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The phylogenetic relationships of the Andean Swamp Rat genus Neotomys (Rodentia, Cricetidae, Sigmodontinae) based on mitochondrial and nuclear markers

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The aim of this study was to assess the phylogenetic position of the South American cricetid genus Neotomys using two molecular markers: one nuclear (Irbp) and one mitochondrial (mt-cyb). This genus is currently considered as incertae sedis in the Sigmodontinae radiation. The phylogenetic relationships were estimated using three approaches: Bayesian inference, maximum likelihood and parsimony. We found the genus Neotomys closely related to the genera Euneomys and Irenomys, which are also considered incertae sedis. Our results suggest a common origin for this group of genera; this fact should be reflected in the taxonomy as a supra generic group with a tribal level. However, further and deeper analysis of both, molecular and morphological data, are needed to diagnose and formalize the proposed tribe. The relationships of this clade to the other members of Sigmodontinae were not clear as assessed by this data set. The three genera are distributed around the Central and Southern Andes in South America evidencing that the Andes have played an important role in the diversification of several tribes of sigmodontine rodents.
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SHORT COMMUNICATION
The phylogenetic relationships of the Andean swamp
rat genus Neotomys (Rodentia, Cricetidae, Sigmodontinae)
based on mitochondrial and nuclear markers
Juan J. Martínez &Luis I. Ferro &Marcos I. Mollerach &
Rubén M. Barquez
Received: 15 June 2011 / Accepted: 18 December 2011 / Published online: 11 January 2012
#Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2012
Abstract The aim of this study was to assess the phyloge-
netic position of the South American cricetid genus Neo-
tomys using two molecular markers: one nuclear (Irbp) and
one mitochondrial (mt-cyb). This genus is currently consid-
ered as incertae sedis in the Sigmodontinae radiation. The
phylogenetic relationships were estimated using three
approaches: Bayesian inference, maximum likelihood and
parsimony. We found the genus Neotomys closely related to
the genera Euneomys and Irenomys, which are also consid-
ered incertae sedis. Our results suggest a common origin for
this group of genera; this fact should be reflected in the
taxonomy as a supra generic group with a tribal level.
However, further and deeper analysis of both molecular
and morphological data are needed to diagnose and
formalize the proposed tribe. The relationships of this clade
to the other members of Sigmodontinae were not clear as
assessed by these data sets. The three genera are distributed
around the Central and Southern Andes in South America
evidencing that the Andes have played an important role in
the diversification of several tribes of sigmodontine rodents.
Keywords Neotomys .Sigmodontinae .Phylogenetics .
Irbp .Cytochrome b
The Andean swamp rat Neotomys, is a monotypic genus of
cricetid rodent distributed along the Central Andean high-
lands (Barquez 1983; Musser and Carleton 2005) and cur-
rently considered as incertae sedis in the Sigmodontinae
radiation (DElía 2006a). The Sigmodontinae genera have
been typically grouped into supra generic entities early in
their zoological classifications (Vorontsov 1959; Reig 1980;
Steadman and Ray 1982; Voss 1988; Olds and Anderson
1989). These pioneer works were not based on quantitative
phylogenetic approaches, but these authors developed one
of the first tribal-level classifications among muroid rodent
subfamily. Later, several authors applied phylogenetic
approaches using both, morphological and molecular char-
acters, to assess phylogenetic relationships either of the
whole subfamily or within tribes (Braun 1993; Steppan
1993;1995; Engel et al. 1998; Smith and Patton 1999;
DElía 2003;DElía et al. 2003; Weksler 2003;DElía et
al. 2006b;Weksler 2006). The results of these studies have
confirmed the existence of several supra generic natural
groups but also changed the limits and genera composition
of many tribes. Additionally, some genera (i.e., Juliomys,
Punomys,Andinomys,Irenomys,Euneomys) could not be
placed into any tribe or monophyletic group less inclusive
than Sigmodontinae and are provisionally considered as
Communicated by: Mabel D. Giménez
J. J. Martínez (*)
Facultad de Ciencias Exactas, Físicas y Naturales,
Universidad Nacional de Córdoba,
Av. Vélez Sarsfield 299,
Córdoba, Argentina
e-mail: juan_jmart@yahoo.com.ar
J. J. Martínez
Departamento de Ciencias Naturales,
Universidad Nacional de Río Cuarto,
Río Cuarto, Argentina
J. J. Martínez :L. I. Ferro :R. M. Barquez
Consejo Nacional de Investigaciones
Científicas y Técnicas (CONICET),
Buenos Aires, Argentina
L. I. Ferro :M. I. Mollerach :R. M. Barquez
Programa de Investigaciones de Biodiversidad Argentina (PIDBA),
Facultad de Ciencias Naturales e Instituto Miguel Lillo,
Universidad Nacional de Tucumán,
Tucumán, Argentina
Acta Theriol (2012) 57:277287
DOI 10.1007/s13364-011-0070-9
incertae sedis (Smith and Patton 1999;DElía 2003;DElía
et al. 2006a).
Neotomys ebriosus was first described by Thomas (1894)
from specimens collected in Vitoc valley, Junín department,
Peru. Later Thomas (1921) described Neotomys vulturnus
from Sierra de Zenta, Jujuy province, Argentina. After-
wards, Sanborn (1947) reviewed the genus and considered
N. vulturnus as a subspecies of N. ebriosus. The genus
Neotomys was traditionally considered either as a Phyllotini
in sensu lato or as a member of the Reithrodon group in
sensu stricto (Olds and Anderson 1989). To date, phyloge-
netic analysis including the genus Neotomys have been
conducted only based on morphological evidence. Steppan
(1995) based on 98 characters, recovered a clade consisting
of Neotomys,Reithrodon,andEuneomys, supporting the
Reithrodon group. On the other hand, Braun (1993) recov-
ered Reithrodon and Neotomys as sister genera based on 46
morphological characters, but Euneomys was not included
in this clade. Later, the Reithrodon group was not recovered
as monophyletic by DElía (2003) in his molecular analysis
(using two genes: Irbp and mt-cyb)ofthephylogenetic
relationships of Sigmodontinae. He supports the view of
Vorontsov (1959 cited in Reig 1980) in the sense that
Reithrodon together with other fossil species conforms the
tribe Reithrodontini (DElía 2003, see also Ortiz et al.
2000). Despite the absence of molecular data to assess the
phylogenetic position of Neotomys,DElía et al. (2006a)
considered Neotomys as incertae sedis based on the poly-
phyletic nature of the Reithrodon group and the fact that
neither Reithrodon nor Euneomys are members of tribe the
Phyllotini (DElía 2003). In this context, molecular data of
Neotomys may be useful to resolve the phylogenetic rela-
tionships of these genera.
Here, we use evidence from two molecular markers to
assess the phylogenetic position of the genus Neotomys in
the Sigmodontinae radiation. We used one nuclear marker,
the first exon of the gene encoding interphotoreceptor
retinoid binding protein (Irbp) and one mitochondrial
marker, the cytochrome b(mt-cyb) gene. Both markers
have been widely employed in phylogenetic studies of
sigmodontine rodents (Smith and Patton 1999;DElía
2003;DElía et al. 2003;Weksler2003;DElía et al.
2006b; Weksler 2006).
The type locality of N. ebriosus vulturnus, was originally
indicated by Thomas in Sierras de Zenta and later relocated
by Díaz and Barquez (2007) in Sierras de Tilcara, Jujuy
province. During a field trip to the type locality of N.
ebriosus vulturnus, we collected two specimens in Sierras
de Tilcara, 12 km ESE of Maimará, 14 km ESE of Tilcara
(23°39.926 S 65°17.917 W), 4, 092 m. The specimens are
now deposited at the Colección Mamíferos Lillo (CML),
Facultad de Ciencias Naturales e Instituto Miguel Lillo,
Universidad Nacional de Tucumán, collection numbers CML
7679 and CML 7680 and original field numbers LT-RMB 77
and LT-RMB 56, respectively.
Total deoxyribonucleic acid (DNA) was extracted from
the specimen CML 7680 following the protocol of salt
extraction (Bruford et al. 1992), precipitated in absolute
ethanol, and dried and stored in TE buffer (Tris-EDTA)
pH 8. The mt-cyb gene was amplified using the primers
Mus14095 and Mus15398 (Anderson and Yates 2000) and
the cycling protocol described in Ferro and Martínez (2009).
The first exon of Irbp gene was amplified using PCR beads
(Qiagen, UK) following Weksler (2003). Double-stranded
PCR products were purified and sequenced by Macrogen
USA (http://www.macrogenusa.com) using BigDye Termi-
nator in an ABI3730×l DNA automatic analyzer. A se-
quence of 1,138 bp of mt-cyb gene was obtained using the
same amplification primers. For Irbp sequencing, we used
two additional internal primers (F and E2; Weksler 2003)
and obtained a sequence of 1,278 bp. Both sequences were
deposited in GenBank under the following accession numb-
ers: HM061604 and HM061605 for mt-cyb and for Irbp,
respectively.
In order to assess the phylogenetic position of Neotomys
in the Sigmodontinae radiation, we included in our taxo-
nomic sampling sequences obtained from GenBank of all
the available genera of sigmodontine tribes and the incertae
sedis considered by DElía et al. (2007)(Table1). The two
matrices (1,143 bp for mt-cyb and 1,278 bp for Irbp) were
aligned independently using the default parameters of Mus-
cle program version 3.6 (Edgard 2004). The two data sets
were then analyzed independently and together by means of
three approaches: Bayesian inference, maximum likelihood,
and maximum parsimony analysis. We performed a Bayes-
ian inference of phylogenetic relationships using MrBayes
3.1 (Ronquist and Huelsenbeck 2003). The models that best
fitted our data sets were selected using AIC-corrected
(AICc) criterion implemented in ModelTest Server 1.0
(http://darwin.uvigo.es/software/modeltest_server.html)
which uses Modeltest 3.8 (Posada and Crandall 1998).
Instead, the TVG+Γ+I model, which was selected by
Modeltest 3.8, we used the GTR+Γ+I model for both genes
because the former model cannot be implemented in
MrBayes 3.1, and we thereby proceeded to realize the next
complex model. The Bayesian analyses were initiated with
two random starting trees with four chains each one (one
cold and three heated chains) and run for 15 million gen-
erations for Irbp and 20 million generations for mt-cyb and
the combined analysis of both genes. The Markov chains
were sampled every 1,000 generations. Of the resulting
trees, the first 25% were discarded as burn-in, while the
remaining trees were summarized in 50% majority rule
consensus tree. Branch lengths were estimated using mean
values of branch lengths of sampled trees after discarded
the burn-in samples. In order to determine the number of
278 Acta Theriol (2012) 57:277287
Table 1 Taxonomic sample employed for the phylogenetic analyses indicating the species included; the tribe according to DElía et al. (2007) and
the GenBank accession numbers for each gene
Species Sigmodontinae tribe mt-cyb GenBank accession
numbers
Irbp GenBank accession
numbers
Cricetus cricetus AJ973392 AY277410
Scotinomys teguina EF990029 AY163639
Neotoma micropus EF989953 EF989853
Peromyscus melanosis EU574701 EF989891
Arvicola terrestres AY332709 AY277407
Tylomys nudicaudus DQ179812 AY163643
Euneomys chinchilloides Incertae sedis AY275115 AY277446
Andinomys edax Incertae sedis AF159284
Irenomys tarsalis Incertae sedis U03534 AY277450
Juliomys pictipes Incertae sedis EU157764 AY163588
Delomys sublineatus Incertae sedis AF108687 AY163582
Neotomys ebriosus Incertae sedis HM061604 HM061605
Calomys lepidus Phyllotini EU579473 AY163580
Graomys chacoensis Phyllotini EU579472 EU649037
Eligmodontia typus Phyllotini EU377643 AY277445
Phyllotis xanthopygus Phyllotini AY956739 AY277471
Andalgalomys pearsoni Phyllotini AF159285 EU649038
Auliscomys pictus Phyllotini U03545 AY277434
Salinomys delicatus Phyllotini EU377608
Tapecomys primus Phyllotini AF159288
Apeomys lugens Thomasomyini DQ003722
Rhipidomys nitela Thomasomyini EU579475 AY163636
Thomasomys baeops Thomasomyini DQ914654 AY163642
Chilomy instans Thomasomyini AF108679
Rhagomys rufescens Thomasomyini AY206770 DQ003723
Bibimys labiosus Akodontini DQ444329 AY277436
Oxymycterus nasutus Akodontini EF661854 AY277468
Blarinomys breviceps Akodontini AF108668 AY277437
Kunsia tomentosus Akodontini AF108670 AY277455
Akodon azarae Akodontini DQ444328 AY163578
Deltamys kempi Akodontini AY195862 AY277444
Juscelinomys huanchacae Akodontini AY275119 AY277453
Lenoxus apicale Akodontini U03541 AY277456
Necromys urichi Akodontini AY273919 AY277463
Scapteromys tumidus Akodontini AY445570 AY277477
Thalpomys cerradensis Akodontini AY273916 AY277481
Thaptomys nigrita Akodontini AF108666 AY277482
Reithrodon auritus Reithrodontini EU579474 AY163634
Abrothrix andinus Abrotrichini AF108671 AY277418
Geoxus valdivianus Abrotrichini U03531 AY277448
Chelemys macronyx Abrotrichini U03533 AY277441
Notiomys edwarsi Abrotrichini EU416275 AY163602
Pearsonomys annectens Abrotrichini AF108672 AY851749
Wiedomys pyrrhorhinos Wiedomyini EU579477 AY163644
Sigmodon leucotis Sigmodontini EU652909 EU635712
Rheomys raptor Ichthyomyini AY163635
Neusticomys monticolus Ichthyomyini EU649036
Acta Theriol (2012) 57:277287 279
discarded trees as burn-in, we plotted the log likelihood
values of cold chains over the sampled generations. Stan-
dard deviation of split frequencies was sufficiently low
(<0.005) and all the values of potential scale reduction
factor (PSRF) in the evolution model were close to 1.00.
These parameters were used as convergence diagnostic.
Maximum likelihood analyses were performed at RAxML
BlackBox on CIPRES portal (http://www.phylo.org/sub_
sections/portal/;Stamatakisetal.2008). We used the
same model as the indicated for Bayesian inference
(GTR+Γ+I). Node support values were evaluated by
means of 1,000 bootstrap replicates. We performed max-
imum parsimony analyses using the program TNT
(Goloboff et al. 2003,2008a). Gaps were treated as
missing data, and characters were considered under equal
weights and implied weights (Goloboff et al. 2008b).
This latter approach weights characters according to a
concave function of homoplasy (Goloboff 1993). The
concavity constant (k) is set by the user and negatively
correlates with how strongly homoplasious characters are
down-weighting. DNA sequence data are usually more
homoplasious than morphological data. Therefore, large k
values (>10) for DNA sequence data are preferable to
avoid extreme down-weighting (Arnedo et al. 2009). We
chose kvalues of 6, 15, 50, and 100. The optimal trees
were estimated by means of the driven search option of
New Technology Search implemented in TNT (Goloboff
1999). The approach used here consisted in finding 100
times the minimum length. Robustness of the nodes was
evaluated by 1,000 bootstrap (Felsenstein 1985) and jack-
knife (Farris et al. 1996) replicates. Jackknife was per-
formed with a removal probability of 0.36. Finally, we
assessed the incongruence of both genes using the incon-
gruence length difference (ILD) test (Farris et al. 1994,
1995). We made 1,000 replications in order to estimate
statistical significance. All the trees were rooted using the
following taxa as outgroups: Cricetus cricetus (Criceti-
nae), Scotinomys teguina,Neotoma micropus,Peromyscus
melanotis (Neotomyinae), Arvicola terrestris (Arvicoli-
nae), and Tylomys nudicaudus (Tylomyinae).
The genetic distances between members of the same tribe
versus different tribes were calculated with the program
MEGA 5.01 (Tamura et al. 2011) using maximum compos-
ite likelihood method and uncorrected pdistances. Tamura
Table 1 (continued)
Species Sigmodontinae tribe mt-cyb GenBank accession
numbers
Irbp GenBank accession
numbers
Oligoryzomys nigripes Oryzomyini DQ826004 AY163612
Euryoryzomys russatus Oryzomyini EU579486 AY163625
Nectomys squamipes Oryzomyini AF181283 EU273419
Scolomys ucayalensis Oryzomyini EU579518 AY163638
Aegialomys xanthaeolus Oryzomyini EU074632 EU273420
Amphinectomys savamis Oryzomyini EU579480 AY163579
Cerradomys scotti Oryzomyini EU579482 EU649040
Ereoryzomys polius Oryzomyini EU579483 AY163624
Handleyomys rostratus Oryzomyini EU579491 EU649045
Holochilus sciureus Oryzomyini EU579497 EU649049
Hylaeamys laticeps Oryzomyini EU579498 EU649050
Lundomys molitor Oryzomyini EU579501 AY163589
Melanomys chrysomelas Oryzomyini EU340018 EU649053
Microryzomys minutus Oryzomyini EU258535 AY163592
Neacomys spinosus Oryzomyini EU579504 AY163597
Nephelomys albigularis Oryzomyini DQ224407 AY163614
Nesoryzomys fernandinae Oryzomyini EU579506 EU649058
Oecomys concolor Oryzomyini EU579508 AY163606
Oreoryzomys balneator Oryzomyini EU258534 EU649068
Oryzomys couesi Oryzomyini EU074662 EU273425
Pseudoryzomys simplex Oryzomyini EU579516 EU649070
Sigmodontomys alfari Oryzomyini EU340016 EU649071
Sooretamys angouya Oryzomyini EU579512 EU649072
Transandinomys talamancae Oryzomyini EU579514 EU649074
Zygodontomys brevicauda Oryzomyini EU579519 EU649075
280 Acta Theriol (2012) 57:277287
et al. (2004) showed that pairwise distances and the related
substitution parameters are accurately estimated by maxi-
mizing the composite likelihood, which is defined as a sum
of related log-likelihoods. Estimates of variance were per-
formed by means of 1,000 bootstrap replicates. According
to phylogenetic results (see below), we included Neotomys,
Euneomys, and Irenomys in a group that was compared with
others previous recognized tribes (e.g., Phyllotini, Akodontini,
etc.). The composition of each tribe is listed in Table 1.
The multiple-sequence alignment yielded no internal
gaps; all of them were external resulting from the use of
different length sequences deposited in GenBank. There
were 319 of 1,278 and 553 of 1,143 phylogenetic informa-
tive sites for Irbp and mt-cyb, respectively. The three criteria
used here to estimate phylogenetic relationships (Bayesian
inference, maximum likelihood, and maximum parsimony)
yielded similar results regarding to the phylogenetic position
of the genus Neotomys either for the two data sets (Irbp and
mt-cyb) analyzed separately or combined. The genus Neo-
tomys was established to be closely allied to Irenomys and
Euneomys, constituting a monophyletic group (Figs. 1,2,3).
The equal weight parsimony analysis yielded 435 mini-
mum length trees (length01,262, consistency index00.567,
retention index00.609) for the Irbp data set (Fig. 1). How-
ever, the implied weighting approach drastically reduced the
number of parsimony trees to 9, 6, 2, and 1 tree for k06, 15,
50, and 100, respectively. Main changes in the results using
this approach were between tribes relationships. However,
all the implied weighting analysis recovered every Sigmo-
dontinae tribe as monophyletic just as depicted in the strict
consensus tree of equal weight analysis (Fig. 1). The clade
formed by Neotomys,Euneomys, and Irenomys was always
highly supported by parsimony analysis with bootstrap and
jackknife values of 96% and 98%, respectively. Maximum
likelihood and Bayesian inference analysis for the Irbp data
set yielded similar results to parsimony analysis regarding to
the phylogenetic relationships of genus Neotomys, which
also grouped together with Euneomys and Irenomys with
high support values (bootstrap and posterior probability;
Fig. 1).
The mt-cyb data set analyzed under the maximum likeli-
hood approach recovered all sigmodontine tribes as mono-
phyletic with two exceptions. Rhagomys was not recovered
within the Thomasomyini, and Juliomys was recovered
within the tribe Oryzomyini (Fig. 2). However, support
values for the recognized tribes were low to moderately
high (e.g., 77% for Abrotrichini and 74% for Phyllotini).
As for the Irbp data set, the analysis of mt-cyb data alone
recovered a very well supported clade formed by Neotomys,
Irenomys,andEuneomys (Fig. 2).
Bayesian inference recovered almost all the recognized
tribes as monophylectic with exception of Thomasomyini.
Rhagomys was grouped as sister genus of the node
composed by Reithrodon,Euneomys,Irenomys, and Neo-
tomys. These last two genera were related (Bayesian poste-
rior probability01.00; Fig. 2). Unlike the maximum
likelihood analysis, the tribe Oryzomyini was recovered as
monophyletic by Bayesian inference with moderate support
(Bayesian posterior probability00.86).
The equal weighted parsimony analysis of the mt-cyb data
set, recovered three minimum length trees (length07,459,
consistency index00.154, retention index00.313). The strict
consensus tree was highly unresolved and with low support
values of bootstrap and jackknife for the Sigmodontinae
tribes. The genus Euneomys was recovered as sister genus of
Neotomys, although with low support (52 and 56 of bootstrap
and jackknife, respectively). When the implied weighting
method was conducted for mt-cyb data set, one completely
resolved tree was obtained for k06, 15, 50, and 100. Although
weakly supported, almost all the tribes were recovered. The
exceptions were Thomasomyini and Oryzomyini for k06and
15 and Thomasomyini for k050 and 100. Under implied
weights, the genus Neotomys was always recovered together
with Euneomys and Irenomys in a monophyletic group.
Finally, the analysis conducted on the combined matrix of
Irbp and mt-cyb sequences yielded similar results to the
independent analysis concerning the phylogenetic position
of Neotomys. The Bayesian phylogram (50% majority rule
consensus) of partitioned analysis of the two genes is pre-
sented in Fig. 3. All previously recognized tribes were recov-
ered as monophyletic, with only two exceptions. First,
Rhagomys was recovered as sister genus of Juliomys but not
within the tribe Thomasomyini (Fig. 3). Second, the two
members of the tribe Ichthyomyini included in this study,
Rheomys and Neusticomys, were not closely related to each
other. Nevertheless, the genus Neotomys still grouped together
with Irenomys and Euneomys in very well supported clade
(Bayesian posterior probability01.00). The maximum likeli-
hood analysis, for the combined data set, confirms the close
relationship among these three genera (Fig. 3). Although
subtle topological differences are apparent in comparison with
Bayesian inference, the tree obtained by maximum likelihood
analysis recovered Neotomys,Irenomys,andEuneomys as a
high supported monophyletic group (99% bootstrap). Again,
Rhagomys was recovered outside of the Thomasomyini and
closely related to Juliomys. However, the remaining sigmo-
dontine tribes were recovered as monophyletic in this analysis
(Fig. 3). The equal weight maximum parsimony analysis
recoverd two trees of 8,814 steps (consistency index00.211,
retention index00.343; Fig. 3). The topology of the strict
consensus is different to those obtained by the Bayesian
phylogenetic inference and maximum likelihood analyses.
Even when not all recognized tribes were recovered as
monophyletic (e. g., Abrotrichini, Thomasomyini, and Ich-
thyomyini), the parsimony analysis still support the monophy-
leticnatureofNeotomys,Euneomys,andIrenomys, with
Acta Theriol (2012) 57:277287 281
relatively high support values (70% bootstrap and 84% jack-
knife). The different values of kin implied weighting ap-
proach produced one resolved tree. The results of ILD test
indicate that the matrices of the Irbp and mt-cyb genes were
significantly incongruent (p<0.01).
Within and between tribes, genetic divergences, expressed
as maximum composite likelihood, were compared with the
group formed by Neotomys,Euneomys,andIrenomys for both
genes Irbp and mt-cyb (Tables 2and 3). The within-group
divergence values of the Neotomys group (1.6%) was similar
to the within-group divergence values of recognized tribes
(1.22.5%) for the Irbp sequence (Table 2). Accordingly,
mean values of between-group divergence for the Neotomys
group (2.66.1%) fell within the range of variation for com-
parisons among recognized tribes (2.68.0%; see Table 2). On
the other hand, within-group divergence values of the Neo-
tomys group for mt-cyb sequences were slightly higher
(24.3%) than the observed values for the other recognized
tribes (13.523.8%). However, between-group divergence
values for the Neotomys group range from 26.3% to 31.2%,
Fig. 1 Strict consensus tree of 435 minimum length trees obtained by
parsimony (equal weight analysis) using Irbp sequences. Values of
1,000 bootstrap and jackknife replicates are indicated in bold and
italics, respectively (only values above 50% are shown). Support
values of bootstrap obtained by maximum likelihood analysis, for
shared nodes with parsimony, are showed in bold italics. Also, the
posterior probability support of Bayesian inference for each shared
node are indicated by means of symbols: white symbols values between
0.75 and 0.89, grey symbols values of 0.90 or higher
282 Acta Theriol (2012) 57:277287
Fig. 2 Maximum likelihood tree [-37,890.165, the estimated parame-
ters were: A00.259, C00.281, G00.207, T00.254, Gamma parameter
α00.579, and I00.437; rate substitution matrix (AC)06.073, (AG)0
7.902, (AT)05.385, (CG)00.699, (CT)045.182, and (GT)01] obtained
using mt-cyb data set. Bootstrap nodal supports (only values above
50% are shown) are indicated in bold italics. Values of 1,000 bootstrap
and jackknife replicates of equal weight maximum parsimony analysis,
for shared nodes, are indicated bold and italics, respectively. The
posterior probability support of Bayesian inference for the shared
nodes are indicated by means of symbols on nodes: white symbols
values between 0.75 and 0.89, grey symbols values of 0.90 or higher
Acta Theriol (2012) 57:277287 283
whereas the range of variation of between-group divergence
among recognized tribes was 15.238.6% (Table 3). The
uncorrected pdistances for Irbp were very similar to those
obtained by maximum composite likelihood. Contrary, and
probably as a consequence of multiple hits, the uncorrected p
distances obtained for mt-cyb data set were lower than those of
maximum composite likelihood method. However, propor-
tions of divergences between and within groups are similar
to those obtained by the maximum composite likelihood
method for mt-cyb (results not shown).
Fig. 3 Bayesian inference 50% majority rule consensus tree obtained
by means of partitioned analysis of Irbp and mt-cyb data sets. The
posterior probability support of Bayesian inference for each node is
indicated by means of symbols on nodes: white symbols values be-
tween 0.75 and 0.89, grey symbols values of 0.90 or higher. The values
in bold and italics represent support values for common nodes obtained
with 1000 bootstrap and jackknife replicates of parsimony (equal
weight analysis; only values above 50% are shown), respectively.
Additionally, support values of bootstrap obtained of maximum likeli-
hood analysis is showed in bold italics
284 Acta Theriol (2012) 57:277287
Our phylogenetic reconstructions assess the phylogenetic
position of Neotomys in the Sigmodontinae radiation from a
molecular perspective. The results obtained in this work
suggest that Neotomys, together with Euneomys and Iren-
omys, belongs to a monophyletic group of genera distinct to
the Phyllotini and not closely related to Reithrodon. Con-
versely, the phylogenetic position of Neotomys, inferred
from morphological data, suggested a close relationship to
Reithrodon (Braun 1993)ortoReithrodon and Euneomys
(Steppan 1993,1995). Our molecular phylogenetic analysis
revealed that Neotomys is allied to Irenomys and Euneomys.
The phylogenetic position of Irenomys had been also elu-
sive. Steppan (1995) identified an Andinomys group includ-
ing Andinomys and Irenomys, while DElía et al. (2006b)
found Irenomys closely related to Euneomys. Beside this,
Irenomys had no clear affinities with other genera, either by
means of morphological or molecular phylogenies (Braun
1993; Smith and Patton 1999;DElía 2003). The well-
supported Neotomys,Irenomys,andEuneomys clade we
have recurrently recovered would probably deserve a tribal
status in order to taxonomically identify this monophyletic
group of genera. The within and between group genetic
differences for Irbp support this suggestion. The values of
consistency index and retention index of Irbp data set are
higher than mt-cyb one. This evidence indicates that the Irbp
data set has lower levels of homoplasy than the mt-cyb data
set. Recently, Feijoo et al. (2010) in a comprehensive anal-
ysis of the systematics of Abrothrix lanosus showed the
congruence between Irbp-based phylogeny and morpholog-
ical variation within Abrothrix, contrary to the mt-cyb-based
Table 2 Mean and standard error (between parentheses) of maximum
composite likelihood distances, expressed as percentage of divergence,
of Irbp sequences within and between the recognized tribes of
Sigmodontinae and the clade obtained in phylogenetic analyses
integrated by Neotomys,Euneomys,andIrenomys, here called the
Neotomys group
Irbp
Tribes 12345678910
1. Abrotrichini (N05) 1.2 (0.3)
2. Akodontini (N013) 3.6 (0.6) 2.1 (0.3)
3. Ichthyomyini (N02) 4.3 (0.7) 4.0 (0.7) 1.7 (0.5)
4. Neotomys group (N03) 3.2 (0.5) 3.0 (0.5) 3.6 (0.6) 1.6 (0.4)
5. Oryzomyini (N025) 4.0 (0.6) 4.1 (0.6) 5.0 (0.7) 3.5 (0.5) 2.5 (0.3)
6. Phyllotini (N06) 3.9 (0.6) 3.7 (0.5) 4.5 (0.7) 3.2 (0.6) 4.4 (0.6) 2.1 (0.3)
7. Reithrodontini (N01) 3.6 (0.7) 2.9 (0.5) 3.8 (0.7) 2.9 (0.6) 3.9 (0.6) 3.2 (0.6) n/a
8. Sigmodontini (N01) 7.3 (1.1) 7.2 (1.0) 5.2 (0.9) 6.1 (0.9) 8.0 (1.0) 7.4 (1.1) 7.0 (1.1) n/a
9. Thomasomyini (N04) 3.0 (0.5) 2.8 (0.4) 3.5 (0.6) 2.3 (0.4) 3.4 (0.5) 3.0 (0.5) 2.6 (0.5) 6.6 (1.0) 2.1 (0.4)
10. Wiedomyini (N01) 3.0 (0.6) 3.1 (0.6) 4.0 (0.7) 2.6 (0.6) 3.9 (0.7) 3.4 (0.6) 3.2 (0.7) 7.0 (1.1) 2.6 (0.5) n/a
n/a Not available values
Table 3 Mean and standard errors (between parentheses) of maximum
composite likelihood distances, expressed as percentage of divergence,
of mt-cyb sequences within and between the recognized tribes of
Sigmodontinae and the clade obtained in phylogenetic analyses inte-
grated by Neotomys,Euneomys, and Irenomys, here called the Neo-
tomys group
Mt-cyb
Tribes 1 2 3 4 5 6 7 8 9
1. Abrotrichini (N05) 13.5 (2.4)
2. Akodontini (N013) 22.2 (3.1) 19.6 (2.5)
3. Neotomys group (N03) 29.4 (4.5) 30.7 (4.4) 24.3 (4.1)
4. Oryzomyini (N025) 16.6 (2.7) 22.1 (3.1) 28.5 (4.2) 15.2 (2.3)
5. Phyllotini (N08) 17.5 (2.8) 24.8 (3.5) 28.9 (4.3) 17.4 (2.6) 17.2 (2.8)
6. Reithrodontini (N01) 28.1 (4.7) 30.3 (4.5) 28.2 (4.8) 29.6 (4.9) 34.4 (5.7) n/a
7. Sigmodontini (N01) 16.2 (3.3) 23.3 (3.8) 31.2 (5.0) 15.2 (2.8) 19.3 (3.4) 28.5 (5.8) n/a
8. Thomasomyini (N04) 20.1 (3.0) 24.5 (3.2) 27.2 (3.8) 21.4 (3.0) 22.0 (3.1) 32.0 (5.1) 22.4 (3.7) 23.8 (3.7)
9. Wiedomyini (N01) 18.8 (3.6) 23.1 (3.7) 26.3 (4.7) 21.0 (3.7) 18.8 (3.3) 38.6 (7.1) 20.9 (4.6) 19.8 (3.4) n/a
n/a Not available values
Acta Theriol (2012) 57:277287 285
phylogeny which was largely incongruent. We believe that
more evidence should be achieved, both molecular and
morphological, to refute or confirm our results. Further-
more, additional morphological data will provide more ro-
bustness to our results and the hypothesis concerning the
tribal status of this clade. From a molecular perspective, an
essential point in further analysis should be the inclusion of
other incertae sedis genera such as Punomys and Andinomys
(including Irbp sequence) as well as additional genes to
elucidate the phylogenetic relationship of this group. A
formal definition and diagnosis of the proposed tribe will
be desirable such as the recently formalized Abrotrichini
tribe (DElía et al. 2007) that was previously identified by
means of molecular phylogenetic analysis (Smith and Patton
1999;DElía 2003).
The three genera that comprise this lineage are mainly
distributed along the Andes. Neotomys is in the highlands of
the Central Andes (Pardiñas and Ortiz 2001;Anderson
1997; Barquez 1983; Sanborn 1947). Irenomys inhabits the
Patagonic forest of the southern Andes of Chile and
Argentina, whereas the genus Euneomys is distributed from
the highlands of the southern Andes to Patagonian region
(Musser and Carleton 2005;DElía et al. 2006a;Martin
2010; Pardiñas et al. 2010). The geographic distribution of
this monophyletic group of genera suggests that the Andes
may have played an important role in the diversification of
these genera as well as for several tribes of Sigmodontinae
such as Akodontini and Phyllotini (Reig 1984; Braun 1993).
In our analysis, the genus Neotomys was found to be
part of a quite stable, well-supported, and previously
unrecognized lineage in Sigmodontinae radiation. These
results provide enlightenment for the understanding of
the sigmodontine radiation and clues for further inves-
tigations about the systematic relationships of these
rodents.
Acknowledgments We are grateful to CONICET for the fellowship
given to JJM and LIF and for the financial support through PIP
CONICET 6197 to Ulyses F. J. Pardiñas and Rubén M. Barquez. We
are also grateful to Noemí Gardenal for her kindness in providing lab
infrastructure support. We thank two anonymous reviewers whose
valuable comments improved considerably this work.
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