EVOLUTIONARY GENETICS AND PHYLOGEOGRAPHY OF
TASSEL-EARED SQUIRRELS (SCIURUS ABERTJ)
TRIP LAMB, THOMAS
R. JONES, AND
PETER
J.
WETTSTEIN
Department of Biology, East Carolina University,
Greenville, NC 27858 (TL)
Biology Department, Grand Canyon University,
Phoenix, AZ 85017 (TRJ)
Departments of Surgery and Immunology, The Mayo Foundation,
Rochester, MN 55905 (PJW)
The tassel-eared squirrel (Sciurus aherti) is confined to a montane archipelago of mixed
conifer forests in the American Southwest. Explanations for its fragmented distribution
vary, invoking historical scenarios that stress late-Pleistocene vicariance, dispersal, or some
combination thereof. To test among these hypotheses, we examined the phylogeography of
S. aberti, as determined by variation in mtDNA restriction sites among 22 populations
sampled range-wide. Genetic distance and maximum-parsimony analyses revealed three
distinct lineages of mtDNA, which in turn form two major phylogeographic assemblages;
eastern (Mexico; New Mexico-Colorado-Utah) and western (Arizona-southwestern New
Mexico). Comparisons between the maximum-parsimony tree and an area cladogram of
regional mountain ranges showed marked topological discordance, dismissing late-Pleistocene vicariance as a principal phylogeographic factor. Certain mtDNA data support the
post-Pleistocene dispersal hypothesis, in which squirrels dispersed northward in conjunction
with the rapid range expansion of ponderosa pines (Pinus ponderosa). However, divergence
levels observed between assemblages (1.8%) also suggest a significant, underlying vicariant
event responsible for major separation of lineages during the early Pleistocene. Thus, the
evolutionary genetics of S. aberti has been influenced profoundly, and perhaps repeatedly,
by climatic change during the Pleistocene.
Key words: Sciurus aberti, tassel-eared squirrel, mitochondrial DNA, phylogeography,
biogeography.
Some 26 species of nonvoIant forest
mammals are confined to a montane archipelago of mixed-conifer forests in the
American Southwest, including Arizona,
New Mexico, Colorado, and southern Utah
(Lomolino et aI., 1989). Explanations for
their present distribution patterns vary, invoking historical scenarios that stress vicariant events, dispersal events, or some combination of these two processes (Davis and
Brown, 1989; Lomolino et aI., 1989;
McKee, 1941; Patterson, 1984; Sullivan,
1985). For example, all three hypotheses
have been offered to account for the fragmented distribution of the tassel-eared
squirrel (Sciurus aherti), a prominent speJOllnza/ of Mamma/o8Y, 78{ I): 117-133, 1997
cies in conifer forests of the Rocky Mountains Disjunct populations of S, aberti were
traditionally considered to be vicari ant relicts of a widespread, essentially continuous
distribution within a vast Pleistocene coniferous forest (McKee, 1941). Increasing
aridity during the Holocene caused the coniferous forest and its contingent of squirrels to fragment, forming remnant montane
populations (McKee, 1941). A competing
view suggests that post-Pleistocene dispersal, including extensive migration across unsuitable habitat, accounts for much of the
present distribution of S. aberti (Davis and
Brown, 1989). A third view holds that there
was an inceptive vicariant component from
117
lIB
JOURNAL OF MAMMALOGY
which major dispersal ensued during the
Pleistocene and continued post-Pleistocene
to the present (Lomolino et aI., 1989).
General correlative support for the two
(largely compatible) dispersal hypotheses is
provided by significant relationships between richness of mammalian species and
current isolation of montane habitats, as
well as between species richness and area
(bOlh P < 0.01; Lomolino et aI., 1989).
These correlations can neither support nor
refute an underlying vicariant component,
which also may have influenced the montane fauna of the region. An alternative assessment involves examining genetic structure of populations, whose pattern and magnitude may reveal clues to historical demographic and biogeographic events. In
particular, variation among mitochondrialDNA (mtDNA) haplotypes can be used to
associate intraspecific phylogenies with
geographic distribution. Variation in mtDNA examined in this context forms the
basis of intraspecific phylogeography,
which can be broadly defined as the processes that govern geographic distributions
of genealogical lineages (A vise et aI.,
1987). A phylogeographic approach often
allows the detection of, and distinction between, past demographic conditions (dispersal) and historical environmental disjunctions (vicariance). Here we report the
phylogeography of S. aberti based on variation of mtDNA detected by restriction-site
analysis. We compare phylogeographic
structure in mtDNA of S. aberti with competing biogeographic predictions based on
late-Pleistocene vicariant versus dispersal
events. In this respect, our survey provides
important baseline data regarding a genetic
approach to the biogeographic history of
the montane mammalian fauna in the
American Southwest. The mtDNA lineages
uncovered in our survey also allow comparisons to subspecific designations for S.
aberti. Our data complement and extend recent molecular surveys by Wettstein et al.
(1994, 1995), which examined variation of
mtDNA to establish a temporal framework
Vol. 78, No.1
for the evolution of the major histocompatibility complex and T-cell receptor genes in
S. aberti (Wettstein and States, 1986a,
1986b; Wettstein et aI., 1990).
A highly specialized herbivore, the tassel-eared squirrel feeds largely, if not entirely, on the seeds and inner bark of ponderosa pine (Pinus ponderosa) and associated hypogeous fungi (Hall, 1981; Keith,
1965). The dietary selectivity of the squirrel
is underscored by preferences for particular
target trees that exhibit significantly lower
levels of oleoresin monoterpenes and reduced rates of xylem flow (Snyder, 1992).
Squirrels also rely on pines for cover, and
although individuals occasionally are observed in other habitats, reproducing populations are restricted to forests of ponderosa pine (Hall, 1981; Keith, 1965). The
close ecological ties of squirrels to host
trees are clearly revealed in their discontinuous, although largely coincident, distributions in montane settings from southern
Wyoming to northern Durango, Mexico. It
should be noted, however, that S. aberti is
absent from the majority of ponderosa pine
forests, which are widespread throughout
western North America (Little, 1971). The
discrepancy in respective ranges indicates
that this herbivore-host relationship does
not involve reciprocal dependency.
Morphological variation among disjunct
populations of S. aberti is evident, and nine
geographic races have been described by
differences in cranial features and coloration of pelage. In the most recent taxonomic
revision, Hoffmeister and Diersing (1978)
dismissed the systematic value of coloration
of pelage and concluded that S. aberti comprised six subspecies, based on multivariate
analysis of external and cranial measurements. We made a special effort to secure
representatives of each of the classically defined and currently recognized geographic
races.
MATERIALS AND METHODS
We collected 95 squirrels, representing 22 locales throughout the range of the species (Table
February 1997
119
LAMB ET AL.-PHYLOGEOGRAPHY OF SClURUS ABERTl
TABLE l.~Sample locales, mountain ranges, sample sizes, and subspecies of the tassel-eared
squirrel (Sciurus aberti). Locales are depicted in Fig. 1 and detailed in Appendix /.
State and
locality number
Mountain range
n
Subspecies
(fanner subspecies)
COLORADO
1
2
Medicine Bow
Pike's Peak
10
ferreus
ferreus
NEW MEXICO
3
4
5
6
7
8
9
10
11
12
Cimarron
Sangre de Cristo
San Juan
Jemez
Mount Taylor
Zuni
Datil
San Mateo
Mogollon Mountains
Pinos Altos
4
3
4
3
3
5
2
2
1
4
ferreus
ferreus
aberti (mimus)
aberti (mimus)
aberti (mimus)
abem' (mimus)
aberti (mimlls)
abem'
aberti
aberti
UTAH
13
Elk Ridge
aberti (navajo)
ARIZONA
14
15
16
17
18
19
20
Kaibab Plateau
Coconino Plateau
San Francisco
Mogollon Plateau
Sierra Ancha
Chuska
Defiance Plateau
9
6
4
4
10
5
kaibabensis
aberti
aberti
aberti
aberti
chllscensis
chllscellsis
CHIHUAHUA
21
22
Sierra Madre Occidental
Sierra Madre Occidental
1; Fig. 1; Appendix I). Samples of liver were
stabilized in MSB-EDTA buffer (Lansman et aI.,
1981) within 10 min of collection and held at
4°C for 2-7 days before processing. About 1 g
of liver was homogenized in fresh MSB-EDTA
buffer, from which closed-circular mtDNA was
isolated by CsCI-gradient centrifugation (Lansman et aI., 1981). Purified samples of mtDNA
were digested separately with the 18 informative
endonucleases listed in Table 2. Samples also
were digested with Bam HI, but this enzyme
proved uninformative (Le., generating either one
or no restriction fragments), and these data were
not included for analysis. Digestion fragments
were end-labeled with 35S-dNTPs, separated
through 1-1.8% agarose gels, and revealed by
autoradiography. Restriction-site changes involving small fragments (200-600 bp) were
confirmed using 2.5-3.5% Nusieve GTG aga-
12
barberi
dllrallgi
rose (FMC Bioproducts, Rockland, ME) or 5%
polyacrylamide gels. Sizes of fragments were
determined by comparison to a l-kb standard
(Bethesda Research Labs, Gaithersburg, MD) or
the Gelmarker ladder (Research Genetics,
Huntsville, AL).
Distinct restriction profiles for each endonuclease were identified by an uppercase letter
code, with "e" designating the most common
profile. Each squirrel was assigned a composite
genotype of mtDNA (its haplotype or clonal
designation) compiled from the restriction profiles across all enzymes. Size polymorphism was
negligible, and differences in patterns of fragments could be readily attributed to transformations involving simple losses or gains of specific restriction sites. Inferred site data for the
genotypes were assembled in a presence-absence matrix, and estimates of nucleotide-se-
JOURNAL OF MAMMALOGY
120
Vol. 78, No.1
:.
'- ..
"-'I
I
•
,"
1
/
~ i~
, ,.
(fe)
13 (ab)
19 (ch)
20 (ch)
,
(ka) 14
(ab)
(ab)
(ab) 1
(ab) 18
(ab) 9
(ab) 11
(ab) 10
(ab) 12
(fe)
,
, .e l
oto
..... -iJ- r·- -.- ...... _-'
.,
(fe)
(ab)
(fe)
3
5
4
6
(ab)
7
(ab)
8
(ab)
.
"l!
------~------21
~~
JL-~Y:'--\ 22
(du)
/
,- 'ill
i
-,j.
'"'"\..
\
.",
ID
)
FIG. l.--Collection locales superimposed on a distribution map of ponderosa pine modified from
Little (1971). Numbers correspond to the locales listed in Table 1. Subspecific designations for each
locale, based on Hoffmeister and Diersing (978), are encoded as follows: ab = aberti; ba = barberi;
ch = chuscensis; du = durangi; fe = ferreus; ka = kaihabensis. Cross marks in New Mexico and
Arizona represent 35°N IOSOW and 35°N llOoW, respectively.
February 1997
LAMB ET AL.-PHYLOGEOGRAPHY OF SC1URUS ABERT!
121
TABLE 2.-Description and distribution of mtDNA haplotypes observed in Sciurus aberti. Letters
of the composite genotypes refer to digestion profiles produced by the following endonucleases (from
left to right): Ava!, AvaIl, Bell, BglI, BgUI, BstEll, CIa!, Eeo01091, EeoRI, EeoRV, HhaJ, Hindlll,
Pst!, Pvull, Saci, Spel, Stul, and XbaJ.
Haplotype
a
CCCCCCCCCCCCCCCCCC
b
CCCCCCCCCBCCCCCCCC
CCCCBCCCCCCCCCCCCC
c
Mountain range
(locality code)
Composite genotype
Datil (9)
Pinos Altos (12)
San Mateo (10)
San Francisco (16)
Sierra Ancha (18)
San Mateo (10)
Pinos Altos (12)
Mogollon Mountains (1 I)
Mogollon Plateau (17)
San Francisco (16)
Coconino Plateau (15)
Mogollon Plateau (17)
San Francisco (16)
Chuska (19)
Defiance Plateau (20)
e
CCCCCCCCCCCCCCCBCC
CCBCCCCCCCCCCCCCCC
f
CCCCDCCCCCCCCCCCCC
g
CCCCCCCCCCCCCCCACC
h
CCCCCCCCCCCDCCCCCC
Mogollon Plateau (17)
San Francisco (16)
Coconino Plateau (15)
j
CCCBCCCCCDCDCCCCCC
CBDCCBCBCFCCCBCECC
Kaibab Plateau (14)
Chuska (19)
Defiance Plateau (20)
Zuni (8)
Chuska (19)
d
k
BBDCCBCBCFCCCBCECC
CBDCCBCBCFCCCBCECC
Jemez (6)
Mount Taylor (7)
m
n
CBDCCBCBBFDCCBCDCC
CBDCCBCBCFCBCBCECC
Elk Ridge (l3)
San Juan (5)
0
p
CBECCACBCFCCCBCECC
CBECCBCBCFCCCBCECC
Sangre de Cristo (4)
Sangre de Cristo (4)
Cimarron (3)
Pike's Peak (2)
q
CBECEBCBCFCBCBCECC
Cimarron (3)
c
CBHCCBCBCFCCCBCECC
,
CBFCCBCBCGCCCCBECC
Medicine Bow (1)
Pike's Peak (2)
Sierra Madre Occidental (21.22)
u
DBFCCBCBCGCCCCBECC
CBFCCACBCGCCCCBECC
Sierra Madre Occidental (21)
Sierra Madre Occidental (21)
quence divergence (P) between genotypes of
mtDNA were calculated by the site approach of
Nei and Li (1979).
Haplotypes were clustered by neighbor-joining analysis (Saitou and Nei, 1987), and alternatively. by using the unweighted pair-group
n
2
3
1
2
5
3
2
1
4
9
3
2
5
2
3
3
1
4
2
3
3
1
1
7
10
2
Species
represented
aberti
aberti
aberti
aberti
aberti
aberti
aberti
aberti
aberti
aberti
aberti
aberti
aberti
chuscensis
chuscensis
aberti
aberti
aberti
kaibabensis
chuscensis
chuscensis
aberti
chuscensis
aberti
aberti
aberti
aberti
ferreus
/erreus
ferreus
ferreus
ferreus
ferreus
ferreus
barber;
durangj
barberi
barberi
method using arithmetic means (UPGMA), using p-values as input matrix to the NJOIN and
SAHN programs. respectively, of NTSYS-pc
(Rohlf, 1992). In addition, maximum-parsimony
analysis of the restriction-site data was conducted using the branch-and-bound search procedure
JOURNAL OF MAMMALOGY
122
of PAUP (Swofford. 1993), with presence-absence of sites as character states. Although general statements exist regarding putative relationships among North American sciurids (Allen,
1915; Burt, 1960), no comprehensive cladistic
analysis has been reported. In the absence of a
reliable phylogeny, we selected two species,
Sciurus niger and S. carolinensis, as potential
outgroup taxa. A bootstrap analysis involving
1,000 iterations (Bootstrap option in PAUP) was
conducted to estimate confidence limits for the
topological patterns revealed by parsimony analysis.
RESULTS
The IS-enzyme assay generated a total of
81 restriction sites (X = 70/individual) and
identified 21 haplotypes of mtDNA (Table
2; Appendix II). Geographic localization
was an evident feature of distribution of
haplotypes; 13 of the 21 clones were observed only at single locales, and in effect,
characterized populations of squirrels inhabiting specific mountain ranges (Table 2).
Perhaps the best example of such a diagnostic haplotype involved clone i, which
appears restricted to the Kaibab Plateau and
was found in all nine squirrels sampled
there. The more geographically wide-spread
haplotypes (e.g., a, h, p, r) were distributed
across I) the Mogollon Plateau of central
Arizona and southwestern New Mexico, or
2) the eastern front of the Rocky Mountains
from northern New Mexico to northern
Colorado. Both geographic settings support
nearly continuous stretches of ponderosa
pine forests (Little, 1971).
The neighbor-joining tree (Fig. 2) revealed two major genetic groupings, henceforth called the eastern and western assemblages, which are separated by an average
sequence divergence of p = 0.0183. The
eastern assemblage contains 12 haplotypes
and encompasses a much larger area, ranging from northern Colorado to southern
Chihuahua. Geographic structure is evident
within the assemblage, which can be partitioned into three well-defined subunits. The
most genetically distinct of these is the
Mexican subunit, confined to the Sierra Ma-
Vol, 78, No.1
dre Occidental and differing from the other
two subunits at p = 0.0079. A second subunit is rather broadly distributed from the
Sangre de Cristo Mountains of northern
New Mexico, north through Colorado along
the eastern front of the Rocky Mountains
(sample locales 1, 2, 3, and 4). The third
subunit lies west of the Rio Grande Valley
in a region roughly defined by the Jemez,
San Juan, Zuni, Abajo, and Chuska ranges
(sample locales 5, 6, 7, 8, 13, 19, and 20).
The western assemblage, comprising
nine haplotypes, is considerably more homogeneous both genetically and geographically. Seven haplotypes (a-f, h) are variously represented in the Datil, San Mateo,
Pinos Altos, and Mogollon Mountains of
southwestern New Mexico, as well as in
Arizona along the Mogollon Plateau north
to the Coconino Plateau. As noted previously, the Kaibab Plateau is characterized
by an eighth unique, although closely related, haplotype (i). The ninth western haplotype (g) appears restricted to the Chuska
Mountains, where it was observed in roughly equivalent frequency with two eastern
haplotypes, j and k, the latter of which also
appears restricted to the Chuskas.
Both eastern and western assemblages
were also resolved in the UPGMA analysis,
as were the three subunits of the eastern
assemblage. The branching topology for the
UPGMA phenogram differed only slightly
from that of the neighbor-joining tree with
respect to hierarchical arrangements within
both subunits and, therefore, is not illustrated.
Maximum-parsimony analysis of 31 variable restriction sites (Appendix II) resulted
in a single most-parsimonious tree involving 34 steps, with a relatively high consistency index of 0.870, excluding uninform_
ative characters. The digestion-fragment
profiles between S. aberti and the outgroup
taxa (S. niger and S. carolinensis) were so
distinct that it was not possible to interpret
particular changes of sites across species.
With so little phylogenetic information provided by either S. niger or S. carolinensis,
February) 1997
LAMB ET
AL.~PHYLOGEOGRAPHY
r
OF SClURUS ABERT!
123
e (15 ,16)
a (9,10,12,16,18)
/(16,17)
Western
h (15,16,17)
I
i (14)
g (19,20)
d(17)
b (10)
c(ll,12)
j (8,19,20)
k (19)
r-
1 (6,7 )
m (13)
Eastern
n (5)
q (3)
0(4)
P (2,3,4)
r (1,2)
t(21)
~
s (21,22)
u (21)
Scale: - - - - - is approximately equal to the distance of 0.00163
FIG. 2.-Neighbor-joining tree of haplotypes of mtDNA for Sciurus aberti. Numbers in parentheses
are collection locales represented by haplotypes (Table 2).
we concluded that their role as outgroups
(with respect to the restriction-site data)
was inappropriate. Thus, the maximum-parsimony tree was rooted mid-point in the absence of an outgroup. The maximum-parsimony tree depicts the same major groupings (assemblages and subunits) resolved
by both genetic-distance analyses (Fig. 3).
The eastern versus western clades differ by
nine unique restriction-site changes and are
supported by a bootstrap value of 100%.
DISCUSSION
Biogeographic inferences from phylogeography of squirrels.-Our discussion
of biogeography requ·ires an important initial assumption; the historical distribution
of S. aberti was closely tied with that of
P. ponderosa. All available data currently
support this association, although ecological studies of S. aberti have been limited
to the United States, where montane-co-
JOURNAL OF MAMMALOGY
124
a
----i===
r
Vol. 78, No.1
(8,9, 10, 12, 16, 18)
h (IS, 16, 17)
i (14)
d
(17) 16)
e (IS,
1 - - - f (16, 17)
1 - - - - g (19, 20)
Western
'--_ _ C (11, 12)
L -_ _ _ _
r---
b
(10)
j
(8, 19, 20)
I - - - k (19)
I (6, 7)
m
'--_ _ n
53
100
(13)
(5)
0
(4)
q
(3)
Eastern
p (2, 3,4)
r
82
(I, 2)
S (21,22)
t (21)
U
(21)
FIG. 3.-Maximum-parsimony tree of haplotypes of mtDNA for Sciurus aberti. Mid-point rooting
was used in the absence of an appropriate outgroup. Numbers above the branches indicate the proportion of bootstrap replicates that supported the depicted groupings. Numbers in parentheses are
collection locales (Table 2).
niferous forests are dominated by ponderosa pines (Hall, 1981; Keith, 1965). No
comparable data exist for S. aberti in Mexico, where Madrean, montane-coniferous,
forests are often of mixed-species composition (Styles, 1993). Nonetheless, in the
absence of data to the contrary, a reconstruction of the evolutionary history of the
squirrels requires a biogeographic perspective on ponderosa pines.
Although much remains to be understood
about the Pleistocene distribution of ponderosa pines. it is clear that this species was
absent from the northern part of its current
range. Among data from Wisconsinan-aged
middens of packrats in Arizona and New
Mexico, ponderosa pines are recorded only
from the San Andres Mountains in southcentral New Mexico (ca. 14,900 years
ago-Van Devender, 1990a) and in the
Santa Catalina Mountains near Tucson, Arizona (ca. 18,000-11,900 years ago; Van
Devender, I 990b). Although data are lacking for many of the mountain islands currently supporting ponderosa pines, the data
on packrat middens clearly demonstrate that
pine forests did not extend north of the 35th
parallel during the Wisconsinan glaciation
February 1997
LAMB ET AL.-PHYLOGEOGRAPHY OF SC1URUS ABERTl
(Betancourt et aI., 1990; Van Devender,
1990a, I 990b ).
The earliest definitive records of ponderosa pine north of the 35th parallel include
10,400 years ago from the Mogollon Plateau (Anderson, 1993) 10,300 years ago
from the Abajo Mountains, Utah (Betancourt, 1990),9,100 years ago from the eastern Grand Canyon (Cole, 1990), and 8,300
years ago from Chaco Canyon, New Mexico. Once established, however, the pines
soon became abundant, dominating the
Chaco Canyon site by ca. 6,700 years ago
and the Abajo Mountains by ca. 7,200 years
ago (Betancourt, 1990). It is apparent that
ponderosa pine experienced a rapid expansion in the Holocene from the south, and
although a refugium has yet to be confirmed (Anderson, 1993), the species likely
was "an important component of montane
communities in the highlands south of
35°[N], and probably was most prevalent in
the Sierra Madre Occidental" (Betancourt
et aI., 1990:443). Ponderosa pines presumably reached their present distribution via
long-distance dispersal or island hopping
during the early Holocene (Betancourt et
aI., 1990). Genetic data for Great Basin
populations of Douglas fir (Pseudotsuga
menziesii) support a similar pattern of rapid
post-glacial expansion northward (Betancourt et aI., 1991; Schnable et aI., 1993).
Thus, the paleo-distribution of ponderosa
pines offers little support for McKee's
(1941) scenario in which current pines and
populations of squirrels are considered vicariant remnants of a vast, late-Pleistocene
pine forest. Indeed, the data from middens
suggest that about one-third of the present
range was uninhabitable during the Wisconsinan glaciation. Additional evidence
against the role of post-Pleistocene vicariance in shaping phylogeographic structure
in S. aberti is apparent when the maximumparsimony tree (Fig. 3) is compared to a
geographical, or area cladogram (sensu
Kluge, 1988). Sullivan (1994) espoused the
utility of this approach for testing vicariance hypotheses for montane mammals in
125
c
~
A
E
1~
------- --+- 2300 m
----- --------------- --- +- 1800 m
2 ~ ---
3~=+-1500m
A
BED
c
1500 m
FIG. 4.-Diagrammatic representation of postWisconsinan subdivision of montane conifer forests and the geographical c1adogram constructed
from the sequence of fragmentation. 1 = approximate lower elevation, 2,300 m, of montane
(Petran and Madrean) conifer forest at present
(Pase and Brown, 1994); 2 = lower limit of
montane conifer forest of 1,800 m at an arbitrary
early Holocene time; 3 = approximate lower
limit, 1,500 m, of montane conifer forest during
late Wisconsinan (Betancourt et aI., 1990; modified from Sullivan, 1994).
the American Southwest. The area c1adogram that Sullivan (1994) generated for this
region depicts the fragmentation sequence
of biotic communities from the late Wisconsinan to the present, thereby providing
a hypothesis for genetic differentiation
among populations of S. aberti sundered by
the fragmentation of contiguous pine forests.
Figure 4 illustrates the method for constructing an area c1adogram for a series of
hypothetical mountain ranges. Range A,
separated from other ranges by the lowest
elevation, is the first to become isolated and
thus forms the lowest branch of the cladogram. Range C is the terminal taxon, the
last to sever connections to other ranges.
However, ranges Band E are unresolved in
the cladogram (despite the fact that they
represent different geographic areas) because both experienced isolation at the
same elevation. Thus, it is not possible to
distinguish cladistically between them; such
unresolved nodes cannot be compared using the criteria outlined by Kluge (1988).
126
JOURNAL OF MAMMALOGY
Using this general approach, we examined
topographical maps (United States Geological Survey I :500,000 and I: 100,000) of
the region to identify the highest elevational
contours connecting mountains inhabited
by S. aberti. The result was an area cladogram depicting the mountain ranges encompassed by the current distribution of the
squirrels (Fig. SA).
Before interpreting the area cladogram,
we offer two caveats regarding our vicariance model and null models for montane
biogeography in general (e.g., Sullivan,
1994). First, it is nearly impossible to avoid
unresolved nodes in any vicariance model
for montane organisms. If the elevation limits of biotic communities are altered by climatic change, then coincident fragmentation of geographically disparate mountain
islands is inevitable. Second, our vicariance
model makes biological assumptions that
undoubtedly are violated, most notably that
biotic communities are predictable at given
elevations. Elevationallimits for both modern and paleo-communities are approximations at best, as local edaphic and microclimatic conditions often support communities
that would not otherwise be predicted by
elevation (Betancourt et aI., 1990; Pase and
Brown, 1994). For example, at ca. 34°15'
and 2,100 m, Rocky Mountain-montane-conifer forest occurs on and below the Mogollon Plateau, but grassland dominates the
Plains of San Agustin, New Mexico, which
in tum is surrounded by montane-conifer
forests of the Rocky Mountains at slightly
higher elevations. In other instances, sites
separated by low elevations might actually
be connected via canyons that support communities associated with higher elevations.
Thus, sites that are connected or separated
in our area cladogram by objective criteria
might not conform with apparent limits imposed by elevation. However, none of this
precludes resolution of these conflicts with
additional evidence (sensu Kluge and Wolf,
1993),
How do these caveats temper an interpretation of our vicariance hypothesis? The
Vol. 78, No.1
distribution of S. aberti encompasses several mountain ranges whose montane-conifer forests would have been isolated at
about the same elevation and time period,
yielding an area cladogram with several unresolved nodes (Fig. Sa). As a result, we
cannot compare on a fine scale, i.e., range
by range, the level of concordance between
the area cladogram and the phylogeny from
maximum-parsimony analysis. In broadscale comparison, however, the area cladogram and maximum-parsimony tree display
substantial topological discordance (Fig. 5).
First, the maximum-parsimony tree reveals
two major assemblages of mtDNA, partitioned east and west, but there is nothing in
topology of the area cladogram that predicts
an east-west split. Moreover, terminal lineages of the maximum-parsimony tree such
as the haplotypes Kaibab Plateau and Sierra
Ancha should form basal branches accroding to our geographical hypothesis. Thus,
our mtDNA data falsify the hypothesis predicted by our model and indicate that postPleistocene vicariance was not a major factor in the evolutionary genetics of S. aberti.
If the paleo-distribution of ponderosa
pines offers little support for post-Pleistocene vicariance in S. aberti, it strongly corroborates the role of dispersal. Davis and
Brown (1989) argued that S. aberti dispersed across woodland (non-ponderosa
pine) barriers or along corridors in a northward expansion roughly contemporaneous
with that of the island-hopping pines during
the late Wisconsinan-early Holocene. Lomolino et al. (1989) offered strong support
that similar dispersal across woodland barriers at this time played a central role in
determining geographic distribution of several montane-forest mammals in the American Southwest. These studies suggest that
many of the populations of squirrels in OUf
survey derive from a substantive northward
wave of dispersal. What aspects of the
mtDNA data are consistent with, or have
bearing on, a dispersal-dominated history
for S. aberti in its northern range? Diversity
of haplotypes does appear greater below
LAMB ET AL.-PHYLOGEOGRAPHY OF SClURUS ABERTJ
February J997
127
> 2300 m
1980 m
1830 m
1525 m
1220-1300m
1000 m
ad
bf
cg
a
s
h
i
e
t
u
o
p
q
r
j
k
n
I
m
b
FIG. 5.-a) Geographical cladogram illustrating the sequence of fragmentation and isolation of
montane (Petran and Madrean) conifer forest on mountains within the range of Sciurus aberti. The
nodes indicate the highest elevation that separates mountain clades. Abbreviations include: S = Sierra;
S. Madre = Sierra Madre Occidental; Jemez = Jemez Mountains, San Juan Mountains, Ahajo Mountains-Elk Ridge; Sangre = Sangre de Cristo Mountains; SFP/MP = San Francisco Peaks region and
western Mogollon Plateau; Mogrrular = Mogollon and Tularosa mountains. Our genetic analysis did
not include samples from the Black Range, Magdalena Mountains, or White Mountains; they are
included here for completeness. b) Maximum-parsimony tree of haplotypes from Fig. 3 collapsed
into regional geographies: hap!otypes a-d, f, g = Chuskas, Mogollons, Sierra Anchas, Mogollon
Plateau, San Francisco Peaks area, Datils, Pinos Altos, San Mateos; II = Mogollon Plateau, Coconino
Plateau; i = Kaibab Plateau; e = San Francisco Peaks area, Coconino Plateau; s, t, U = Sierra Madre
Occidental; 0, p, q, r = Sangre de Cristos, Medicine Bow Range; j, k, II = Chuskas, Zunis, San
Juans; { = Jemez, Mount Taylor; III = Elk Ridge.
128
JOURNAL OF MAMMALOGY
36°N than above (14 haplotypes versus seven) despite a comparable number of sampling locales (11 versus 10). This distribution pattern of haplotypes is consistent with
a recent, rapid, range expansion, where effective population size (Ne ) and thus diversity of haplotypes of the dispersal contingent are expected to be reduced proportionally.
The geographic distribution of certain
haplotypes also allows us to postulate the
direction of dispersal in some cases. For example, the Kaibab haplotype (i) probably is
derived from the Coconino Plateau-Mogollon Plateau h haplotype (Figs. 2 and 3),
with which it shares a restriction-site gain.
The Jemez Mountains-Mount Taylor I and
Elk Ridge m baplotypes share a site loss
and a site gain (Fig. 3), suggesting a northwestern New Mexico origin for the populations in Utah. On a broader scale, dispersal northward in New Mexico likely proceeded in two directions, represented by the
two distinct lineages of mtDNA (j, k, 1, m,
nand 0, p, g, r; Figs. 2 and 3). The Sangre
de Cristo populations are sister groups to
the northern-Colorado haplotype (r), suggesting dispersal along the Front Range of
the Rocky Mountains.
Despite strong inferential evidence for
post-Pleistocene dispersal, the phylogeographic structure observed among haplotypes suggests that S. aberti has been subject
to significant, earlier vicariant events as
well. Eastern and western assemblages of
mtDNA differ by a minimum of nine restriction sites and at a sequence-divergence
estimate of 1.8%. Assuming the general
rate estimate of 2% sequence divergence
per million years for evolution of mammalian mtDNA (Brown et aI., 1979, 1982)
is appropriate (if not somewhat conservative-Martin and Palumbi, 1993) for S.
aberti, then the eastern and western assemblages trace to an early Pleistocene separation. Thus, the evolutionary genetics of S.
aberti has been altered profoundly and perhaps repeatedly by climatic change
throughout the Pleistocene. An intriguing
Vol. 78, No. J
bit of evidence to this effect involves the
presence of ponderosa pines in Wyoming
during the Sangamonian interglacial (Baker,
1986).
Subspecies and variation of mtDNA.-It
is well established, both theoretically and
empirically, that a gene tree (e.g., mtDNA)
can differ topologically from the species
tree through which it has been transmitted
(Avise, 1994). Thus, phylogeographic
structure among lineages of mtDNA in S.
aberti need not coincide with existing subspecific designations or the environmentalgeographical boundaries currently separating subspecies. Our mtDNA data support
some of the subspecies limits defined by
Hoffmeister and Diersing (1978), but call
into question the validity of others as cohesive evolutionary units. For example, our
data support the monophyly of S. a.ferreus,
(haplotypes 0, p, q, r), although the mtDNA
distinction is not great, involving just two
site changes relative to other haplotypes of
the eastern assemblage. The Mexican haplotypes, although distinct from other eastern
haplotypes, form an unresolved trichotomy
in our maximum-parsimony analysis. Moreover, haplotype s is represented in both S.
a. barberi and S. a. durangi, suggesting that
either little genetic differentiation or, possibly, secondary contact has occurred between these taxa. Our data speak more
clearly to the subspecies S. a. aberti, S. a.
chuscensis, and S. a. kaibabensis. According to Hoffmeister and DiersiIig (1978), S.
a. aberti comprises all populations of the
Mogollon Plateau, populations in western
New Mexico (exclusive of the Chuska
Mountains), populations in the San Juan
Mountains (formerly S. a. mimus), and populations in the Abajo Mountains-Elk Ridge
(formerly S. a. navajo). As presently defined, S. a. aberti includes haplotypes from
both eastern and western assemblages, although these respective clones do not OCCur
sympatrically. Our data suggest distinct
evolutionary histories for the two assemblages, and therefore, challenges the validity of a single S. a. aberti composed of such
February 1997
LAMB ET AL.-PHYLOGEOGRAPHY OF SCIURUS ABERT!
highly divergent genetic lineages. The distribution of the eastern haplotype contingent of S. a. aberti is largely coincident
with the western range of the former subspecies s. a. mimus.
Sciurus a. chuscensis also is characterized by haplotypes from both the eastern
and western assemblages. However, it differs from the situation for S. a. aberti in a
most important respect, and, in fact, provides an empirical example of a rare phylogeographic outcome; one in which pronounced phylogenetic discontinuities (i.e.,
distinct haplotypes) occur without spatial
separation. One tenable explanation for
such a pattern involves secondary contact
between allopatrically evolved assemblages
or geographic races (Avise et aI., 1984).
Admixture of divergent eastern and western
haplotypes in the Chuska Range (Chuska
Mountains, Defiance Plateau), which lies
between 35-36°N in northeastern Arizona,
is consistent with the northern expansion of
(and presumably secondary contact between) eastern and western assemblages.
Did the contact zone in the Chuska Mountains involve the dispersal of squirrels of
the eastern assemblage into a western-assemblage resident population, or vice versa? It is interesting to note that S. a. chuscensis is represented by one western haplotype (g), which differs from other western
haplotypes by a single site loss, and by two
eastern haplotypes, one differing by a single
site gain (k) and the other identical to the
haplotype in the Zuni Mountains (j). Thus,
minimal divergence of nucleotides observed between the haplotypes in the Chuska Range and their respective assemblages
indicate that none have undergone extended
isolation in the Chuska Range, and that dispersal of eastern and western ancestral
forms to this region may have been roughly
contemporaneous. In the absence of nuclear
gene markers or morphological indices,
conclusions about the extent and direction
of mitochondrial gene flow are compromised. A future survey analyzing both nuclear and mitochondrial genes is required to
129
fully disclose patterns of dispersal and introgression in the Chuska Range.
The genetic status of S. a. kaibabensis
bears special mention because squirrels assignable to this subspecies differ markedly
in color of pelage from the typical countershading of other S. aberti, with dark gray
to black be1Iies and solid white tails (Cockrum, 1960). Confined to the Kaibab Plateau, S. a. kaibabensis originally was described as a separate species (Merriam,
1904) and for years served as a standard
example of aIIopatric speciation in college
biology texts (e.g., Hardin and Bajema,
1978; Keeton, 1980; Wallace et aI., 1981).
Nash and Seaman (1977) summarized the
available literature for S. aberti and continued to recognize S. kaibabensis. More recently, the tenor of the example has been
altered, stressing population differentiation
in response to geographic isolation (e.g.,
Campbell, 1993; McFadden and Keeton,
1995). Both explanations identify an ancestral population sundered by regional events
that formed the Grand Canyon and subsequently gave rise to distinctive northern
(kaibabensis) and southern (aberti) rim
forms.
However, disparate lines of evidence suggest that populations of S. aberti from the
Grand Canyon area probably were not in
position, spatially or temporally, to have
been separated by formation of the Canyon
(ca. 4-5 X 10 6 years ago-Lucchitta,
1979). To reiterate, evidence from packrat
middens from the Wisconsinan glaciation
demonstrates that ponderosa pines were absent from the southcentral Colorado Plateau, including the Grand Canyon, until ca.
10,300 years ago (Betancourt, 1990; Cole,
1990). Thus, without a base of ponderosa
pines, it is unlikely that the Kaibab Plateau
could have sustained an isolated population
of S. aberti. In addition, S. a. kaibabensis
exhibits limited morphological change relative to populations of S. a. aberti. Hoffmeister and Diersing (1978) stressed that
cluster analysis of cranial and external characters revealed little, if any, differentiation
JOURNAL OF MAMMALOGY
130
between specimens from the Kaibab Plateau (n = 20) and those from the Coconino
and Mogollon plateaus (n = 88). Moreover,
dark-bellied specimens are observed in other parts of the range, and white-bellied individuals are occasionally sighted on the
Kaibab Plateau (Hoffmeister and Diersing,
1978). Wettstein and States (1986a) have
suggested that variation in coat color may
involve a single gene, like the agouti locus
of Mus, and that aberrant color patterns in
S. aberti might result from new retroviral
insertions, just as those reported in mice
(Jenkins et aI., 1981).
OUf mtDNA data for S. Q. kaibabensis
are consistent with the phenetic and paleoclimatic interpretations above. With just
two unique site changes, the Kaibab haplotype, i, exhibits minimal divergence (p =
0.004) from others in the western assemblage. One would anticipate a p some
20-fold higher (p = 0.090) than the observed value, had an ancestral Kaibab population persisted in continuous isolation following the inception of the Grand Canyon.
Complementing the distance analyses, the
maximum-parsimony tree depicts the Kaibab haplotype lying well within the western
clade. As noted previously, the Kaibab haplotype shares a unique HindIII site gain
with haplotype h (in effect, a synapomorphy) found in four of the six individuals
from the Coconino Plateau (i.e., South Rim
of the Grand Canyon) sample. Collectively,
the genetic, morphologic, and paleoclimatic
data offer strong support for a late-Pleistocene origin for S. a. kaibabensis via northward dispersal from central Arizona.
ACKNOWLEDGMENTS
This research was supported by an East Carolina University College Research Award and
Faculty Travel Awards to T. Lamb, and by grants
GM-41260 and AI-18972 from the National Institutes of Health to P. 1. Wettstein. We thank R.
Babb, K. Crawford, T. Esque, A. Jones, and D.
Mahoney for assistance in collecting specimens.
S. Anderson and J. Betancourt provided insightful discussion about ponderosa pines. We grate-
Vol. 78, No.1
fully acknowledge B. Balderrama H. and G.
Quintana M. for logistic support in Chihuahua.
Chihuahuan samples were obtained on permits
(Permiso de Caceria) 4884 and 4885, issued by
Secretaria de Desarollo Urbano y Ecologia (SEDUE). Other samples were secured through collecting permits provided by the state fish and
game departments of Arizona, Colorado, New
Mexico, and Utah, and by the Navajo Fish and
Wildlife Branch of the Navajo Nation.
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ApPENDiX I
Approximate locality data for Sciurus aberti
used in this study; subspecies conform to Hoffmeister and Diersing (1978). Locality codes are
in parentheses, and numbers of the museum
specimen are in brackets. All but three of the
specimens from New Mexico are deposited in
the Museum of Southwestern Biology (MSB);
specimens from Mexico are in the University of
Michigan Museum of Zoology (UMMZ).
S. a. aberti. ARIZONA-Coconino Plateau
(15): vicinity of Hull Tank; vicinity of Grandview Lookout; Skinner Ridge; Coconino Wash,
San Francisco Mountains (16): Anderson Mesa;
ca. 3 miles S, 5 miles W Flagstaff; Crater Lake
ca. 8.5 miles N. 6.5 miles W Flagstaff. Mogollon Plateau (17): vicinity of Gentry Lookout. Sierra Ancha (18): Workman Creek. NEW MEXICO-Jemez Mountains (6): vicinity of La Cueva Forest Service Station (MSB 61584); along
Vol. 78, No.1
Rio Cebolla (MSB 61576). Zuni Mountains (8):
ca. 7.0 miles S, 1.5 miles W Bluewater State
Park (MSB 61572-61574)~ vicinity of Cerro
Colorado (MSB 61575, 61583). San Juan Mountains (5): Valle Grande Peak (MSB 61577); ca.
5.5 miles S, 3.5 miles E Canjilon (MSB 61578,
61582, 61589]. Mount Taylor (7): ca. 1.0 mile
S, 1.5 miles W Mount Taylor (MSB 61590); ca.
2.5 miles N, 2.0 miles W Mount Taylor (MSB
61595); ca. 1.0 mile N, 4.5 miles W Mount Taylor, San Mateo Mountains (10): Beartrap Canyon
(MSB 61591). Datil Mountains (9): ca. 10.5
miles N. 4.0 miles W Datil (MSB 6159761598). Mogollon Mountains (11): ca. 12.0
miles S, 5.5 miles E Reserve (MSB 61596). Pinos Altos Range (12): vicinity of Lookout Point
(MSB 61592); Sapillo Creek (MSB 61599); vicinity of Signal Peak (MSB 61593-61594).
UTAH-Elk Ridge (13): Kigalia Point.
S. a. barberi. CHIHUAHUA-Sierra Madre
Occidental (21): (BI-4) Mesa Cuesta Blanca,
ca. 7.0-10.0 km N, 1.0 km W Mesa del Huraca.n
(UMMZ); (B5-7, 9-11) Cuesta Nalgas, ca. 22.0
km N, 6.0-8.0 km W Mesa del Huracan
(UMMZ); (B8) Arroyo Las Ratas ca. 25 km N,
2.5 km W Mesa del Huracan (UMMZ); (BI2)
San Juan, ca. 15.0 km N, 4.5 km W Mesa del
Huracan (UMMZ).
S. a. chuscensis. ARIZONA-Chuska Mountains (19): Tsaile Creek on road 7500. Defiance
Plateau (20): Defiance Plateau on road 9000. S.
a. durangi. CHIHUAHUA-Sierra Madre Occidental (22): S of Laguna Arareco, ca. 6.5 km
S, 5.5 km E Creel (UMMZ).
S. a. ferreus. COLORADO-Medicine Bow
Range (1): 5 miles S, 3 miles E Rustic; Pike's
Peak region (2). NEW MEXICO-Sangre de
Cristo Mountains (4): vicinity of Truchas (MSB
61579-61581). Cimarron Range (3): near
McCrystal Creek Campground (MSB 6158561588).
S. Q. kaibabensis. ARIZONA-Kaibab Plateau (14): Orderville Canyon; Jolly Sink; ca. 3.5
miles S, 2.5 miles E Jacob Lake; Fracas Lake;
W of Dry Park; Tater Ridge.
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1111110
1111110
1111110
1111110
11 II 110
1111101
II II 101
1111101
1111101
lllllOl
1111101
1111101
1111101
1111101
1111101
IJ 11101
IllllOl
1110
1110
1110
1110
1110
1110
IIlO
1110
1110
1110
1010
11 10
J I 10
1110
1110
1110
1110
1110
1110
I I 10
Illl
III
111
III
III
111
111
III
111
111
III
III
110
111
111
111
III
III
III
III
111
8gm
Bgll
Bell
AvaIl
AvaI
1111
1111
1111
Illl
1111
Illl
1111
1111
IIlI
lOll
1011
1011
lOll
lOll
1001
1011
1011
lOll
1011
1001
lOll
8stEII
III
III
III
lli
III
111
III
III
111
III
III
III
III
111
III
III
111
III
111
III
III
etal
111111
lltllI
IIlIU
Ililil
111111
111111
111110
11l11O
II II 11
111111
!llIll
111111
!lllil
111111
III III
llllli
llllll
111111
IIUll
llllll
111111
EcoRI
111100
111000
111100
111100
111100
111100
111100
111100
1l11l0
1l01O1
110101
110101
1l01O1
110101
110101
1l0lDi
1l01O1
110101
010101
OlO101
010101
Illll
1111O
11110
11110
11110
111I0
ill 10
11110
11110
11110
11l1O
11110
II 110
1IIll
11111
lllli
11111
11Ill
Illil
11111
IIlll
EcoRV EcoOlO9
1111100
1111100
1111100
1111100
1111100
1111100
IIllIOO
IIIllIO
1111110
II II 100
llillOO
1111100
IIlllOO
1111lOl
1111100
1111100
1111101
1111100
1111100
llliloo
IllllOO
HindIII
s.
II
II
II
11
II
II
II
III
III
III
III
III
III
I II
III
111
110
110
llO
110
110
llO
110
llO
110
III
III
III
10
10
10
II
II
11
II
II
II
II
11
II
II
II
11
II
II
II
11
II
II
Pst! Pvull Sad
1110
111O
1110
II
1110
11
1110
II
1110
II
lIlI
II
II J i l l
1110 II
1110
II
1IIO 11
1110 II
1110 11
IliO
11
1110 11
1110
II
111O
IllO
1110
1110
1110
HhaI
Presence (I)-absence (0) matrix of inferred restriction sites for the 21 haplotypes resolved for
ApPENDIX II.
IIlllll1l
Illll1lll
111111111
111111111
llllIll11
111111110
111111111
Illllllll
111111111
lllllllOO
111I 11100
llIlllloo
IIllDlloo
111111100111111100
101111100
111111100
IIIIIIIOO
Illllllll
111111111
111111111
SpeI
aberti.
II
II
II
II
II
11
11
II
II
11
11
II
II
11
II
11
II
II
III
III
III
III
III
III
III
III
III
11
III
III
111
111
III
III
III
III
111
II
II
Xhal
III
III
111
StuI
w
w
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