SEPTEMBER2002
VOL. 58
NO. 3
Herpetologica, 58(3), 2002, 277-292
? 2002 by The Herpetologists' League, Inc.
GENETIC RELATIONSHIPS AMONG POPULATIONS OF
SCELOPORUS UNDULATUS FAIL TO SUPPORT PRESENT
SUBSPECIFIC DESIGNATIONS
DONALD B. MILES', ROBERT NOECKER, WILLEM M. ROOSENBURG, AND
MATrHEW M. WHITE
Department of Biological Sciences and Program in Conservation Biology, Ohio University,
Athens, OH 45701, USA
ABSTRACT: The eastern fence lizard, Sceloporus undulatus, is a broadly distributed polytypic
species. We surveyed allozyme variation with the goal of generating an intraspecific phylogeny to
evaluate the current classification of the species. We electrophoretically assayed 24 loci from 12
populations of S. undulatus, which comprised 6 of the 11 recognized subspecies, 3 additional species
of Sceloporus (S. occidentalis, S. virgatus, and S. woodi), and an outgroup taxon, S. clarki. Out of
the 24 loci, 14 loci were variable. Phylogenetic analyses using distance, likelihood, and parsimony
resulted in trees that were inconsistent with current subspecific designations. Three species of
Sceloporus (S. occidentalis, S. virgatus, and S. woodi) arose within S. undulatus. Two major lineages
of populations of S. undulatus were identified: (1) a midwestern grasslands group that includes the
population from Missouri, and (2) various populations from the eastern woodlands and western
canyonlands. The subspecies S. u. hyacithinus and S. u. undulatus are polyphyletic, whereas S. u.
garmani and S. u. tristichus are paraphyletic. No fixed allele differences were observed among the
populations of S. undulatus, or among the other species of Sceloporus. Our results indicate that the
present subspecies designations do not portray patterns of evolutionary relatedness and require reevaluation.
Key words:
tus
Allozymes; Geographic variation; Phrynosomatidae; Phylogeny; Sceloporus undula-
SPECIES characterized by geographic
distributions spanning a variety of habitats
typically exhibit marked variation in numerous character complexes (Armbruster
et al., 2001; Roff, 1992; Sinervo, 1990).
Comparative analyses of geographic variation have been a cornerstone in evolutionary biology for assessing the adaptive significance of phenotypic traits (Garland and
Adolph, 1991; Gould and Johnston, 1972).
Most studies that reveal significant levels
of population differentiation suggest that
the spatial variation provides evidence for
adaptation to local conditions in response
1 CORRESPONDENCE:
e-mail, [email protected]
277
to selective factors arising within the environment (Gould and Johnston, 1972; Irschick and Shaffer, 1997; Straney and Patton, 1980). However, a number of alternative mechanisms may lead to population
differentiation, including genetic drift,
population bottlenecks, and vicariance
events (Zink, 1996). Therefore, a population-level phylogeny should be estimated
before inferences about the adaptive significance of geographic variation are adduced (Thorpe et al., 1995). A comparison
of the evolutionary relationships among
populations and their geographic distributions can lead to inferences regarding
the importance of barriers to gene flow
278
HERPETOLOGICA
[Vol. 58, No. 3
and historicalbiogeographicevents (Avise, subspecies: S. u. tristichus, S. u. elongatus,
1992, 2000; Turner et al., 1996).
The eastern fence lizard, Sceloporus undulatus, is a broadly distributed, polytypic
species. Fence lizards are found from the
east coast of the United States, west to
Utah and Arizona and from Pennsylvania
south into northern Mexico (Lemos-Espinal et al., 1998). The species has a broad
elevational range, from near sea level to
>2000 m and occupies a variety of habitats, including eastern deciduous forest,
grassland, desert grassland, and western
coniferous forests. A hallmark of S. undulatus is the extensive phenotypic differentiation among populations (Andrews,
1998; Ferguson et al., 1980; Niewiarowski,
1994). Intraspecific variation has been
demonstrated in scalation (Crenshaw,
1955; Smith et al., 1992), coloration (Gillis,
1989; Rand, 1990), chromosomes (Cole,
1972, 1977, 1983), and ecological traits
(e.g., Ferguson and Talent, 1993; Niewiarowski and Roosenburg, 1993; Tinkle and
Ballinger, 1972). The species has been the
focus of a number of comparative life history analyses (Adolph and Porter, 1993,
1996; Niewiaroski, 1994, 1995, 2001;
Smith et al., 1996). In addition, the paraphyly among seven subspecies of S. undulatus, indicated by phylogenetic analysis
of morphological and molecular data
(Wiens and Reeder, 1997), merits additional investigation.
Earlier taxonomies recognized seven
subspecies (Smith, 1946). However, additional studies have resulted in the current
classification that recognizes at least 11
subspecies (Smith et al., 1992). Most of
the sub-specific designations have been
defined principally by external moxphological characters, such as scalation and color
patterns (Smith, 1938; Smith et al., 1992).
Recent taxonomic studies have treated S.
undulatus as a superspecies, in which the
subspecies can be arranged into three
groups (Smith et al., 1992). Two subspecies comprise an eastern woodlands group:
S. u. undulatus and S. u. hyacinthinus.
The second or grasslands group has four
subspecies: S. u. consobrinus, S. u. cowlesi,
S. u. garmani, and S. u. tedbrowni. The
last group, canyonlands, contains three
and S. u. erythrocheilus. The groups are
separated geographically. The eastern
woodlands group is restricted to the eastern half of North America whereas the
canyonlands group is located in the Rocky
Mountain region. The grassland group is
broadly distributed throughout the Great
Plains. In addition, habitat preferences
within the groups correlate with substrate
use. The eastern woodland group tends to
have an arboreal lifestyle (Crenshaw, 1955;
Parker, 1994; Tinkle and Ballinger, 1972),
the grassland group is terrestrial (Ballinger
et al., 1981; Ferguson et al., 1980; Vinegar,
1975), and the canyonlands group is predominantly saxicolous (Tinkle, 1972; Tinkle and Ballinger, 1972; Tinkle and Dunham, 1986). Hybridization and introgression is known among several of the presumed subspecies (McCoy, 1961; Sites et
al., 1992; Smith et al., 1991, 1993). However, apart from the analysis by Wiens and
Reeder (1997), little information is available about the levels of genetic divergence
among populations of S. undulatus.
In a preliminaxy analysis of allozyme
variation among populations of S. u. hyacinthinus, Spohn and Guttman (1976)
suggested that differentiation among populations of hyacinthinus was as great as
differentiation between hyacinthinus and
S. u. garmani. However, their analyses did
not consider the genetic relationships
among the remaining subspecies of S. undulatus. In a phylogenetic analysis of the
genus Sceloporus using morphology and
genetic data, Wiens and Reeder (1997)
found that the subspecies of S. undulatus
do not form a monophyletic group. They
showed that S. occidentalis, S. virgatus,
and S. woodi were interspersed among
various subspecies of S. undulatus in their
combined-data tree. In this study, we examine the pattern of genetic variation
among 12 populations of S. undulatus. We
also include three additional species that
have been placed within undulatus group
(Wiens and Reeder, 1997): S. occidentalis
S. virgatus, and S. woodi. Our approach
uses both phenetic and phylogenetic analyses of allozyme data in order to determine the genetic relationships among the
TABLE
1.-Sample
279
HERPETOLOGICA
September 2002]
designations, sample sizes (n), subspecific affiliation, and locations of populations of Sceloporus sampled for this study.
Sample
(n)
Ohio
Florida
Northern Arizona
Northern New Mexico
Utah
Nebraska
Texas
Mississippi
South Carolina
Missouri
Kansas
Central Arizona
woodi
occidentalis
virgatus
clarki
(36)
(24)
(29)
(14)
(11)
(15)
(15)
(15)
(16)
(14)
(5)
(6)
(6)
(14)
(14)
(14)
Taxon
S. u. hyacinthinus
S. u. undulatus
S. u. tristichus
S. u. tristichus
S. u. elongatus
S. u. garmani
S. u. consobrinus
S. u. undulatus
S. u. undulatus
S. u. hyacinthinus
S. u. garmani
S. u. tristichus
S. woodi
S. occidentalis
S. virgatus
S. clarki
Location
Vinton Co., Ohio
Alachua Co., Florida
Coconino Co., Arizona
Sandoval Co., New Mexico
Uintah Co., Utah
Thomas Co., Nebraska
Schleicher Co., Texas
Lowndes Co., Mississippi
Bamwell Co., South Carolina
St. Louis Co., Missouri
Scott Co., Kansas
Sunflower, Maricopa Co., Arizona
Ocala Co., Ocala National Forest, Florida
Riverside Co., Santa Rosa Mountains, Califomia
Chiricahua Mountains, Cochise Co., Arizona
Pima Co., Arizona
recognized subspecies. This study is part
of a larger project involving the analysis of
morphological and physiological differentiation among populations of S. undulatus.
In general, our analyses do not lend support to the reality of the subspecies of S.
undulatus; rather, our findings suggest the
need for a taxonomic revision.
rpm for 20 min at 4 C. The supernatants
were stored at -80 C. Horizontal starch
gel electrophoresis was carried out in 12%
gels (Starch Art). Electrophoresis procedures follow Murphy et al. (1990). Specific
enzymes and buffers are listed in Table 2.
Enzyme, locus, and allele nomenclature
follows Murphy and Crabtree (1985).
MATERIALS AND METHODS
Data Analysis
Collection of Animals
We collected a total of 190 individuals
of S. undulatus from 12 populations, encompassing 6 recognized subspecies, 14
individuals of S. occidentalis, 14 individuals of S. virgatus, 6 individuals of S. woodi,
and 14 individuals of S. clarki during 1992,
1993, and 1994. We used S. clarki as an
outgroup, because it belongs to the sister
clade of the undulatus species group
(Wiens and Reeder, 1997). Population
sample sizes and specific location information are included in Table 1. Voucher
specimens are catalogued in the Ohio University Vertebrate Collection.
We coded allozyme data for all variable
loci as genotype counts and analyzed them
with the BIOSYS-1 program (Swofford
and Selander, 1981). We estimated overall
genetic variability, including allele frequencies, percent polymorphism, and heterozygosities. Deviations from HardyWeinberg equilibrium and inter-population genic heterogeneity were determined
using chi-square statistics. We used the allelic frequency data to construct a matrix
of all possible pair-wise comparisons
among populations using Nei's (1978) unbiased genetic distance. We chose Nei's
statistic because it is unbiased if using
small sample sizes.
Considerable debate exists regarding
the best analytical method for reconstructing phylogenies from polymorphic data,
such as allozymes. In a series of papers,
Wiens evaluated the performance of various methods for phylogenetic analyses of
polymorphic data (Wiens, 2000; Wiens
and Servedio, 1998) and found that con-
Protein Electrophoresis
We removed liver and skeletal muscle
from specimens and separately stored
them at -80 C in an equal volume of an
aqueous homogenizing buffer (0.1 M
Tris-0.001 M EDTA-0.0001
M NAD0.0001 M NADH, pH 7.0). Tissues were
homogenized and centrifuged at 10,000
[Vol. 58, No. 3
HERPETOLOGICA
280
and electrophoretic conditions used in population surveys of Sceloporus undulatus.
2.-Enzymes
Names, enzyme commission numbers (EC), and abbreviations follow Murphy and Crabtree (1985).
TABLE
Enzyme
EC number
Locus
Tissue*
Buffer**
Adenylate kinase
Aspartate aminotransferase
Aspartate aminotransferase
Catalase
Creatine kinase
Dipeptidases
"General protein"
Glucose-6-phosphate isomerase
Glycerol-3-phosphate
dehydrogenase
Isocitrate dehydrogenase
L-iditol dehydrogenase
Lactate dehydrogenase
Lactate dehydrogenase
Malate dehydrogenase
"Malic enzyme"
Manose-6-phosphate isomerase
Phosphoglucomutase
Phosphogluconate dehydrogenase
Purine-nucleoside phosphorylase
Superoxide dismutase
Xanthine dehydrogenase
2.7.4.3
2.6.1.1
2.6.1.1
1.11.1.6
2.7.3.2
3.4.13.11
5.3.1.9
Ak-A
Aat-A
Aat-B
Cat-A
Ck-A
PEP (A, B, C, D)
Gp-1
Gpi-A
M
L
L
L
M
M
M
L
A
B
B
A
A
C
B
D
1.1.1.8
1.1.1.42
1.1.1.14
1.1.1.27
1.1.1.27
1.1.1.37
1.1.1.40
5.3.1.8
5.4.2.2
1.1.1.44
2.4.2.1
1.15.1.1
1.1.1.204
G3pdh-A
Idh-A
Iddh-A
Ldh-A
Ldh-B
Mdh-A
Me-A
Mpi-A
Pgm-A
Pgd-A
Pnp-A
Sod-A
Xdh-A
M
L
L
L
L
L
M
L
M
M
L
L
L
A
A
A
B
B
B
A
D
A
A
B
B
A
-
Tissue symbols: L = liver, M = skeletal muscle.
** A: Tris-citrate pH 8.0, (20 h at 50 V; Selander et al., 1971); B: Lithium-hydoxide, (20 h at 50 V; Selander et al., 1971); C: Tris-hydrochloric
acid pH 8.5, (8 h at 200 V, Selander et al., 1971); D: Phosphate-citrate pH 7.0, (20 h at 50 V Selander et al., 1971).
*
tinuous maximum likelihood, additive distance methods, and frequency parsimony
were among the most accurate methods
for allozyme data (Wiens, 2000). Therefore, we followed the recommendations
presented in Wiens (2000) for analyzing
the allozyme data. In particular, we employed three methods for phylogenetic reconstruction: least-squares approach using
pair-wise distances (Felsenstein, 1997;
Fitch and Margoliash, 1967), continuous
maximum likelihood (CONTML) (Felsenstein, 1981, 1983), and maximum parsimony (MP) (Swofford, 1998).
Additive distance method.-Phylogenetic analysis of the distance data for S. undulatus was accomplished with PHYLIP
3.572c (Felsenstein, 1995) using the program FITCH, for which the input was a
matrix of Nei's (1978) unbiased genetic
distances. Optimal trees were determined
by implementing the "global rearrangements" option. We randomly varied the order with which taxa were included in the
tree using the jumble option with 50 replicates.
Continuous
maximum likelihood.-
Maximum likelihood analyses were conducted using the CONTML program in
PHYLIP 3.572c. In this analysis, we used
populations of S. undulatus as terminal
units and species as terminal units for the
other species in the undulatus group. Allele frequencies for each terminal unit
were used in the analysis. Global rearrangements were employed to find the
best tree. Furthermore, to minimize the
likelihood of obtaining locally-optimal
trees, we randomly varied the order with
which taxa were included in the initial tree
using the jumble option with 50 replicates.
Parsinony analysis. -Parsimony analyses were conducted using PAUP* 4.0 Beta
(Swofford, 1998). We implemented the
MANOB (Manhattan distance, observed
allele frequency arrays) criterion for determining optimal trees (Berlocher and Swofford, 1997; Wiens, 1995). The allozyme
data were coded by considering the locus
as the character (Murphy, 1993) and sets
of allele frequencies as character states. A
matrix of Manhattan Distances was created for each polymorphic locus. This distance matrix was used as a step matrix for
HERPETOLOGICA
September 2002]
parsimony analysis. The MANOB criterion
is similar to the Mabee and Humphries
(1993) approach, but it differs by using
frequency coding rather than presence/absence coding. The phylogenetic analysis
used the heuristic search option, with 50
random addition sequence searches. We
retained only minimal trees using TBR
branch swapping with the steepest descent
option. The trees were rooted using S.
clarki.
We used bootstrapping for all phylogenetic analyses to determine support for the
resolved clades in all phylogenetic analyses
(Felsenstein, 1985). In each analysis, we
generated 500 pseudo-random data sets.
Following the arguments presented in Hillis and Bull (1993) and Wiens and Reeder
(1997), branches with bootstrap values exceeding 70% were considered strongly resolved (but see their caveats).
Finally, we determined whether the
phylogenetic reconstructions were consistent with the habitat/geographical affiliation of the terminal units. We assigned the
populations of S. undulatus and the other
species of Sceloporus into one of three categories: grassland, eastern woodland, or
canyonland. We used the program MacClade 4.01 to trace habitat/geographical
affiliation on each of the three phylogenetic trees using the program MacClade
4.01 (Maddison and Maddison, 2000).
RESULTS
Genetic Variation
Ten of the 24 resolved loci were monomorphic for all populations sampled. Electromorph frequencies, percentages of
polymorphic loci (P), mean number of alleles per locus, and mean heterozygosities
(H) for the 16 populations/species are provided in Table 3. No fixed allele differences were observed among populations or
subspecies of S. undulatus. Also, no fixed
differences were evident between the other species of the undulatus group (S. virgatus, S. occidentalis, and S. woodi) and
the populations of S. undulatus. All 14
polymorphic loci exhibited highly significant genic heterogeneity among populations. Two fixed allele differences were ob-
281
served between S. undulatus and S. clarki
(Gpi and Pgd, Table 3). Values of P ranged
from 4.1 (sunflower population of S. undulatus and S. clarki) to 33.3 (Texas, Table
3). The mean number of alleles per polymorphic locus within a populations varied
from a low of 1.1 (c. AZ, S. clarki) to a
high of 1.6 (Florida and Texas). Heterozygosities were lowest in the South Carolina population (0.008) and highest in the
Florida population (0.129, Table 3).
Table 4 presents a matrix of pair-wise
comparisons of genetic distances (Nei,
1978) calculated from the allele frequency
data in Table 3. Values of Nei's D range
from a low of 0.009 between the populations of S. undulatus from Utah and New
Mexico to a high of 0.271 between the
Missouri and South Carolina populations.
The mean among all populations of S. undulatus was 0.115.
Phylogenetic Relationships
Distance method.-The
Fitch-Margoliash tree identified three main clusters
(Fig. 1). One cluster contains the populations from Nebraska, Kansas, Texas, and
Missouri. Notably, these are populations
(excluding Missouri) that comprised the
grassland populations. A second cluster
contained a mixture of three eastern
woodland populations (Florida, Ohio, and
South Carolina), four western populations
(New Mexico, central and northern Arizona, and Utah), and S. woodi. In this
cluster, the populations from Florida and
Ohio were grouped together. However, the
western populations were joined with S.
woodi and the South Carolina population
of S. undulatus. The placement of these
last two species suggests a western ancestor for S. woodi and the South Carolina
population. A third cluster joined the population of S. undulatus from Mississippi
with S. occidentalis and S. virgatus. The
population from Mississippi was a sister
group to the two remaining species of Sceloporus. None of the branches attained
support exceeding 50% in the bootstrap
analysis.
Continuous maximum likelihood.-A
single maximum likelihood tree was found
(ln L = 324.35). Several major features are
3.-Allele frequencies and variability estimates for polymorphic loci resolved in 12 populations of Sceloporus
(SO), S. woodi (SW) and S. clarki (CLK). Abbreviations for S. undulatus populations are: NM: New Mexico; AZ:
UT: Utah; NB: Nebraska; TX: Texas; MS: Mississippi; SC: South Carolina; MO: Missouri; KS: Kan
TABLE
Locus
(N)
Ak
Aat-1
Cat
Ck
Gpi
Iddh
Ldh-1
Ldh-2
Mdh
Me
Pnp
Pgm
Pgd
Sod
Allele
NM
(14)
AZ
(29)
FL
(24)
OH
(36)
UT
(11)
NB
(15)
TX
(15)
MS
(15)
SC
(16)
MO
(14)
KS
(5)
a
0.929
0.173
0.957
1.000
1.000
1.000
1.000
1.000
1.000
1.000
1.000
b
c
0.071
0.000
0.654
0.173
0.043
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
a
b
c
a
b
c
a
b
a
b
a
b
a
b
a
b
a
b
a
b
c
a
b
a
b
c
d
a
b
c
d
e
a
b
1.000
0.000
0.000
1.000
0.000
0.000
0.604
0.396
0.000
0.681
0.319
0.000
1.000
0.000
0.000
0.967
0.033
0.000
1.000
0.000
0.000
0.867
0.133
0.000
0.000
1.000
0.000
0.929
0.000
0.071
1.000
0.000
0.000
0.143
0.500
0.636
0.500
0.045
0.000
0.167
0.000
0.000
0.036
0.000
0.857
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
0.000
0.821
0.179
1.000
0.000
0.000
0.000
0.300
0.600
0.000
0.100
0.000
1.000
0.000
0.500
0.000
0.923
0.077
1.000
0.000
1.000
0.000
0.768
0.232
1.000
0.000
1.000
0.000
0.828
0.172
0.000
0.786
0.214
1.000
0.000
0.000
0.000
0.276
0.724
0.000
0.000
0.000
1.000
0.000
0.364
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
0.800
0.200
1.000
0.000
0.000
0.935
0.065
0.938
0.063
0.000
0.000
0.523
0.477
0.000
0.000
0.000
1.000
0.000
0.500
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
0.742
0.258
0.543
0.413
0.043
0.875
0.125
1.000
0.000
0.000
0.000
1.000
0.000
0.000
0.000
0.000
1.000
0.000
0.955
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
0.000
0.955
0.045
1.000
0.000
0.000
0.000
0.000
0.955
0.000
0.045
0.000
0.864
0.136
0.000
1.000
1.000
0.000
1.000
0.000
0.867
0.133
1.000
0.000
0.933
0.067
1.000
0.000
1.000
0.000
0.000
0.900
0.100
0.400
0.600
0.000
0.000
0.094
0.906
0.000
0.000
0.000
0.967
0.033
0.000
0.833
1.000
0.000
1.000
0.000
0.933
0.067
1.000
0.000
0.233
0.767
1.000
0.000
0.933
0.000
0.067
0.833
0.167
0.933
0.000
0.067
0.000
0.000
0.133
0.000
0.867
0.000
0.933
0.067
1.000
0.000
1.000
0.000
1.000
0.000
0.633
0.367
1.000
0.000
0.933
0.067
1.000
0.000
0.933
0.067
0.000
0.933
0.067
0.000
0.000
1.000
0.000
0.000
0.067
0.633
0.300
0.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
0.969
0.031
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
0.000
0.969
0.031
1.000
0.000
0.000
0.000
0.000
0.813
0.063
0.125
0.000
1.000
0.000
0.000
0.964
1.000
0.000
1.000
0.000
0.964
0.036
1.000
0.000
0.071
0.929
1.000
0.000
1.000
0.000
0.000
1.000
0.000
0.286
0.000
0.464
0.250
0.000
0.393
0.000
0.607
0.000
1.000
0.000
0.000
1.000
1.000
0.000
1.000
0.000
1.000
0.000
1.000
0.000
0.700
0.300
1.000
0.000
1.000
0.000
0.000
1.000
0.000
0.600
0.400
0.000
0.000
0.750
0.250
0.000
0.000
0.000
1.000
0.000
HERPETOLOGICA
September 2002]
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"t +1
+
283
apparent from this tree (Fig. 2). First, the
population of undulatus from Mississippi
diverged fairly early. Second, the only
branch length significantly different from
0 was the clade formed by the grassland
populations plus Missouri. However, rather than diverging relatively early, the grassland populations form a sister group to the
eastern and western populations. The tree
did not support the monophyly of the
western populations. The position of S.
woodi and the South Carolina population
suggests that they diverged from an ancestral western population. As in the previous
tree, Florida and Ohio were united. This
grouping along with the group consisting
of S. occidentalis and S. virgatus was
strongly supported by the bootstrap analysis. Third, S. occidentalis and S. virgatus
appear to have arisen from an undulatusancestor, but diverged earlier than S. woodi. The tree also suggests that S. u. undulatus and S. u. hyacinthinus are polyphyletic, but S. u. tristichus and S. u. garmani are paraphyletic.
Parsimony analysis. -Parsimony analysis of the allozyme data yielded a single
tree (L = 28.35, CI = 0.61, RI = 0.53).
Several patterns are evident from the parsimony analysis (Fig. 3). First, little support was found for monophyly of the individual subspecies. For example, S. u.
tristichus, S. u. garmani, and S. u. undulatus are paraphyletic whereas S. u. hyacinthinus is polyphyletic. Second, the
grassland populations are grouped in the
same clade. As in the previous trees, the
Missouri population is placed with the
grassland populations. The two western
species, S. virgatus and S. occidentalis,
were placed within the grassland group.
Only the association between the Texas
and Missouri populations was strongly
supported by the bootstrap (Fig. 3). Third,
the branching patterns fail to group the
populations together with respect to habitat or geography. In addition, the Mississippi population is placed basal to the remaining populations and species. The canyonland populations do not form a distinct
cluster, but rather they have eastern populations interspersed within group. A bootstrap analysis provided strong support for
284
TABLE
Population
NM
AZ
FL
OH
UT
NB
TX
HERPETOLOGICA
[Vol. 58, No. 3
4.-Matrix of Nei (1978) unbiased genetic distances for all pair-wise comparisons among samples of
Sceloporus used in this study. See Table 3 for population or species abbreviations.
NM
AZ
FL
OH
UT
NB
TX
MS
SC
MO
KS
SUN
SV
SO
SW
CLK
***
0.05
0
0.03
3
0.06
7
0.06
7
0.11
1
0.03
2
0.00
8
0.06
8
0.05
7
0.11
4
0.09
8
0.14
4
0.10
9
0.18
3
0.09
8
0.13
4
0.19
4
0.15
0
0.18
9
0.15
7
0.11
5
0.18
0
0.21
1
0.14
1
0.19
3
0.21
1
0.19
2
0.20
3
0.07
8
0.15
0
0.07
3
0.13
7
0.07
3
0.17
6
0.23
3
0.26
7
0.17
9
0.24
5
0.19
8
0.25
7
0.19
4
0.10
5
0.03
0
0.18
4
0.27
0
0.09
1
0.14
5
0.08
8
0.10
5
0.12
6
0.03
3
0.07
3
0.19
6
0.20
5
0.08
0
0.00
2
0.06
6
0.05
2
0.09
6
0.00
2
0.10
1
0.14
1
0.20
1
0.07
0
0.18
3
0.11
3
0.17
5
0.22
1
0.17
0
0.24
3
0.18
5
0.13
1
0.29
3
0.15
9
0.27
1
0.28
8
0.19
2
0.18
5
0.48
9
0.42
7
0.50
2
0.55
0
0.54
5
0.32
5
0.52
5
0.52
4
0.66
1
0.50
9
0.33
4
0.52
8
0.31
8
*
0.23
9
0.33
1
0.22
6
0.31
1
0.22
9
0.23
1
0.28
3
0.36
4
0.14
6
0.22
6
0.25
3
0.22
8
0.27
6
0.66
0.44
1
0.48
5
0.47
2
0.40
9
0.41
1
0.48
6
0.38
7
0.38
9
0.50
2
0.32
3
0.42
9
0.39
2
0.55
9
0.71
***
***
***
***
***
***
MS
SC
MO
KS
SUN
SV
SO
***
***
***
***
***
***
7
SV
7
0.40
0
CLK
the grouping of two eastern woodland
(Florida and Ohio) populations.
Concordance among the Trees
We determined the concordance among
the three trees by a consensus analysis using the PHYLIP 3.572c program CONSENSE (Fig. 4). Several relationships suggested by the individual analyses were supported by the consensus tree. A group
comprising the populations from Texas,
Nebraska, Kansas, and Missouri formed a
basal lineage. Most authors treat the Missouri population as a member of the eastern woodland group. However, the close
relationships with the grassland taxa suggest that it recently invaded the woodland
habitats. A clade consisting of S. occidentalis and S. virgatus was consistently recovered in the analyses. The western canyonland populations of S. undulatus were
clustered together along with several eastern woodland populations. Because the
clade made up of S. undulatus from Florida and Ohio was basal to the remaining
eastern and western populations, we infer
that the western populations may have diverged from an eastern woodland ancestor.
The emergence of South Carolina and S.
woodi within a group of western populations of S. undulatus may be consistent
with a secondary invasion of the eastern
woodlands.
We explicitly evaluated the evolutionary
transitions in habitat affinity suggested by
the phylogenetic trees using parsimony
analysis. Optimization of habitat indicated
an ancestor of western canyonlands habitat
in all three trees (Fig. 5, 6, 7). In addition,
a single origin of the grassland populations
was evident in all three trees. Four transitions to an eastern woodland habitat was
285
HERPETOLOGICA
September 2002]
S. occidentalis
S.u=. uonhybrintX
S. u.hyacinthinus MO
S.
u. a unulatus FL
S. u. tristichusNo. AZ
D.u. tristichusNM
S.u.garmanirgNEu
_1S.
u. tristichus c. AZ
F
S. u. elongatusUT
_S
S. u. undulatus SC
woodi
~~~~~~~.
S. u. garmaniNE
S. u. consobrinusTX
u. hyacinthinus MO
~~S.
,
_S. u.garmaniKS
_
"
o.Oo
0.16
0.08
0.24
clarki
~~~~~~~~S.
0.32
0.40
Distance from Root
FIG. 1.-Fitch-Margoliash
tree portrayingthe relationshipsamong the populationsof S. undulatus and S.
clarki. Populationand species abbreviationsare given in Table 3.
evident in all optimizations. Three transitions occurred from a canyonlands ancestor, whereas one transition was from a
grasslands ancestor. In two trees (likelihood and parsimony), an eastern woodlands population (S. undulatus from Mississippi) evolved quite early. However, the
Fitch-Margoliash tree suggests that the
grasslands populations evolved first. Optimization of habitat on the parsimony tree
resulted in one instance of a grassland ancestor giving rise to a canyonlands species.
DISCUSSION
Although considerable amounts of allozyme variability may be expected in a
wide-ranging or polytypic species, the levels of differentiation observed among populations of S. undulatus are large relative
to some previously reported estimates of
divergence between other phrynosomatid
lizard species (Sites et al., 1988, S. grammicus complex, 0.0-0.162; Aguilars-S et
al., 1988, Petrosaurus mearnsi and P. thalassinus, 0.132). Our estimates are low relative to other among-species comparisons
(e.g., de Queiroz, 1992, sceloporine sand
lizards; Mink and Sites, 1996, S. scalarHs
complex, 0.00-0.71). Published estimates
of intraspecific differentiation in other lizard taxa tend to be even lower (e.g., Adest,
1977, 1987, Callisaurus; Sattler and Reis,
1995, Phrynosoma; but see Bezy and Sites,
1987; Zamudio et al. 1997). Therefore, our
results indicate a significant amount of genetic structuring among the surveyed populations of S. undulatus. A notable result
is the absence of fixed differences among
the populations of S. undulatus. The lack
of fixed allelic differences argues that S.
286
HERPETOLOGICA
[Vol. 58, No. 3
S. u. hyacinthinusMS
S. occidentalis
S. virgatus
{~~
{
S. u. undulatusFL
6
l
I
X
~~S.u. hyacinthinusOH
+
rA
~~~59
S. u. undulatusSC
S. woodi
S.u. elongatusUT
u. tristichusc. AZ
__S.
NM
S. u. tristichus
1
S1.1 Su.
tristichusNo. AZ
S. u. garmaniKS
rS.u. garmaniNE
~~S.u. hyacinthinus
MO
<
a
g
t
Bootp vs
l
o.oo
>.
I
e
a_ sw
l
0.10
s.Nconso brinusTX
ae
te b
l
S. clark
s A
l~~~~j
0.20
lI
i
|
0.30
0.40
Distance from Root
FIG. 2.-Maximum Likelihood phylogramof S. undulatus using S. clarki as the outgroup. Bold branches
are strongly supported by the ML analysis. Non-significant branches canl be collapsed to yield polytomies.
Bootstrap values >50 are shown above the branches. Abbreviations of the terminal units are as in Fig. 1.
undulatus comprises one large interbreeding species. Interestingly,we also demonstrate that other species have emerged
from within S. undulatus, which is consistent with conclusions of Wiens and Reeder
(1997).
The subspecific designations of S. undulatus have largely been based on external phenotypic traits: patterns of coloration, geographicvariationin scalation,and
body size. For example, a recent descrip-
tion of S. u. tedbrowni used size, scalation,
and dorsal color pattern for diagnosis
(Smith et al., 1992). Apart from studies by
Spohn and Guttman (1976), Rachuk
(1987), and Wiens and Reeder (1997), little information is available about genetic
divergence among the subspecies of S. undulatus. Our analyses based on allele frequencies suggest that the subspecies designations do not reflect patterns of genetic
relatedness.
HERPETOLOGICA
September 2002]
287
S. u. tristichus NM
53
S. u. tristichusNo. AZ
S. u. hyacinthinus OH
83
S. u. undulatusFL
__ S. u.elongatus UT
S. u undulatusSC
53
_
woodi
~~~~~~~~S.
S. u. trisntchusc. AZ
S. u. garmaniNE
I
r
_
70
L
{
:
irgatus
p~~~~~~~.
occidentalis
~~~~~~~~~~~S.
u. garmani KS
~~~~~~~S.
S. u. consobrinus TX
S. u. hyacinthinusMO
S. u. hyacinthinus MS
S.clarki
0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 5.0 5.5 6.0 6.5 7.0 7.5 8.0 8.5
FIG. 3.-Estimated
phylogeny of the S. undulatus group based on parsimony analysis. The tree is presented
as a phylogram, with branch lengths drawn proportional to the estimated amount of evolutionary change.
Bootstrap values >50 are shown above the branches.
Evolutionary Relationships among
Populations of S. undulatus
In a more extensive phylogenetic analysis of species relationships within Sceloporus, Wiens and Reeder (1997) included
seven subspecies of S. undulatus in a cladistic analysis of morphological and molecular data. Their tree suggests that S. undulatus is a polyphyletic taxon, with several species of Sceloporus derived within
S. undulatus. Notably, Wiens and Reeder
(1997) also found that the eastern and
western populations of S. undulatus were
more closely related to one another than
either was to the central or plains populations. Unfortunately, Wiens and Reeder
did not include multiple populations of
each subspecies as terminal units, hence
our results are not completely comparable
with theirs. Nevertheless, our results support the conclusions of Wiens and Reeder
(1997) regarding the pattern of relationships among geographic races. For example, we also show that the eastern and
western populations of S. undulatus are
closely related. Unraveling evolutionary
relationships among the populations is
likely to be complicated, because of the
possibility that other species may have
been derived from within S. undulatus (K.
de Queiroz, personal communication;
Wiens and Reeder, 1997). The placements
of S. woodi, S. virgatus, and S. occidentalis
revealed by Wiens and Reeder (1997)
were similar to those in our analysis. For
example, the tree based on DNA data
[Vol. 58, No. 3
HERPETOLOGICA
288
3- r
2
2
S. woodi
S. u. undulatus SC
S. u. tristichus NM
_________________
S. u. elongatus UT
S. u. tristichus c. AZ
_
,_____,_________
S. u. tristichus
No. AZ
S. u. undulatus FL
3{
S. u. hyacinthinusOH
3
S. u. hyacinthinus
MO
S. u. consobrinusTX
2
2
_
S. u. garmani
NE
S. u. garmani
KS
S. virgatus
S. occidentalis
I____________________________
S.u.hyacinthinusMS
S. clarki
FIG. 4.-Taxonomic congruence tree. This tree presents only those clades that were present in the shortest
trees from the Fitch-Margoliash, Continuous Maximum Likelihood, and Parsimony analyses. The numbers at
each node indicate the number of times the clade occurred among the three trees.
(Wiens and Reeder, 1997, their figure 2)
places S. woodi with a population of S. u.
undulatus, which is consistent with our results. Their analysis did not place S. virgatus and S. occidentalis as sister taxa as
in our Fitch-Margoliash and likelihood
trees. However, the parsimony tree positioned both species within a clade consisting of S. u. garmani and S. u. consobrinus,
which is similar to the result given in
Wiens and Reeder (1997).
The genetic relationships among the
populations of S. undulatus are inconsistent with current subspecific designations,
based on scale characters, numbers of
thigh pores, and coloration. For example,
the consensus tree shows that two subspecies are paraphyletic (S. u. tristichus, S. u.
garmani) and two are polyphyletic (S. u.
undulatus, S. u. hyacinthinus). Some of
the subspecies relationships suggested by
Smith et al. (1992), an eastern North
American arboreal group (S. u. undulatus
and S. u. hyacinthinus), and a western
North American saxicolous group (S. u.
tristichus, S. u. elongatus, and S. u. erythrocheilus) also are not supported by our
analysis. However, we did identify a midwestern/grasslands group similar to the
Great Plains/terrestrial group of Smith et
al. (1992) that contained S. u. garrnani and
S. u. consobrinus. Unlike Smith et al.
(1992), this grassland clade also contained
a population of S. u. hyacinthinus. We
found that the Missouri population, which
would have been placed by other authors
in the eastern woodland group based on
its subspecific designation, instead falls
within the midwestern grasslands lineage.
Several studies have suggested that S.
Tree
Fitch-Margoliash
S. occidentalis
\
289
HERPETOLOGICA
Septemnber2002]
\
\
)
}
\\
ContinuousMaximumLikelihood Tree
S. virgatus
S. u. undulatusMS
S. u. hyacinthinusOH
S. u. hyacinthinusOH
S. u. undulatusFL
S. u. undulatusFL
S. u. undulatusSC
S. u. tristichusNM
S. u. woodi
S. u. tristichusc AZ
S. u. elongatus UT
S. u. elongatus UT
S. u. tristichusc AZ
S. u. undulatusSC
S. u. tristichus NM
u. wood!
~~~~~~S.
S. u. tristichusAZ
S. u. tristichusAZ
S. u. garminiKS
~~~~S.
u. garmaniICS
S. u. hyacinthinusMO
S. u. hyacinthinusMO
Habitat
EasternWoodland_
WXVestem
Canyonland
Grassland
\+
S. occidentalis
S. u. virgatus
S. u. consobrinusTX
S. u. consobrinusTX
S. u. garminiNE
S. u. garmaniNE
S. u. undulatusMS
'NS. clarkic
trees of the S. undulatus
5.-Phylogenetic
group showing optimization of the habitat/geography
character on the Fitch-Margoliash tree. Shading of
the branches indicates the character state for each
population or species.
FIG.
undulatus may represent a species comet al., 1998;
plex (see Lemos-Espinal
Wiens and Reeder, 1997). The placement
of recognized species such as S. virgatus,
S. woodi, S. occidentalis, S. exsul, and S.
cautus within S. undulatus suggests that
either the subspecies of undulatus should
be considered (1) as distinct species, (2)
some of the presently recognized species,
e.g., S. woodi, may be subspecies or races
within S. undulatus, or (3) that S. undulatus is a large, variable interbreeding species and, despite giving rise to several other species, S. undulatus maintains its cohesion as a species (Wiens, personal communication). Whether such designations
are appropriate will require additional molecular and morphological analysis. The
absence of fixed allele differences, lack of
differentiation, and the abundance of evidence of hybridization among the subspecies that we surveyed do not support the
elevation of any of the populations of S.
undulatus to the status of species.
In summary, we believe that the patterns of genetic relationships among the S.
undulatus populations mirror the results of
similar studies that have investigated the
patterns of genetic variation of other geographically widespread species (Irschick
S. clarki
trees of the S. undulatus
FIG. 6.-Phylogenetic
group showing optimization of the habitat/geography
character on the continuous likelihood tree. Shading
of the branches indicates the character state for each
population or species.
and Shaffer, 1997; Mulcahy and Mendelson, 2000, Rodriguez-Robles and JesusEscobar, 2000; Weisrock and Janzen, 2000;
Zink and Dittman, 1993). Such studies
have revealed weak phylogeographic structuring among populations. Generally, the
MaximumParsimonyTree
S. u. tristichusNM
S. u. tristichusAZ
S. u. undulatusFL
S. u. hyacinthinusOH
S. u. elongatus UT
S. u. undulatusSC
S. u. woodi
S. u. tristichusc AZ
S. u. garmaniNE
S. occidentalis
S. virgatus
S. u. garmaniKS
S. u. hyacinthinusMO
S. u. consobrinusTX
S. u. undulatusMS
S. clarki
trees of the S. undulatus
FIG. 7.-Phylogenetic
group showing optimization of the habitat/geography
character on the maximum parsimony tree. Shading
of the branches indicates the character state for each
population or species.
290
HERPETOLOGICA
evidence shows that geographically proximate populations are not necessarily closely related. Zink and Dittman (1993) argued that three factors may account for
such a pattern. First, the present distribution may reflect relatively recent colonization events from a geographically restricted ancestral population. The low levels of genetic differentiation would be consistent
with a historic
population
bottleneck followed by rapid range expansion. Hence, there has been relatively little
time for geographic differentiation to occur. Second, there may be high levels of
gene flow. Third, there could be similar
rates of gains or losses of alleles.
The patterns emerging from our analysis
of S. undulatus are largely consistent with
the first hypothesis of Zink and Dittman
(1993). For example, apart from the close
relationship between the grassland populations, we found little correspondence between genetic similarity and geographic
proximity (note the placement of Florida
and Ohio, or South Carolina with the
western populations). We argue that the
recency of divergence among the various
eastern and western populations has limited the opportunity for differentiation.
Hence, we found no evidence that geographical races are reflected in genetic differentiation. Therefore, we have the scenario where "morphology" (scalation and
coloration) has evolved at a different rate
than molecules and suggests that the subspecies reflect convergence in morphology.
Acknowledgments. -We thank K. Kelly, M. A.
Robson, M. Hohmann, D. Irschick, and D. Gluesenkamp for assistance at various stages in this project.
W Parker allowed us to collect individuals on his
study site. J. Losos kindly sent specimens from Missouri. J. Congdon allowed P. Niewiarowski to collect
individuals from the Savannah River Ecological Laboratory site. K. de Queiroz tolerated our questions
regarding phylogenetic inference. Denise Anderson
drew the phylogenetic trees. We thank M. Morris, K.
de Queiroz, C. J. Cole, J. Wiens, and two anonymous
reviewers for critical comments and suggestions. D.
B. Miles was supported by NSF BSR 86-17688 and
IBN 92-07895 and a grant from the National Geographic Society. A Baker Fund Award to D. B. Miles
and M. M. White also supported various stages of the
project. W A. Roosenburg was supported by an Ohio
University Postdoctoral Fellowship.
[Vol. 58, No. 3
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