged. The cause of this
diversification pulse remains obscure. The inclusion of more
representatives of Caviomorpha and more calibration points
and loci would provide a better understanding of the timing of
the radiation.
Some nominal species appear to be polyphyletic or bear
little or no divergence from other named species; however, we
are not proposing formally any taxonomic change because our
analysis is based solely on 1 gene and lacks specimens from
several type localities. We concur with Freitas (2005) for the
need for further integration of molecular and morphological
analyses, including the study of type and topotype specimens
to propose a classification scheme that better reflects
phylogeny. Until these issues are addressed the distinctiveness
of several taxonomic forms and the species diversity will
remain elusive.
The lack of monophyly for several forms could reflect a
disagreement between the inferred gene tree and the species
tree because of random fixation of alternative ancestral
haplotypes via incomplete lineage sorting (Neigel and Avise
1986). In addition, potential discrepancies could be caused by
mtDNA introgression (Patton and Smith 1994). Despite these
limitations, species groups could be identified using mtDNA
sequences, and these were similar to groups identified by
nuclear intron data (Castillo et al. 2005), morphology, or
chromosomes (Contreras and Bidau 1999). However, a need
exists for multilocus analyses to build on the previous studies
by Castillo et al. (2005) and Galewski et al. (2005) that used
loci in the closely related Echimyidae, including nuclear
RAG-1 (Patterson and Velazco 2008), for a better understand-
ing of phylogenetic relationships within Ctenomys.
RESUMEN
Presentamos aquı
´el estudio ma´s exhaustivo hasta la fecha
de los grupos de especies en Ctenomys (tuco-tucos), un ge´nero
de roedores Neotropicales conocido por su riqueza especı
´fica.
Para explorar las relaciones filogene´ticas de 38 especies y 12
formas indeterminadas, se secuencio´ el citocromo b completo
de 34 especı
´menes y se incorporaron 50 secuencias pre-
viamente publicadas. Se tuvieron en cuenta ana´lisis por
Parsimonia, Verosimilitud y Bayesianos empleando histro-
cognatos como grupo externo. La dicotomı
´ama´s basal lleva a
C. sociabilis por una parte y al resto de los tuco-tucos por otra.
Dentro de los tuco-tucos, se identifican 8 grupos de especies:
boliviensis,frater,mendocinus,opimus,talarum,magellani-
cus,torquatus ytucumanus. Mientras que la mayorı
´a de los
grupos aluden a clados identificados mediante estudios de
cromosomas o morfologı
´a el grupo torquatus ymagellanicus
son hipo´ tesis taxono´micas nuevas. Las relaciones basales entre
los grupos de especies se encuentran con poco apoyo. La
posicio´n de C. leucodon,C. maulinus yC. tuconax son
conflictivas o irresueltas y estas podrı
´an representar linajes
independientes. Adicionalmente, de acuerdo a nuestros
estimados, los grupos de especies se habrı
´an originado hace
alrededor de 3 millones de an˜os.
ACKNOWLEDGMENTS
We are grateful for the tissue samples kindly provided by Agustina
Ojeda, Eileen Lacey, Gabriela Fernandez, Matı
´as Mora, Richard
Sage, Sergio Vinco´n, Thales R. O. Freitas, and Ulyses Pardin˜ as.
Financial support was given by National Geographic Society 7813-
05, Comisio´n Sectorial Investigacio´ n Cientı
´fica-Universidad de la
Repu´blica, Programa de Desarrollo de las Ciencias Ba´ sicas, and
Fondo Nacional de Desarrollo Cientı
´fico y Tecnolo´gico 11070157.
Last, we thank B. Lim and 2 anonymous reviewers for their
comments and suggestions on previous versions.
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APPENDIX I
List of the specimens of Ctenomys used in the present study.
Accession numbers are indicated for those specimens whose
sequences were retrieved from GenBank. See Fig. 1 for locality
numbers and locations of sites. Museum and collection acronyms and
personal field numbers are as follows: Argentina, Universidad de Mar
del Plata (Matı
´as Mora, IF); Instituto Argentino de Investigaciones de
Zonas A
´ridas, Mendoza (Agustina Ojeda, AO); Centro Nacional
Patago´nico, Puerto Madryn (Proyecto National Geographic, PNG and
Proyecto Localidades Tı
´picas–Ulyses Pardin˜as, LTU); Universidad
Nacional de Patagonia, Esquel (Sergio Vinco´n, SV); Brazil, Instituo
Oswaldo Cruz, Rı
´o de Janeiro (Claudio J. Bidau, CB); Universidad
Federal Rı
´o Grande do Sul, Porto Alegre (Thales R.O. Freitas, TJ,
CML and TR); and USA, Museum of Vertebrate Zoology, University
California, Berkeley (Eileen Lacey, EAL).
Voucher numbers for new sequences are given after the accession
number in parentheses.
Ctenomys argentinus.—Colonia Benitez, Argentina, 22 (AF370680).
Ctenomys australis.—Necochea, Argentina, 46 (AF370697, topo-
type).
Ctenomys boliviensis.—Las Lomitas, Bolivia, 4 (AF007038,
topotype).
Ctenomys colburni.—
´o Ecker, 47u079S, 70u519W, Santa Cruz,
Argentina, 58 (HM777474/LTU191, topotype).
Ctenomys conoveri.—Carandayti, Bolivia, 9 (AF007055).
Ctenomys coyhaiquensis.—Chile Chico, Chile, 57 (AF119112,
topotype).
Ctenomys flamarioni.—Taim, Brazil 32 (AF119107, topotype).
Ctenomys fodax.—Lago Blanco, 45u559S, 71u189W, Chubut,
Argentina, 56 (HM777475/sv52, topotype).
Ctenomys frater.—Rancho Tambo Bolivia, 11 (AF007045).
Ctenomys fulvus.—fulvus1, San Pedro de Atacama, Chile, 13
(A0F370688, topotype); fulvus2, Turi, Chile, 12 (AF370687).
Ctenomys goodfellowi.—goodfellowi1, goodfellowi2, San Ramon
Bolivia, 7 (AF007050-51).
Ctenomys haigi.—haigi1, Nahuel Huapi, Argentina 49 (AF422920);
haigi2, Bariloche, Argentina 50 (AF007063); haigi3Maiten,42u39S,
71u109W Chubut, Argentina 51 (HM777476/sv62, topotype).
Ctenomys lami.—Beco dos Cegos, 30u519S, 51u109W, Rio Grande
do Sul, Brazil, 31 (HM777477/TJ186, topotype).
Ctenomys latro.—latro1, latro2, Tapia, 26u369S, 65u159W, Tucu-
ma´n, Argentina, 17 (HM777478/CB286 or C-04679, AF370704,
topotype).
Ctenomys leucodon.—San Andres de Machaca, Bolivia, 1
(AF007056, topotype).
Ctenomys lewisi.—Iscayachi, Bolivia, 10 (AF007049).
Ctenomys magellanicus.—magellanicus1, Estancia Sara, 56u269S,
68u119W, Tierra del Fuego, Argentina, 64 (HM777479/PNG365);
magellanicus2, Tres Arroyos, Tierra del Fuego, Chile, 63 (AF370690).
Ctenomys maulinus.—maulinus1, Pelechue, Chile 42 (AF370703);
maulinus2, Rio Colorado, Chile 47 (AF370702).
June 2011 PARADA ET AL.—DIVERSIFICATION OF TUCO-TUCOS 681
Ctenomys mendocinus.—mendocinus1, Cerro de la Gloria,
32u529S, 68u489W, Mendoza, Argentina 36 (HM777480/AO59,
topotype); mendocinus2, Las Heras, Argentina 35 (AF007062);
mendocinus3, Tupungato, Argentina 37 (AF370695).
Ctenomys minutus.—minutus1, Praia do Barco 29u409S, 48u589W,
Brazil, 29 (HM777481/CML431); minutus2, Jaguaruna 28u379S,
49u019W Rio Grande do Sul, Brazil, 28 (HM777482/TR40); minutus3
Osorio, 29u529S, 50u129W,RioGrandedoSul,Brazil30
(HM777483/TR02).
Ctenomys nattereri.—Santa Cruz de la Sierra, 17u369S, 63u049,
Santa Cruz, Bolivia 4 (HM777484/CB3968 or C-03968).
Ctenomys occultus.—Simoca, 27u159S, 65u219W, Tucuma´n, Ar-
gentina 21 (HM777485/CB291 or C-04685).
Ctenomys opimus.—opimus1, Huancaroma Bolivia 2 (AF007042);
opimus2, Tres Cruces Argentina, 14 (AF370700).
Ctenomys pearsoni.—pearsoni1 El Potrerillo Uruguay 34
(AF119108); pearsoni2 Limetas, 34u119S, 58u69, Colonia, Uruguay
41 ( HM777486/EV1454, topotype).
Ctenomys perrensi.—perrensi1, Chavarrı
´a, 28u579S, 58u349W,
Corrientes, Argentina 27 (HM777487/CB349 or C-04822); perrensi2,
San Miguel, 27u599S, 57u359W, Corrientes, Argentina 25
(HM777488/CB554 or C-05503); perrensi3, Mburucuya´, 28u029S,
58u139W, Corrientes, Argentina 24 (HM777489/CB778 or C-05142).
Ctenomys porteousi.—Bonifacio 36u489S, 62u139W, Buenos Aires,
Argentina 44 (AF370682, topotype).
Ctenomys pundti.—pundti1, Puente Olmos, 32u289S, 63u199W,
Co´rdoba, Argentina 39 (HM777490/CB589 or C-03755); pundti2
Manantiales, 29u529S, 63u549W, Co´rdoba, Argentina 38 (HM777491/
CB592 or C-04042).
Ctenomys rionegrensis.—Las Can˜ as, Uruguay 40 (AF119103,
topotype).
Ctenomys roigi.—Empedrado, 27u569S, 58u459W, Corrientes,
Argentina 23 (M777492/CB198, topotype).
Ctenomys saltarius.—Tolombo´n, 26u119S, 65u569W, Salta, Argen-
tina 15 (HM777493/CB295 or C-04689).
Ctenomys scagliai.—Tafı
´del Valle, 26u269S, 65u579W, Tucuma´n,
Argentina 20 (HM777494/CB299 or C-04696, topotype).
Ctenomys sericeus.—La Porten˜a, Rio Lista, 48u029S, 71u569W,
Santa Cruz, Argentina 61 (HM777496/sv45, topotype).
Ctenomys sociabilis.—Nahuel Huapi, 41u069S, 71u189W, Neuque´n,
Argentina 48 (HM777495/EAL 545, topotype).
Ctenomys steinbachi.—Buen Retiro, Bolivia 5 (AF007044).
Ctenomys talarum.—talarum1, El Guanaco, 36u329S, 66u269W,
Buenos Aires, Argentina 43 (HM777497/315 or C-04773); talarum2
and talarum4, Necochea 38u339S, 58u449W, Buenos Aires, Argentina
46 (AF370698-9, topotype); talarum3 Saladillo, 35u389S, 59u469W,
Buenos Aires, Argentina 45 (HM777498/IF1).
Ctenomys torquatus.—torquatus1, Ipora, Uruguay 33 (AF119111);
torquatus2, Alegrete, Brazil 26 (EF372282).
Ctenomys tuconax.—El Infiernillo, Argentina 18 (AF370684).
Ctenomys tucumanus.—tucumanus1, Ticucho, Argentina 16
(AF370691); tucumanus2 San Miguel de Tucuma´n, 26u239S, 64u419W,
Tucuma´n, Argentina 19 (HM777499/CB277 or C-04670, topotype).
Ctenomys sp.—sp1, Cerro Ventana, 42u019S, 69u569W, Chubut,
Argentina 62 (HM777500/PNG803); sp2, La Paloma, 47u399S,
67u469W, Santa Cruz, Argentina, 59 (HM777501/LTU207); sp3,
Cerro del Paso, 47u549S, 66u239W, Santa Cruz, Argentina 60
(HM777502/PNG1614); sp4, Pichin˜an, 43u339S, 69u049W, Chubut,
Argentina 55 (HM777503/PNG1201); sp5, Quichaura, 43u339S
70u289W, Chubut, Argentina 54 (HM777504/PNG336); sp6, Tala-
gapa, 42u139S, 68u169W, Chubut, Argentina 52 (HM777505/
PNG191); sp7, Somuncura, 41u269S, 67u189W, Rı
´o Negro, Argentina
53 (HM777506/PNG160).
Ctenomys sp. ITA.—ITA, Cerro Itahuaticua Tarija, Bolivia, 11
(AF007047).
Ctenomys sp. LLATHU.—LLATHU, Cochabamba, Bolivia, 3
(AF007048).
Ctenomys sp. MONTE.—MONTE, Monteagudo, Bolivia 8
(AF007053).
Ctenomys sp. MINUT.—MINUT, W of Robore, Bolivia 6
(AF007052).
Ctenomys sp.—ROBO, Robore, Bolivia 6 (AF007039).
Capromys.—AF422915, Cavia.—AY382791, Coendou.—
AF411584, Dactylomys.—L23335, Echimys.—L23341, Myo-
procta.—AF437781, Octodon.—AF007058, Octodontomys.—
AF370706, Proechimys.—AJ251403, Trinomys.—AF422923, Tym-
panoctomys.—AF007060, Bathyergus, AY425911, Thryonomys.—
NC002658.
682 JOURNAL OF MAMMALOGY Vol. 92, No. 3
... The Cytb sequences generated in this study (GenBank: OL311956-OL311960) were compared with other Cytb sequences of Ctenomys obtained from GenBank (Supplementary Table 1), including sequences of C. famosus, as well as for all species of Ctenomys in the "boliviensis", "frater", "magellanicus", "mendocinus", "opimus", "talarum", "torquatus", and "tucumanus" lineages (sensu Parada et al. 2011). Sequences (n = 3) for members of the family Octodontidae were used as outgroups (Supplementary Table 1). ...
... Cacti are not abundant on this sandy areas, but some individuals of Cereus sp., Trichocereus sp., and Tephrocactus can be found (Cabido et al. 2018;Morello et al. 2012). The molecular analyses of Cytb haplotypes indicated a close association between the clades of Ctenomys from Sierra de Famatina and Sierra de Velasco, with relatively low sequence divergence (1.26%) comparable to the divergence observed within other species of Ctenomys (Gardner et al. 2014;Londoño-Gaviria et al. 2019;Parada et al. 2011). The sequence divergence was even similar to that reported for the intrapopulation-level among Potrerillo and San Blas specimens (i.e., Famatina clade) of C. famosus (0.5-1.2%; . ...
... (Londoño-Gaviria et al. 2019;Parada et al. 2011). ...
Article
The Ctenomys population from Anillaco, La Rioja Province, Argentina has been the subject of detailed studies of circadian rhythms, vocalization, ecology and spatial dynamics. However, the taxonomy and systematics of this population as well as populations of Ctenomys inhabiting Andean areas of this province is unknown. In this study, we present the phylogenetic relationship of the "Anillaco tuco-tuco" as well as of two other populations of Ctenomys, all distributed in the northern portion of La Rioja Province, Argentina. Based on molecular analyses and morphological comparisons, we reached to the conclusion that the "Anillaco tuco-tuco" population corresponds to the species Ctenomys famosus. In addition, an undescribed species, member of the "mendocinus" lineage of Ctenomys, is recognized in the Andean portions of the province.
... The genus Ctenomys (Rodentia, Hystricomorpha) is well represented in arid and semiarid regions of southern Patagonia by the polytypic "magellanicus" lineage (Bidau 2015;Parada et al. 2011). Members of this clade have been reported from 42 • S in northeastern Patagonia to 54 • S latitude in Tierra del Fuego, making this the only extant lineage of Ctenomys to occur at such extreme southern latitudes (Bidau 2015;Freitas 2016). ...
... Members of this clade have been reported from 42 • S in northeastern Patagonia to 54 • S latitude in Tierra del Fuego, making this the only extant lineage of Ctenomys to occur at such extreme southern latitudes (Bidau 2015;Freitas 2016). Systematic relationships within this lineage were first assessed by Parada et al. (2011), who recognized six species (C. colburni Allen, 1903;C. ...
... bidaui, C. contrerasi, and C. thalesi) and proposed that C. coyhaiquensis be synonymized with C. sericeus. In a separate analysis, suggested that C. colburni should be synonymized with C. magellanicus and indicated that the clade containing specimens assigned to C. haigi should be revised (see also Parada et al. 2011;. ...
Article
The South American rodent genus Ctenomys is well represented throughout much of southern Patagonia by the polytypic “magellanicus” lineage. In western Argentina, members of this lineage occur from 35 °S to 54 °S latitude. In comparison, the taxonomy of Ctenomys in northeastern Patagonia remains poorly known. This ∼160,000 km² region consists primarily of mostly flat, homogenous tracts of austral Monte desert covering a gravel substrate and is cut by two major fluvial systems associated with the Colorado and the Negro rivers. Here, we use mitochondrial sequences and morphological comparisons to describe phylogenetic relationships among recently sampled populations of Ctenomys from this region. These analyses indicate that the “magellanicus” lineage extends into northeastern Patagonia to at least the Negro river (40°S). Contained within this lineage are three latitudinally distinct clades that are separated by geographic features such as rivers and basaltic plateaus. Identification of these clades generates new insights into the phylogeographic history of the “magellanicus” lineage and marks the end to nearly a century of stasis regarding taxonomic studies of Ctenomys from northeastern Patagonia.
... opimus and C. fulvus) as well as two species (C. saltarius and C. scagliai) from adjacent, lower-elevation chaco habitats (Parada et al. 2011). Contained within this clade is the population of C. opimus at Monumento Nacional Laguna de los Pozuelos, Jujuy Province, Argentina (hereafter referred to as Pozuelos), that has been shown to be group living (O'Brien et al. 2020). ...
... All sequences generated as part of this study were deposited in GenBank (MZ540021-MZ540026). To include the other species in the opimus clade in our analyses and to place sequences from Antofagasta and Pozuelos into a larger phylogenetic context, we used GenBank to obtain cyt-b sequences for an additional 21 specimens of Ctenomys chosen to represent the range of currently recognized subclades within this genus (Parada et al. 2011). Also obtained were cyt-b sequences for two species (Tympanoctomys barrerae, Octodon degus) from the sister family Octodontidae that served as outgroups. ...
... Behavioral variation within the opimus clade.-Currently, the opimus species group of tuco-tucos contains four named forms (Parada et al. 2011;Bidau 2015). No data regarding social organization are available for C. saltarius or C. scagliai, each of which is known from only a few locations in Salta and Tucuman Provinces in northwestern Argentina (Bidau 2015). ...
Article
Full-text available
Comparative studies of closely related species provide a powerful means of identifying the ecological and demographic factors associated with variation in mammalian social systems. Although most members of the subterranean rodent genus Ctenomys are thought to be solitary, the highland tuco-tuco (C. opimus) is group living, meaning that multiple adults share a burrow system and underground nest site. These animals are part of the opimus clade, a monophyletic collection of four named species that occur in northwestern Argentina and adjacent portions of Chile and Bolivia. As a first step toward generating a comparative assessment of social organization within this clade, we characterized spatial relationships among members of a population of Ctenomys at Antofagasta de la Sierra, Catamarca Province, Argentina. Based on geographic location and natural history, these animals were expected to be part of the opimus clade; analyses of mitochondrial cytochrome-b sequences from our study population confirmed this general phylogenetic placement. Radiotelemetry data indicated that the animals at Antofagasta were group living, with up to three adult females and one adult male sharing a burrow system. In contrast to other group-living ctenomyids, however, individuals did not consistently share nest sites. Comparisons of these data with re-analyses of spatial relationships among members of the population of C. opimus studied by O’Brien et al. (2020) revealed several intriguing differences in social organization, potential explanations for which include short-term responses to variable demographic and ecological conditions as well as more enduring responses to differences in local selective pressures. Further comparative analyses of these populations and, more generally, members of this subclade of Ctenomys will help to elucidate the factors contributing to variation in social behavior within this speciose and geographically widespread genus.
... These animals have been referred to as C. haigi, C. maulinus, and C. mendocinus, as well as various combinations of these names (Thomas 1918(Thomas , 1927aThomas and Saint Leger 1926;Yepes 1935;Sage et al. 1986;Tiranti 1996;Pardiñas et al. 2008). This diversity suggests a potentially complex distribution of species in this region, in which the southern "magellanicus" and more northern "mendocinus" lineages (sensu Parada et al. 2011) may come into contact. The latter is characterized by a complex pattern of morphological and genetic differentiation of populations within Mendoza (Rosi et al. 1992(Rosi et al. , 2002Mapelli et al. 2017), suggesting potentially substantial variation among closely related forms for which species boundaries remain undetermined. ...
... This is consistent with the taxonomic hypothesis proposed by Pearson (1984), who concluded that the pelage color of western Andean populations of C. maulinus more closely matches C. m. maulinus (see also Pearson and Christie 1985). This assignation is supported by our molecular analyses, which indicate that the "maulinus" group is composed of two well-supported sister clades that differ by 1.75% sequence divergence, which is only slightly greater than the mean intraspecific divergence (1.5%) suggested for the genus (Parada et al. 2011). One of these clades includes a sequence downloaded from GenBank (AF370702) that corresponds to a topotype of brunneus from Río Colorado, Malleco Province, Chile (Slamovits et al. 2001). ...
... To the best of our knowledge, there is no previous taxonomic reference to this form in the literature. Both our phylogenetic trees and our estimates of genetic distances strongly suggest that Cytb haplotypes in the central clade form a monophyletic group that appears to be associated with the "mendocinus" lineage (sensu Parada et al. 2011). Higher-level relationships among several species within this lineage remain unresolved (see below), possibly due to their recent divergence times (Parada et al. 2011(Parada et al. , 2012Mapelli et al. 2017;Sánchez et al. 2019;Leipnitz et al. 2020). ...
Article
Full-text available
In the Andean portion of northern Patagonia, populations of Ctenomys are found from low-elevation plains to high-elevation meadows and valleys. Despite their prevalence, the taxonomy of these subterranean rodents remains poorly resolved. Using genetic and morphological data obtained from museum specimens and animals collected in the field, we examined the taxonomy of Ctenomys from southwestern Mendoza Province, Argentina. Our analyses suggest the presence of at least five species of Ctenomys within the study area. The highest, innermost portion of the Andes is occupied by C. maulinus. To the east, the mountains and foothills are inhabited by two forms associated with the “mendocinus” and the “magellanicus” lineages, respectively. The former appears to be a local variant of C. emilianus, while the latter is sister to C. pontifex. Although C. pontifex was not encountered during our field sampling, it remains a valid species that likely is restricted to the isolated Valle Hermoso in westernmost Mendoza Province. In addition, we report an undescribed form from Las Leñas Valley that is associated with the “mendocinus” lineage. This complex alpha taxonomic scenario occurs within less than one degree of latitude, thereby highlighting the need to conduct detailed field collections to improve our knowledge of the systematics of Ctenomys.
... In conclusion, C. talarum and C. pundti complex might INTRODUCTION Subterranean rodents of the genus Ctenomys (Ctenomyidae: Caviomorpha; Blainville, 1826) are the most diverse in number of species of all native South American rodents, with about 68 recognized species (Bidau, 2015;Freitas, 2016;D'Elía et al., 2021). However, about 85 names have been assigned to biological entities of this genus and many taxa need to be properly delimited both geographically and systematically (Woods and Kilpatrick, 2005;Parada et al., 2011;Mapelli et al., 2017;Caraballo et al., 2020). In this context, the alpha taxonomy of Ctenomys has been intensively revised in the last decade, and new potential species are recurrently recognized (e.g., Parada et al., 2011;Caraballo and Rossi, 2017;Mapelli et al., 2017; and described (e.g., Freitas et al., 2012;Gardner et al., 2014;De Santi et al., 2021). ...
... However, about 85 names have been assigned to biological entities of this genus and many taxa need to be properly delimited both geographically and systematically (Woods and Kilpatrick, 2005;Parada et al., 2011;Mapelli et al., 2017;Caraballo et al., 2020). In this context, the alpha taxonomy of Ctenomys has been intensively revised in the last decade, and new potential species are recurrently recognized (e.g., Parada et al., 2011;Caraballo and Rossi, 2017;Mapelli et al., 2017; and described (e.g., Freitas et al., 2012;Gardner et al., 2014;De Santi et al., 2021). Furthermore, many of the original classifications of species available in the literature have not been consistent with the geographic and taxonomic limits observed from new molecular information (e.g., Mapelli et al., 2017;. ...
... Regarding the origin of the genus, the fossil record suggests that it was approximately 3.5-3.8 million years ago (mya) (Reguero et al., 2007;Verzi et al., 2010;De Santi et al., 2021). Molecular estimates of divergence times to the most recent common ancestor (tMRCA) of Ctenomys species indicates an older origin for this group, most probably precluding 9.2 mya (range: 6.4-12.6 mya; see Parada et al., 2011). However, it should be noted a recent study using fossil calibrations within Ctenomys place the origin of this genus in a more recent period in relation to that reported by other authors (1.32 mya; range: 0.8-2.1; ...
Article
Full-text available
With about 68 recognized living species, subterranean rodents of the genus Ctenomys are found in a multiplicity of habitats, from the dunes of the Atlantic coast to the Andes Mountains, including environments ranging from humid steppes of Pampas to the dry deserts of Chaco region. However, this genus needs an exhaustive reevaluation of its systematic and phylogenetic relationships regarding the different groups that compose it. This knowledge is essential to propose biodiversity conservation strategies both at species level and at higher hierarchical levels. In order to clarify the taxonomy and the recent evolutionary history from populations of Ctenomys in the Pampas region, Argentina, phylogenetic relationships among them were evaluated using mitochondrial DNA sequences: gene encoding cytochrome b protein (1,140 bp) and the non-coding D-loop region (434 bp). To infer the divergence times inside the Ctenomys clade, a Bayesian calibrate tree using fossil remains data from different families within Caviomorpha was performed at first. Secondly, that calibration data was used as priors in a new Bayesian phylogenetic inference within the genus Ctenomys . This phylogenetic tree emphasized on species currently distributed on the Pampas region, more precisely considering both the talarum and mendocinus groups. Bayesian inferences (BI) were integrated with the results of a Maximum Likelihood approach (ML). Based on these results, the distributional limits of the mendocinus and talarum groups appear to be related to the physiognomy of the Pampas region soils. On the other hand, the validity of C. pundti complex as a differentiated species of C. talarum is debated. According to previous evidence from morphological and chromosomal studies, these results show a very low divergence between those species that originally were classified within the talarum group. Mitochondrial DNA sequences from populations associated with these putative species have not recovered as reciprocal monophyletic groups in the phylogenetic analyses. In conclusion, C. talarum and C. pundti complex might be considered as the same biological species, or lineages going through a recent or incipient differentiation process. The results obtained in this study have important implications for conservation policies and practices, since both species are currently categorized as Vulnerable and Endangered, respectively.
... This unusual cladogenesis has been accompanied by their occupying a very wide diversity of environments through much of southern South America, within which each species is evolved to occupy a particular habitat (Reig et al. 1990;Bidau 2015;Freitas 2016). Hence, this radiation represents a promising model for studies of taxonomic and morphological evolutionary patterns and rates (Reig et al. 1990;Mora et al. 2003;Parada et al. 2011;Borges et al. 2017;Echeverr ıa et al. 2017;Morgan et al. 2017). ...
... A phylogenetic analysis using parsimony was performed to assess the relationships of the new Ctenomys species here in described, 50 living species representing all the recognized Ctenomys groups (Parada et al. 2011), and eight extinct species accepted as valid and represented by cranial and mandibular remains (Supplemental material, Appendix S1). The systematics of living species follows Bidau (2015), and . ...
... Likewise, we consider C. coyhaiquensis to be a junior synonym of C. sericeus and include it in phylogenetic analyses as C. sericeus from Chile Chico (Ays en, Chile). Finally, the attribution of some specimens from R ıo Senguer (Lago Blanco, Chubut, Argentina) to C. fodax (see Parada et al. 2011) has been questioned ; in any case, we maintain this name until this taxonomic issue is revised. ...
Article
Available at https://www.tandfonline.com/eprint/NHMCHA46SJECQUCPMWJF/full?target=10.1080/14772019.2021.1910583___Abstract: The South American Ctenomys is the most speciose genus among both hystricomorphs and subterranean rodents of the world. Here, we present the most exhaustive phylogenies and timetree of living and extinct Ctenomys attempted thus far. We describe Ctenomys rusconii sp. nov., a small-sized species from the upper Early Pleistocene of central Argentina. We analyse its cranial and mandibular shape as well as its phylogenetic position in the context of other extinct Ctenomys and a wide sample of living species. A parsimony analysis shows that Ctenomys rusconii sp. nov. integrates the stem group of Ctenomys together with late Pliocene to Middle Pleistocene species, while the crown group comprises only Middle Pleistocene to recent representatives. Within the crown Ctenomys, nine well-supported major clades were recovered, eight of which are consistent with previously recognized extant species groups. A Bayesian tip-dating analysis provided divergence age estimates of 3.8 Ma and 1.3 Ma for the origin of the genus and the crown clade, respectively. Remarkably, the extinct species recovered as members of the crown clade, i.e. C. dasseni, C. kraglievichi, C. subassentiens and C. viarapaensis, were clustered into the earliest diverging clade corresponding to the frater species group. Age estimates for the divergence of the crown and its major clades are markedly younger than what has been generally considered so far, which implies a new view on the timing of taxonomic, ecological and geographical diversification of the genus. Even considering that this interpretation is affected by biases inherent to the fossil record, the phylogenetic delimitation of the crown clade as restricted to species recorded since the Middle Pleistocene seems to configure a pattern underlain by a fast and late cladogenesis. http://zoobank.org/urn:lsid:zoobank.org:pub:14D8C3B2-CD37-4F30-84A2-14FDC20F1193
Article
Incomplete lineage sorting and introgression have been increasingly recognized as important processes involved in biological differentiation. Both incomplete lineage sorting and introgression result in incongruences between gene trees and species trees, consequently causing difficulties in phylogenetic reconstruction. This is particularly the case for rapid radiations, as short internodal distances and incomplete reproductive isolation increase the likelihood of both ILS and introgression. Estimation of the relative frequency of these processes requires assessments across many genomic regions. We use transcriptomics to test for introgression and estimate the frequency of incomplete lineage sorting in a set of three closely related and geographically adjacent South American tuco-tucos species (Ctenomys), a genus comprising 64 species resulting from recent, rapid radiation. After cleaning and filtering, 5764 orthologous genes strongly support paraphyly of C. pearsoni relative to C. brasiliensis (putatively represented by the population of Villa Serrana). In line with earlier phylogenetic work, the C. pearsoni - C. brasiliensis pair is closely related to C. torquatus, whereas C. rionegrensis is more distantly related to these three nominal species. Classical Patterson’s D-statistic shows significant signals of introgression from C. torquatus into C. brasiliensis. However, a 5-taxon test shows no significant results. Incomplete lineage sorting was estimated to have involved about 9% of the loci, suggesting it represents an important process in the incipient diversification of tuco-tucos.
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Photoperiodism plays an important role in the synchronization of seasonal phenomena in various organisms. In mammals, photoperiod encoding is mediated by differential entrainment of the circadian system. The limits of daily light entrainment and photoperiodic time measurement can be verified in organisms that inhabit extreme photic environments, such as the subterranean. In this experimental study, we evaluated entrainment of circadian wheel-running rhythms in South American subterranean rodents, the Anillaco tuco-tucos ( Ctenomys aff. knighti), exposed to different artificial photoperiods, from extremely long to extremely short photophases (LD 21:3, LD 18:6, LD 15:9, LD 9:15, LD 6:18 and LD 3:21). Artificial photoperiods synchronized their activity/rest rhythms and clear differences occurred in (a) phase angles of entrainment relative to the LD cycle and (b) duration of the daily activity phase α. These photoperiod-dependent patterns of entrainment were similar to those reported for epigeous species. Release into constant darkness conditions revealed aftereffects of entrainment to different photoperiods, observed in α but not in the free-running period τ. We also verified if animals coming from summer and winter natural photoperiods entrained equally to the artificial photoperiods by evaluating their phase angle of entrainment, α and τ aftereffects. To this end, experimental animals were divided into “Matching” and “Mismatching” groups, based on whether the experimental photoperiod (short-day [L < 12 h] or long-day [L > 12 h]) matched or not the natural photoperiod to which they had been previously exposed. No significant differences were found in the phase angle of entrainment, α and τ aftereffects in each artificial photoperiod. Our results indicate that the circadian clocks of tuco-tucos are capable of photoperiodic time measurement despite their natural subterranean habits and that the final entrainment patterns achieved by the circadian clock do not depend on the photoperiodic history.
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The genus Ctenomys includes a high number of taxa, with at least ten species from Patagonia and three recently described species for northeastern Chubut Province (Argentina). Ctenomys sociabilis is a social species of the genus Ctenomys and is currently distributed in the surrounding area of Sierra Cuyin Manzano (Neuquén Province), with a recently extinct population that occurred in Laguna Nahuelquir (Cushamen, Chubut Province). Molecular analyses have placed C. sociabilis at the base of Ctenomys clade, as the sister species to all other Ctenomys. Based on a morphological assessment (qualitative and quantitative) and DNA sequencing, we describe a new species of Ctenomys from Esquel, Chubut Province. Phylogenetic analysis shows the new species to be closely related to C. sociabilis, with evidence of solitary behavior. This new species is the first reported to be closely related phylogenetically to Ctenomys sociabilis at the base of the Ctenomys phylogeny. We provide anatomical comparisons between the new species and other species of Ctenomys from Patagonia, especially C. sociabilis.
Chapter
This chapter examines variation in skull morphology among multiple species of Ctenomys and attempts to relate cranial differences to patterns of karyotypic variation in these animals. It discusses the role of chromosomal speciation in Ctenomys using data from two analyses that explored correlations between karyotypic and morphological variation. The chapter concludes that morphological and karyotypic differentiations in these animals are no concordant, which raises questions concerning the processes generating and maintaining these patterns of variation.