Journal of Mammalogy, 93(6):1431–1439, 2012

Phylogenetics and biogeography of the microendemic rodent

Xerospermophilus perotensis (Perote ground squirrel) in the Oriental
Basin of Mexico
JESÚS A. FERNÁNDEZ*
Department of Biological Sciences and Museum of Natural Science, Louisiana State University, Baton Rouge, LA 70803,

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USA
Present address of JAF: Colección Nacional de Mamı́feros, Instituto de Biologı́a, Universidad Nacional Autónoma de
México, Apartado Postal 70-153, Colonia Ciudad Universitaria, 04310 México, Distrito Federal, México
* Correspondent: jferna9@tigers.lsu.edu

Phylogenetic relationships of the Mexican endemic and endangered Perote ground squirrel, Xerospermophilus
perotensis (Rodentia: Sciuridae), were examined using 2 mitochondrial (cytochrome-b [Cytb] and 12S ribosomal
RNA) and 2 nuclear (growth hormone receptor and interphotoreceptor retinoid-binding protein) genes for a total
of 3,403 base pairs. Gene sequences were analyzed using maximum-likelihood and Bayesian models of
phylogenetic inference. Independent analyses of the 4 gene sequences converged on essentially identical gene
trees, all showing X. perotensis to be sister to X. spilosoma from San Luis Potosı́, Mexico, and nested within
other geographic samples of X. spilosoma. Given the current absence of diagnostic morphological characters to
distinguish X. perotensis from X. spilosoma and the moderate level of Cytb sequence divergence between the 2
forms (3.6%, which is less than divergence values measured between other subspecies of X. spilosoma), X.
perotensis is herein reduced to subspecies status as X. spilosoma perotensis. Based on molecular estimates of
divergence times, phyletic diversification of the genus Xerospermophilus began near the end of the Pliocene and
X. spilosoma perotensis diverged from other Mexican populations of X. spilosoma during Pleistocene times.
Climate cycles during the Pleistocene and the final uplift of the Trans-Mexico Volcanic Belt may have played a
major role in early diversification in this lineage.

Key words: biogeography, endemic species, Mexican Plateau, molecular differentiation, phylogenetic analyses, pygmy
ground squirrel, Trans-Mexico Volcanic Belt
Ó 2012 American Society of Mammalogists
DOI: 10.1644/11-MAMM-A-409.1

The concept of endemism is central to the fields of
biogeography and biological conservation, and areas with high
numbers of endemic species, or ‘‘biodiversity hot spots,’’ often
are included in protected area networks (Myers et al. 2000). In
biogeography, an area of endemism usually is defined as a
region that contains the only known occurrences of 2 or more
taxa (i.e., multiple taxa are restricted to that region), but other
definitions of ‘‘areas of endemism’’ focus on the area’s
geographic delimitation by natural barriers or the distributional
congruence of several species in the area (Harold and Mooi
1994; Hausdorf 1998; Lomolino et al. 2010; Platnick 1991).
Mexico is widely known as a biologically megadiverse
country and a biodiversity hot spot (Lamoreux et al. 2006); the
diverse Mexican biota is the product of interactions between a
dynamic and complex topography and myriad ecological and
historical factors (Velasco de León et al. 2007). In central
Mexico, the highlands and arid valleys of the Trans-Mexico
1431
Volcanic Belt are home to one of the most diverse biotas in the
world (Luna et al. 2007).
Among the mountains at the southeastern edge of the Trans-
Mexico Volcanic Belt lies the Oriental Basin (Cuenca Oriental;
Fig. 1). By any definition of ‘‘area of endemism,’’ this semiarid,
endorheic (closed drainage) basin, which covers portions of the
states of Puebla, Tlaxcala, and Veracruz, is an important area
of endemism in North America. This relatively small
(approximately 5,000-km2) basin is characterized by alkaline
grasslands, bunch grasses, and aridland scrubs in the valleys
and coniferous forests in the surrounding mountains (Valdéz
and Ceballos 1997). The basin supports several endemic taxa
www.mammalogy.org
1432 JOURNAL OF MAMMALOGY
FIG. 1.—Geographical distribution of pygmy ground squirrels of
the genus Xerospermophilus (modified from Hall [1981]). Numbered
dots show collection localities listed in Appendix I for specimens of
Xerospermophilus used in this study. The shaded area near locality 2
shows the approximate extent of the Oriental Basin (Cuenca Oriental),
and rectangle shows location of the Trans-Mexico Volcanic Belt
(TMVB).
of plants and animals, including at least 4 taxa of endemic
mammals: the Oriental Basin pocket gopher (Cratogeomys
fulvescens—Hafner et al. 2005), the Perote deermouse
(Peromyscus bullatus—González-Ruı́z and Álvarez-Castañeda
2005), Nelson’s woodrat (Neotoma nelsoni—González-Ruı́z et
al. 2006), and the Perote ground squirrel (Xerospermophilus
perotensis—Best and Ceballos 1995). As noted by Hafner and
Riddle (2005), the Oriental Basin has been subjected to
extensive agricultural conversion, resulting in damage or loss
of much of the native desert habitat.
Shreve (1942) referred to the Oriental Basin as the
southernmost extension of the Chihuahuan Desert, and most
mammals of the Oriental Basin, including X. perotensis, are
arid-adapted species. Typically, the closest relatives of Oriental
Basin endemics inhabit the deserts of the Mexican Plateau to
the north, and this appears to be the case for X. perotensis,
whose sister species is thought to be X. spilosoma (Fig. 1;
Howell 1938).
In his revision of North American ground squirrels, Howell
(1938) classified all ground squirrels in the genus Citellus (later
transferred to Spermophilus by Hershkovitz [1949]) and
divided the genus into 8 subgenera: Ammospermophilus,
Callospermophilus, Citellus, Ictidomys, Notocitellus, Otosper-
mophilus, Poliocitellus, and Xerospermophilus. Early morpho-
logical and chromosomal studies suggested a close relationship
between Spermophilus perotensis and S. spilosoma (Howell
1938; Uribe-Alcocer and Ahumada-Medina 1990); however,
Vol. 93, No. 6
composition of and relationships among the subgenera of
Spermophilus were not clearly understood at that time. S.
perotensis and S. spilosoma were placed as sister taxa in the
subgenus Ictidomys, along with I. tridecemlineatus, I. mex-
icanus, and the more recently described I. parvidens (Helgen et
al. 2009).
The taxonomic status and systematic affinities of S.
perotensis were not investigated again until molecular studies
by Harrison et al. (2003) and Herron et al. (2004) confirmed the
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close affinity of S. perotensis with S. spilosoma. In fact, both
molecular studies (using the same specimens of S. spilosoma
and based on the cytochrome-b [Cytb] gene) showed S.
spilosoma to be paraphyletic with respect to S. perotensis, with
S. s. pallescens from Mexico sister to S. perotensis, and S. s.
marginatus from Kansas sister to the S. s. pallescens þ S.
perotensis clade. These same studies showed the S. perotensis
þ S. spilosoma clade (subgenus Ictidomys) to be sister to the S.
mohavensis þ S. tereticaudus clade (subgenus Xerospermo-
philus), with prairie dogs (Cynomys) sister to this group.
Helgen et al. (2009) combined new morphological data with
the molecular evidence provided by Harrison et al. (2003) and
Herron et al. (2004) to elevate the subgenus Xerospermophilus
to full generic status. In Xerospermophilus, Helgen et al.
(2009) included the 4 species of pygmy ground squirrels
adapted to arid and semiarid conditions: X. mohavensis, X.
tereticaudus, X. spilosoma, and X. perotensis. In view of the
potential paraphyly of X. spilosoma (Harrison et al. 2003;
Herron et al. 2004), Helgen et al. (2009:294) recommended
future research into species-level boundaries in the spilosoma–
perotensis complex and suggested that ‘‘X. perotensis may
prove to be best classified as the southernmost subpopulation
of X. spilosoma.’’
Despite previous morphological and molecular studies of the
systematic status of X. perotensis and allied taxa, several
uncertainties remain with respect to the species status of X.
perotensis, monophyly of X. spilosoma, and the timing of
diversification events within the genus Xerospermophilus
relative to major geological and climatic events. Each of these
issues is explored in this analysis using newly acquired
samples of X. perotensis, X. spilosoma, and other members of
the genera Xerospermophilus and Ictidomys, and sequence
evidence from multiple mitochondrial and nuclear genes.
MATERIALS AND METHODS
Sampling.—Tissue samples of I. mexicanus (n ¼ 1
individual), I. parvidens (n ¼ 2), I. tridecemlineatus (n ¼ 4),
X. mohavensis (n ¼ 2), X. perotensis (n ¼ 4), X. spilosoma (n ¼
3), and X. tereticaudus (n ¼ 2) were either collected in the field
under the authority of Mexican collecting permit FAUT-0002
(issued to F. A. Cervantes) or donated by museums (Appendix
I). In addition to the DNA sequences generated in this study,
34 sequences were downloaded from GenBank for use in the
molecular analyses (Appendix I). Outgroups in the analyses
included specimens of Urocitellus townsendii (in the Cytb
analysis), Callospermophilus lateralis (in the 12S ribosomal
December 2012 FERNÁNDEZ—SYSTEMATICS OF XEROSPERMOPHILUS PEROTENSIS
RNA [12S] and interphotoreceptor retinoid-binding protein
[IRBP] analyses), and species of the genus Ictidomys (in the
growth hormone receptor [GHR] analysis). The collection and
processing of samples were undertaken following the
guidelines of the American Society of Mammalogists for use
of wild animals in research (Kelt et al. 2010; Sikes et al. 2011).
Laboratory protocols.—Total genomic DNA was extracted
from tissue using a commercial kit (DNeasy Blood and Tissue
Kit; Qiagen Inc., Valencia, California). Portions of 2 nuclear
genes (GHR and IRBP), and 2 mitochondrial genes (Cytb and
12S) were sequenced for subsequent analysis. The genes were
amplified by polymerase chain reaction (Saiki et al. 1988)
using the following universal primers developed for rodents:
GHR1f and GHRend1f for GHR (Jansa et al. 2009); IRBP-A
and IRBP-B for IRBP (Stanhope et al. 1992); MVZ-05 and
H15915 for Cytb (Irwin et al. 1991); and 12S L82 and 12S
H900 for 12S (Nedbal et al. 1994). Polymerase chain reaction
amplification of the GHR gene was performed under the
following parameters: initial denaturation at 948C for 5 min
followed by 34 cycles of denaturation at 948C for 15 s,
annealing at 608C for 1 min, extension at 728C for 1.5 min, and
1 final extension at 728C for 10 min. Amplification of the IRBP
gene began with initial denaturation at 958C for 10 min
followed by 27 cycles of denaturation at 958C for 25 s,
annealing at 588C for 20 s, extension at 728C for 1 min, and 1
final extension at 728C for 10 min. Amplification of both
mitochondrial genes began with initial denaturation at 958C for
2 min followed by 27 cycles at 958C for 1 min, annealing at
498C for 1 min, extension at 728C for 2 min, and 1 final
extension at 728C for 7 min (Mantooth et al. 2000).
Amplifications were performed in a total volume of 25 ll
and 200 ng of DNA. Agarose gels (2%) were used to visualize
amplified products. Polymerase chain reaction products were
purified using either polyethylene glycol or ExoSAP-IT
(Affymetrix, Santa Clara, California). DNA sequencing was
performed for both light and heavy strands with a Big Dye
Terminator version 1.1, version 3.1 in an automated 3100
Genetic Analyzer (Applied Biosystems, Foster City,
California) at the Museum of Natural Science, Louisiana
State University. Editing and alignment of sequences and
matrix manipulations were performed in Sequencher 4.7 (Gene
Codes Corporation, Ann Arbor, Michigan), MacClade
(Maddison and Maddison 2000), and Mesquite (Maddison
and Maddison 2010). Sequences were verified manually, and
authenticity of the gene was confirmed by amino acid
translation and BLAST searches in GenBank (http://blast.
ncbi.nlm.nih.gov/Blast.cgi).
Estimates of genetic divergence.—The identification of
different rates of DNA substitution in a data set is not
uncommon, and the use of a correction for the unobserved
substitutions is suggested (Felsenstein 2004). To enable
comparison of my results with those of previous studies
(Harrison et al. 2003; Herron et al. 2004), sequence divergence
values for the Cytb gene were corrected using the Kimura 2-
parameter substitution model (Kimura 1980) in PAUP* 4.0b10
(Swofford 2003) and MEGA version 5 (Tamura et al. 2011).
1433
Saturation analyses for 3rd codon positions were performed
using the methods of Griffiths (1997), and maximum-
likelihood (ML) analyses were run with and without 3rd
codon transitions to evaluate the effects of 3rd codon
substitutions on phylogenetic reconstruction.
Phylogenetic analyses.—Initial phylogenetic analyses were
conducted using Bayesian inference (BI) in the program
MrBayes (version 3.2-cvs—Huelsenbeck and Ronquist 2001;
Ronquist and Huelsenbeck 2003) and ML in PAUP*. Analysis
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of the Cytb data included 37 sequences of 14 species for which
complete Cytb sequences were available. Phylogenetic analysis
of the 12S gene included 17 specimens of 8 species, analysis of
GHR included 14 specimens of 6 species, and analysis of IRBP
included 16 specimens representing 8 species (Appendix I).
Following analyses of individual genes, a partitioned analysis
including all 4 genes was conducted using ML and BI
frameworks. ML analyses were run in both PAUP* and PhyMl
3.0 (Guindon and Gascuel 2003). Variable nucleotide positions
were considered unordered, discrete characters with 4 possible
states (A, C, G, and T). Best-fit models for ML and BI analyses
were evaluated using the Akaike information criterion and the
program jModeltest 0.1.1 (Guindon and Gascuel 2003; Posada
2008). The following models were selected for Cytb, 12S,
GHR, and IRBP genes, respectively: TrN þ G, TIM3 þ G,
TPM3UF þ I þ G, and TPM3UF þ I. ML clade support was
assessed with 500 bootstrap (bs) replicates in PAUP* and
PhyMl 3.0, and clade support in the BI analyses was evaluated
using posterior probabilities (pp).
Maximum-likelihood analyses were performed with the
starting trees obtained from 100 random, stepwise additions
followed by tree-bisection-reconnection branch swapping. In
the BI analyses, best-fit models were applied to each data
partition with unlinked parameters and allowing rate variation.
The Metropolis Markov chain Monte Carlo analysis consisted
of 2 independent runs of 10 3 106 generations in which trees
were sampled every 103 generations, resulting in 104 samples
for each run. After discarding the initial 10% as burn-in, a
majority-rule consensus tree was constructed using the final 18
3 103 trees. The analysis was stopped when the average
standard deviation of split frequencies approached zero
(,0.01) and convergence was reached, as determined using
Tracer version 1.5 (Rambaut and Drummond 2007) and
AWTY (Nylander et al. 2008). The combined data set was
analyzed in a partitioned manner (genes and model parameters)
to allow for independent convergence on optimal values for
each component (Ronquist and Huelsenbeck 2003). Data
partitions included mitochondrial versus nuclear genes, Cytb
versus 12S, Cytb versus IRBP, and 12S versus IRBP genes.
Nodes were considered well supported if there was .80% bs
support in ML analyses or .95% pp in BI analyses.
Estimates of divergence times.—The program *BEAST
version 1.6.0 (Drummond and Rambaut 2007) was used to
generate estimates of the timing of divergence of X. perotensis
from related species. *BEAST analyses were carried out using a
Yule tree prior and implicitly considering the Cytb gene tree to
represent the species tree. The estimate was calibrated using a
1434 JOURNAL OF MAMMALOGY Vol. 93, No. 6

dated fossil (Goodwin 1995; Harrison et al. 2003; Pizzimenti
1975) to constrain the minimum date for separation of Cynomys
from Xerospermophilus to 2.7 million years ago (mya). To
account for uncertainty in the fossil-based calibration, the fossil
date was modeled on a lognormal distribution rather than a point
calibration (Ho and Phillips 2009). The analysis used a relaxed
clock with a lognormal distribution allowing rate variation
among sites. Two independent analyses were run for 207
generations each, sampling the parameter every 103 generations.
3 in Fig. 1). The other samples of X. spilosoma from Durango
(locality 6), Kansas (locality 5), and New Mexico (locality 4)
are added to the tree in a stepwise fashion. X. mohavensis and
X. tereticaudus also are depicted as sister taxa. Among the
many outgroups used in the analysis (listed above and in
Appendix I), the genus Cynomys was found to be sister to
Xerospermophilus, although this relationship was not well
supported (pp ¼ 0.84; bs ¼ 79%) and therefore is not shown in
Fig. 2.

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Convergence statistics were checked for effective sample sizes
using Tracer version 1.5 and AWTY. Consensus trees were
generated from the resulting 20 3 103 trees using TreeAnnotator
version 1.6.0 (Rambaut and Drummond 2009) after elimination
of 10% as burn-in.
RESULTS
Analyses of DNA sequences involved a total of 3,403 base
pairs (bp), including 1,141 bp of Cytb, 736 bp of 12S, 910 bp
of GHR, and 616 bp of IRBP. ML and BI analyses using only
Cytb sequences from the 37 individuals with complete Cytb
sequences recovered trees with identical branch structure (Fig.
2). In these trees, there is strong support (pp ¼ 1.00; bs ¼
100%) for monophyly of the genus Xerospermophilus. Within
Xerospermophilus, X. perotensis is nested within X. spilosoma,
and most closely allied with its geographically closest neighbor
in the state of San Luis Potosı́ on the Mexican Plateau (locality
The Cytb divergence values (Table 1) show the taxa
included in Fig. 2 to be well differentiated genetically. X.
perotensis is 3.6% genetically divergent from the X. spilosoma
sample from San Luis Potosı́, and these 2 populations together
show an average Cytb divergence of 6.4% from the other
samples of X. spilosoma from Durango, Kansas, and New
Mexico. The X. perotensis þ X. spilosoma clade (including all
samples of spilosoma) shows an average of 11.2% sequence
divergence from the X. mohavensis þ X. tereticaudus clade and
11.8% divergence from specimens of the genus Cynomys.
Independent BI and ML analyses of 12S, GHR, and IRBP
sequences confirmed the Cytb topology shown in Fig. 2,
although nodal support values varied widely depending on the
gene analyzed (trees not shown but available on request). In all
analyses, the genus Xerospermophilus was depicted as mono-
phyletic and sister to Cynomys, and the sister species status of X.
mohavensis þ X. tereticaudus was confirmed with strong
support. All the samples of X. spilosoma and X. perotensis

FIG. 2.—Relationships among major clades of Xerospermophilus based on maximum-likelihood (ML) and Bayesian analyses of cytochrome-b
sequences. Locality numbers (mapped in Fig. 1 and listed in Appendix I) are indicated before taxon names, and numbers on branches indicate ML
bootstrap support (above) and Bayesian posterior probabilities (below). Numbers at nodes are estimated mean divergence dates (million years ago)
calculated in the *BEAST analysis. Shaded bars show 95% credibility intervals.
December 2012 FERNÁNDEZ—SYSTEMATICS OF XEROSPERMOPHILUS PEROTENSIS
TABLE 1.—Mean percent cytochrome-b sequence divergence values (Kimura 2-parameter model) among species of the genus
Xerospermophilus and Cynomys. The specimen of X. spilosoma from San Luis Potosı́ is from locality 3 in Fig. 1, the specimen from Durango
is from locality 6, and the specimens from New Mexico and Kansas are from localities 4 and 5, respectively.
X. spilosoma
X. perotensis San Luis Potosı́
X. perotensis — 3.6
X. spilosoma San Luis Potosı́ — 6.0
X. spilosoma Durango
X. spilosoma New Mexico and Kansas
X. mohavensis
X. tereticaudus
Cynomys
formed a monophyletic group, and the sister relationship
between X. perotensis and the X. spilosoma sample from San
Luis Potosı́ was recovered, but with low nodal support in the
analyses of the nuclear genes (GHR and IRBP).
The BI and ML analyses of the partitioned data sets
(partitioned by mitochondrial genes only, nuclear genes only,
and mitochondrial þ nuclear genes) focused on relationships
within Xerospermophilus (Fig. 3). In all partitioned analyses, the
genus Xerospermophilus was depicted as monophyletic with
high support values. Again, the samples of X. spilosoma and X.
perotensis formed a monophyletic group, and the sister status of
X. perotensis and X. spilosoma from San Luis Potosı́ was
confirmed with high nodal support (pp . 0.97; bs ¼ 100%).
Mean estimates of divergence times (Fig. 2) ranged from a
low of 0.7 mya between X. perotensis and X. spilosoma (San
Luis Potosı́) to a high of 3.5 mya between the genera Cynomys
and Xerospermophilus. All estimates of divergence times
within the genus Xerospermophilus place these events in the
Pleistocene, with the possible exception of the split between
FIG. 3.—Relationships among major clades of Xerospermophilus
based on a maximum-likelihood (ML) analysis of cytochrome-b
(Cytb), 12S ribosomal RNA, growth hormone receptor, and
interphotoreceptor retinoid-binding protein sequences partitioned by
gene. Locality numbers (mapped in Fig. 1 and listed in Appendix I)
are indicated before taxon names, and numbers on branches indicate
ML bootstrap support (above) and Bayesian posterior probabilities
(below). A Bayesian analysis of the same data yielded identical
relationships. Xerospermophilus spilosoma from Durango (locality 6)
was excluded from these analyses because only Cytb sequences were
available for that specimen.
1435
X. spilosoma X. spilosoma
Durango New Mexico and Kansas X. mohavensis X. tereticaudus Cynomys
5.2 7.9 10.0 11.5 11.9
6.4 10.6 12.0 12.0
— 5.5 9.9 11.8 11.2
— 10.6 12.9 12.2
— 4.6 11.0
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— 14.2
—
the X. mohavensis þ X. tereticaudus clade and the X. perotensis
þ X. spilosoma clade, which was estimated at 2.7 mya with a
confidence interval extending from 4.3 to 1.3 mya (Fig. 2).
DISCUSSION
This study of mitochondrial and nuclear DNA sequences
confirms that X. perotensis is a genetically well-differentiated
unit within Xerospermophilus. The sister relationship between
X. perotensis and the sample of X. spilosoma from San Luis
Potosı́ (representing the subspecies X. s. cabrerai) also is
strongly supported in this study and is consistent with evidence
provided by Uribe-Alcocer and Ahumada-Medina (1990), who
reported chromosomal similarities between X. perotensis and
X. s. cabrerai and interpreted this as an indicator of a close
phylogenetic relationship between these taxa.
Species status of X. perotensis.—Since its original
description by Merriam (1893), X. perotensis has been
considered a valid species. However, recent morphological
and molecular studies have questioned its species status, and
some authors have suggested that X. perotensis is best regarded
as a subspecies of X. spilosoma (Harrison et al. 2003; Helgen et
al. 2009; Herron et al. 2004). The present study confirms that
continued recognition of X. perotensis at the species level
renders X. spilosoma paraphyletic (Figs. 2 and 3). Paraphyly of
X. spilosoma could be resolved taxonomically by recognizing
multiple species within X. spilosoma, but unless one recognizes
species based solely on degree of genetic divergence, no
evidence is available at this time suggesting that X. spilosoma
is a composite of multiple cryptic species. It also could be
argued that populations of X. perotensis and X. spilosoma from
San Luis Potosı́ (X. s. cabrerai) should be combined into a
single species. However, again, there is no evidence for
species-level divergence between X. s. cabrerai and other
subspecies of X. spilosoma except for the relatively large Cytb
distances measured between the subspecies examined in this
study (5.2–7.9%; Table 1). Synonymization of X. s. cabrerai
with X. perotensis still would require recognition of multiple
species within X. spilosoma to maintain monophyletic taxa.
Sister species within the sciurid genera Cynomys and
Marmota show Cytb divergence values ranging from 1.2% to
7.7% (Harrison et al. 2003; Steppan et al. 1999), so the
divergence value calculated between X. perotensis and X. s.
1436 JOURNAL OF MAMMALOGY
cabrerai in this study (3.6%) lies within this range but is less
than the ‘‘high genetic divergence’’ value of 5% suggested by
Baker and Bradley (2006:654) to signal possible cryptic
species. Morphologically, X. perotensis differs from X.
spilosoma in ways that are usually used to distinguish among
subspecies of rodents. For example, X. perotensis resembles X.
s. pallescens of the northern Mexican Plateau and Sierra Madre
Oriental, except that X. perotensis is larger overall, has a
shorter tail, is more yellowish dorsally, and has smaller and
less-conspicuous buffy spots (Best and Ceballos 1995). The
skull of X. perotensis is similar to that of X. s. spilosoma (found
in southern Durango, Zacatecas, and parts of nearby states),
except that the skull of X. perotensis is larger, has a relatively
narrower and higher braincase, has auditory bullae that are
broader and more flattened, and has molariform teeth that are
heavier than those of X. s. spilosoma (Best and Ceballos 1995;
Helgen et al. 2009; Uribe-Alcocer et al. 1978).
Considering the absence of morphological or chromosomal
evidence supporting the species status of X. perotensis, I herein
take the conservative route and recognize perotensis as a
subspecies of X. spilosoma (as X. s. perotensis). The relatively
high divergence values measured between the subspecies of X.
spilosoma in this study (Table 1) may signal presence of
multiple cryptic species, but if so, recognition of additional
species must await a thorough study of geographic variation
throughout the range of X. spilosoma.
Biogeography of Xerospermophilus on the Mexican Plateau
and in the Oriental Basin.—Shreve (1942) recognized that the
Mexican Plateau, the Oriental Basin, and other isolated arid
and semiarid regions of central Mexico were relicts of a once-
continuous southern extension of the Chihuahuan Desert. More
recent research suggests that the arid and semiarid lands of
central Mexico were continuous until the mid- to late Miocene,
when rise of the Trans-Mexico Volcanic Belt began to act as a
barrier between populations of arid-adapted species
(Ferrusquı́a-Villafranca and González 2005; Ferrusquı́a-
Villafranca et al. 2005). Hoffmann and Jones (1970)
examined present-day distributions of several mammal
species in Mexico and suggested that many prairie and desert
species may have reached their southernmost distributions
during Pleistocene times, with subsequent range contractions
leaving isolated populations in the south. They suggested that
Cynomys mexicanus was one such peripheral isolate of the
once more-widespread species, C. ludovicianus (Hoffmann and
Jones 1970). The Perote ground squirrel, X. s. perotensis,
isolated in the Oriental Basin of central Mexico, may be
another example of this phenomenon.
Uribe-Alcocer and Ahumada-Medina (1990) speculated that
X. spilosoma stock was once widespread throughout the
highlands of northern Mexico and was able to disperse
southward because of continuous, dry habitats found in
intermontane valleys. Subsequent tectonic or climatic events,
or a combination of both, during the Pleistocene fragmented
the once-continuous grassland habitat in central Mexico,
leaving the present-day patches of arid and semiarid habitats,
including the Oriental Basin (Ferrusquı́a-Villafranca and
Vol. 93, No. 6
González 2005; Ferrusquı́a-Villafranca et al. 2005; Hoffmann
and Jones 1970; Pizzimenti 1975).
The results of this study underscore the biotic importance of
3 understudied biogeographic regions of Mexico: the Oriental
Basin (inhabited by X. s. perotensis), the Mexican Plateau (X.
s. cabrerai), and the Bolsón de Mapimı́ (X. s. pallescens). The
origin of the Oriental Basin is closely linked with the volcanic
activity that gave raise to alkaline lakes and the rain-shadow
effect that caused isolated pockets of arid and semiarid land in
Downloaded from https://academic.oup.com/jmammal/article-abstract/93/6/1431/910757 by UNAM user on 12 June 2019
the Trans-Mexico Volcanic Belt (Caballero et al. 2003; Morán-
Zenteno 1994). The Mexican Plateau formed as a result of
uplifting of the Sierra Madre Oriental, Sierra Madre Occiden-
tal, and Trans-Mexico Volcanic Belt, which created a dry
tableland in the rain shadow of these large mountain ranges.
Recent phylogenetic and biogeographic studies are beginning
to show the importance of the Mexican Plateau as a center of
evolutionary divergence in many rodent taxa (Fernández et al.
2012; Neiswenter and Riddle 2010). Finally, the Bolsón de
Mapimı́, a closed desert basin located north of the Sierra de San
Luis Potosı́, Sierra de Zacatecas, and Sierra de la Breña,
formed during the Wisconsinan glacial period of the Pleisto-
cene and acted as a refugium for many desert organisms (Elias
1992), including the ancestors of X. s. pallescens.
RESUMEN
Se examinaron las relaciones filogenéticas de la ardilla terrestre
de Perote Xerospermophilus perotensis (Rodentia: Sciuridae),
especie mexicana endémica y amenazada, usando 2 genes
mitocondriales (Citocromo b [Citb] y 12S ARN ribosomal) y 2
genes nucleares (Receptor de la hormona del crecimiento y la
Proteı́na de unión al retinoide intersticial) para un total de 3,403
pares de bases. Las secuencias genéticas fueron analizadas
usando máxima verosimilitud y modelos Bayesianos de infer-
encia filogenética. Los análisis independientes de las secuencias
de los 4 genes convergieron esencialmente en árboles de genes
identicos, todos mostrando a X. perotensis como taxa idénticos de
X. spilosoma de San Luis Potosı́, México y anidados dentro de
otras muestras geográficas de X. spilosoma. Dada la ausencia
actual de caracteres morfológicos diagnósticos para distinguir X.
perotensis de X. spilosoma y el nivel moderado de divergencia de
las secuencias de Citb entre las 2 formas (3.6%, que es menor a los
valores de divergencia medidos entre otras subespecies de X.
spilosoma), X. perotensis aquı́ se reduce a status subespecı́fico
como X. spilosoma perotensis. Basado en estimaciones molec-
ulares de tiempo de divergencia, la diversificación filetica del
género Xerospermophilus comenzó cerca del final de Plioceno y
X. spilosoma perotensis divergió de otras poblaciones mexicanas
de X. spilosoma durante el Pleistoceno. Los ciclos climáticos
durante el Pleistoceno y el alzamiento final del Eje Neovolcánico
Trans-Mexicano pudieron jugar un papel importante en la
diversificación temprana de este linaje.
ACKNOWLEDGMENTS
The following persons kindly donated tissues and specimens for use
in this study: J. Cook, Museum of Southwestern Biology, University
December 2012 FERNÁNDEZ—SYSTEMATICS OF XEROSPERMOPHILUS PEROTENSIS
of New Mexico; R. Acosta G., Museo de Zoologı́a ‘‘Alfonso L.
Herrera,’’ Facultad de Ciencias, Universidad Nacional Autónoma de
México; F. Cervantes,Y. Hortelano M., and J. Vargas C., Colección
Nacional de Mamı́feros, Instituto de Biologı́a, Universidad Nacional
Autónoma de México; G. Morgan and P. Gegick, New Mexico
Museum of Natural History; and M. Hafner, Louisiana State
University Museum of Natural Science. Thanks to D. J. Hafner, M.
S. Hafner, J. Merritt, V. Sánchez-Cordero, and 2 anonymous
reviewers for their critical evaluations of this manuscript. Special
thanks to L. León y Z. Ávila of the Colección de Mamı́feros del
Museo de Zoologı́a ‘‘Alfonso L. Herrera,’’ Facultad de Ciencias,
Universidad Nacional Autónoma de México, for their help in
cataloging specimens.
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APPENDIX I
Specimens used in the analysis of phylogenetic relationships
of Xerospermophilus spilosoma perotensis. Specimens are
listed alphabetically by taxon and locality; geographic
coordinates, elevation, catalogue number, sequenced genes,
and GenBank numbers are provided. Specimens are housed in
the following museums: Colección Nacional de Mamı́feros,
Instituto de Biologı́a, Universidad Nacional Autónoma de
México (CNMA); Cornell University DNA collection (CU;
samples from CU are followed by the collector’s field number
in parentheses); Cornell University DNA Sample Number (S);
Los Angeles County Museum of Natural History (LACM);
Louisiana State University Museum of Natural Science
(LSUMZ); Colección de Mamı́feros del Museo de Zoologı́a
‘‘Alfonso L. Herrera,’’ Facultad de Ciencias, Universidad
Nacional Autónoma de México (MZFC); New Mexico
Museum of Natural History (NMMNH); and the Museum of
Southwestern Biology, University of New Mexico (MSB).
Numbers in parentheses in boldface type before localities
indicate localities for specimens of Xerospermophilus mapped
in Fig. 1.
Callospermophilus lateralis.—United States: California, Mono
Co., Sweetwater Mountains; Sweetwater Canyon, Nugent Cabin,
38.469445, 119.265487, 2,100 m, LACM 85487, 12S ¼ AY227530,
IRBP ¼ AY227586.
Cynomys gunnisoni.—United States: Arizona, Apache Co.,
Petrified Forest National Park, 34.909, 109.806, 1,641 m, S 75
(73), Cytb ¼ AF157923; CU 82 (WA1), Cytb ¼ AF157930.
December 2012 FERNÁNDEZ—SYSTEMATICS OF XEROSPERMOPHILUS PEROTENSIS
Cynomys leucurus.—United States: Utah, Uintah Co., 8 km E
Jensen on Highway 40, CU 1 (EY 1138), 40.369, 109.240, 1,689 m,
Cytb ¼ AF157838; 12S ¼ AY227528, IRBP ¼ AY227584. Utah,
Uintah Co., 11 km NW Bonanza on Highway 45, CU 2 (EY1137),
40.094, 109.269, 1,572 m, Cytb ¼ AF157879.
Cynomys ludovicianus.—United States: Nebraska, Omaha Zoo CU
38 (1A), Cytb ¼ AF157890; CU 41 (4A), Cytb ¼ AF157892;
collection locality not available, CU 1 (EY 1138), IRBP ¼ AY227584.
Cynomys mexicanus.—Mexico: Nuevo León, Ejido El Tokio, 18
km E Highway 57 on Highway 58, 24.6, 100.2, 1,891 m, CU 101
(EY 1180), Cytb ¼ AF157841; CU 102 (EY 1181), Cytb ¼ AF157842.
Cynomys parvidens.—United States: Utah, Kane Co., Bryce
Canyon National Park, 1 km from Visitor Center, 37.58, 112.18,
2,466 m, CU 74 (BCU 1), Cytb ¼ AF157922; Utah, Kane Co., Bryce
Canyon National Park, 20 m from boundary, 37.58, 112.18, 2,466 m,
CU 81 (BC1), Cytb ¼ AF157929.
Ictidomys mexicanus mexicanus.—Mexico: México, Parque
Nacional Zoquiapan, 15 km SW Rio Frı́o, 19.3, 98.6, 2,980 m,
CU 108 (EY 1210), Cytb ¼ AF157848.
Ictidomys parvidens.—United States: New Mexico, Chaves Co.,
Eastern New Mexico University, Roswell, West Wells and University
Street, 33.39, 104.52, 1,097 m, MSB 135244, Cytb ¼ JX047304, 12S
¼ JX047294, GHR ¼ JX047262; Mexico: Nuevo León, 3 km NE
Apodaca, approximately 23 km NE Monterrey, 25.80, 100.16, 408
m, CU 111 (EY 1197), Cytb ¼ AF157852; CU 112 (MVA 105), Cytb
¼ AF157853.
Ictidomys tridecemlineatus.—United States: Kansas, Finney Co.,
Garden City, 37.9, 100.8, 866 m, CU 13 (EY 1147), Cytb ¼
AF157870; CU 14 (EY 1148), Cytb ¼ AF157877; collection locality
not available (from personal collection of R. L. Honeycutt), H 2147,
12S ¼ U67290, IRBP ¼ AF287278; South Dakota, Union Co., 1 mile
N, 1.5 miles W Junction City, 42.800, 96.815, 377 m, LSUMZ
10692, Cytb ¼ JX047305, 12S ¼ JX047295, GHR ¼ JX047260; South
Dakota, Clay Co., 3.5 miles N, 3.5 miles E Vermillion, 42.829,
96.857, 376 m, LSUMZ 10728, Cytb ¼ JX047306, 12S ¼ JX047296,
GHR ¼ JX047261, IRBP ¼ JX047282.
Xerospermophilus mohavensis.—United States: (1) California, San
Bernardino Co., 9 miles NNE Johannesburg, 35.473, 117.589, 1,075
m, MSB 40496, 12S ¼ JX047290, GHR ¼ JX047273, IRBP ¼
JX065593; MSB 40503, Cytb ¼ JX047298, 12S ¼ JX047291, GHR ¼
JX047272, IRBP ¼ JX047274.
1439
Xerospermophilus spilosoma perotensis.—Mexico: (2) Puebla,
Tepayahualco, 19.490, 97.489, 2,336 m, CNMA 37253, Cytb ¼
AF157948, 12S ¼ JX047289, GHR ¼ JX047271, IRBP ¼ JX047277;
CNMA 37254, Cytb ¼ AF157840, JX047302, 12S ¼ JX047286, GHR
¼ JX047268, IRBP ¼ JX047279; Veracruz: Municipality of Perote, 3
km S El Frijol Colorado, 19.572, 97.383, 2,435 m, MZFC 11089,
Cytb ¼ JX047303, 12S ¼ JX047287, GHR ¼ JX047269, IRBP ¼
JX047278; Municipality of Perote, 5 km W Perote, 19.587, 97.330,
2,400 m, MZFC 11090, Cytb ¼ JX047301, 12S ¼ JX047288, GHR ¼
JX047270, IRBP ¼ JX065593.
Downloaded from https://academic.oup.com/jmammal/article-abstract/93/6/1431/910757 by UNAM user on 12 June 2019
Xerospermophilus spilosoma cabrerai.—Mexico: (3) San Luis
Potosı́, 10 miles S Villa de Ramos, 22.666, 101.953, 2,200 m,
NMMNH 3651, Cytb ¼ JX047299, 12S ¼ JX047283, GHR ¼
JX047263, IRBP ¼ JX065594.
Xerospermophilus spilosoma marginatus.—United States: (4) New
Mexico, Bernalillo Co., 8 km W Albuquerque, 35.084, 106.738,
1,631 m, LSUMZ 01, 12S ¼ JX047285, GHR ¼ JX047264, IRBP ¼
JX047276; LSUMZ 05, Cytb ¼ JX047300, 12S ¼ JX047284, GHR ¼
JX047265, IRBP ¼ JX047275. (5) Kansas, Finney Co., 13 km S, 2 km
E Holcomb, 37.872, 100.964, 893 m, CU 3 (EY1142), Cytb ¼
AF157885; CU 6 (EY1146), Cytb ¼ AF157911.
Xerospermophilus spilosoma pallescens.—Mexico: (6) Durango, 4
km E Ceballos, 26.523, 104.089, 1,117 m, CU 105 (EY 1195), Cytb
¼ AF157845; Durango, Ejido La Flor, 20 km E Ceballos, 26.524,
103.929, 1,146 m, CU 106 (EY 1193), Cytb ¼ AF157846.
Xerospermophilus tereticaudus neglectus.—United States: (7)
Arizona, Pima Co., Tucson, 32.221, 110.926, 917 m, MSB 86022,
12S ¼ JX047292, GHR ¼ JX047266, IRBP ¼ JX047280; MSB 92638,
Cytb ¼ JX047297, 12S ¼ JX047293, GHR ¼ JX047267, IRBP ¼
JX047281; Arizona, Pima Co., 18 km W Tucson, Ryan Field, 32.223,
111.116, 735 m, CU 91 (EY 1169), Cytb ¼ AF157940; CU 92 (EY
1167), Cytb, ¼ AF157941.
Poliocitellus franklinii.—United States: Nebraska, Omaha Zoo CU
42 (1A), Cytb ¼ AF157893; CU 43 (2A), Cytb ¼ AF157894.
Urocitellus townsendii idahoensis.—Collection locality not
available, CU 86 (EY 1062), Cytb ¼ AF157949.
Urocitellus townsendii.—Collection locality not available, CU 87
(EY 1064), Cytb ¼ AF157938.