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Unisexual Lizards (Genus Cnemidophorus)
of the Madrean Archipelago
Charles J. Cole1 and Herbert C. Dessauer
2
Abstract.-About 20 species of Cnemidophorus occur in the vicinity of
the Sky Islands of the southwestern United States and northwestern
Mexico, in habitats ranging from woodland to desert. Many of these
whiptail lizards occur in populations with a 50:50 sex ratio, and
reproduction depends on mating and internal fertilization. However, half
of the species of the Madrean Archipelago are unisexual species for
which only females exist. These remarkable vertebrates are important
biological resources for basic research.
Here we review our comparative multidisciplinary research on
reproduction, genetics, evolutionary biology, and systematics,
integrating field and laboratory investigations. Results include the
following: (1) females of the unisexual species reproduce independently
by parthenogenetic cloning; (2) a diversity of clones occupies the area,
including both diploid and triploid species; (3) the unisexual species
originated from F1 hybrids among bisexual species, and various unique
combinations of hybrids were involved; (4) in each instance, the switch
from
sperm-dependent
reproduction
to
sperm-independent
reproduction occurred in a single generation; and (5) these remarkable
animals have considerable potential for improving knowledge of
reproductive biology and other basic phenomena in addition to revealing
the natural history of the Madrean Archipelago and adjacent lands.
BISEXUAL AND UNISEXUAL SPECIES
Whiptaillizards of the genus Cnemidophorus
(fig. 1) are alert, wary, and fast terrestrial animals
that forage actively (usually for insects) in sunny
habitat$. There are about 50 species in the genus,
their composite ranges extending from about the
southern two-thirds of the United States southward through Mexico and Central America to and
throughout much of South America east of the
Andes (for reviews see Maslin and Secoy, 1986;
Wright, 1993).
Most species of whiptail are bisexual species
(Le., populations consist of males and females in a
50:50 sex ratio). In these, reproduction requires
mating, and fertilization is internal (for the reproductive biology of a bisexual species, see
Goldberg and Lowe, 1966).
Figure 1.-Cnemldophorus sonorae, a triploid unisexual species
(reproduced from Dessauer and Cole, 1989, fig. 2F; reptile
specimen number 126976 of the American Museum of Natural
History, New York).
Approximately one-quarter of the species of
Cnemidophorus, however, are unisexual species.
In these, only one sex exists; all individuals are
females (Minton, 1959; Duellman and Zweifel,
1962; Maslin, 1962).
The whiptail fauna of the Madrean Archipelago includes approximately 20 species (Table 1),
of which about half are unisexual. This represents
the largest concentration of all-female species and
1Curator in Herpetology, American Museum of Naturel History, Cen-
tral Park West at 79 Street, New York, NY 10024-5192.
2Professor Emeritus in Biochemistry and Molecular Biology, Louisiana State University Medical Center, 1100 Florida Avenue, New
Orleans, LA 70119-2799.
267
already under study for other vertebrates, particularly some fishes and salamanders (for reviews,
see Reinboth, 1975; Dawley and Bogart, 1989), but
true parthenogenesis (development of eggs in the
complete absence of sperm) waS not documented
as the normal means of reproduction in any species of vertebrate prior to 1981.
The best way to obtain controlled data on
these questions was to establish colonies in the
laboratory and observe the development of multiple generations within individual family trees
(lineages) of known ancestry and relationships.
With this approach (for methods of maintaining
colonies see Townsend, 1979; Townsend and Cole,
1985), the following has been demonstrated about
unisexual species: (1) their eggs develop in the
absence of males; (2) all normal hatchlings are immature females that go through the same
maturation process as the females of bisexual species; (3) the lizards are not self-fertilizing
hermaphrodites and completely lack testicular tissue, spermatozoa, and males; and (4)
consequently, we must conclude that their eggs
develop parthenogenetically (Hardy and Cole,
1981).
their bisexual relatives found anywhere on Earth
(Wright and Lowe, 1968). For reviews of unisexual
lizards, including those in other genera, see Cole
(1975) and Darevsky (1992).
REPRODUCTION IN UNISEXUAL SPECIES
After realizing that certain population samples
of Cnemidophorus consisted of females only, herpetologists collected additional specimens in
expectation of finding males. Nevertheless, males
consistently failed to materialize for certain populations. Consequently, several biologists began
investigating reproduction of the all-female lizards, particularly after seeing Darevsky's (1958)
intriguing pioneering studies of unisexual lizards
(genus Lacerta) from Armenia, the first report of
apparently normal unisexuality in reptiles.
Anatomical and histological studies of fieldcaptured lizards suggested that the reproductive
tracts in females of unisexual species were similar
to those in females of bisexual species (e.g., Cuellar, 1968, 1970; Christiansen, 1971). However,
several questions concerning unisexual species
still required attention, such as: (1) are the eggs of
these species triggered to develop by sperm from
males of other species; (2) do these females actually begin life as males but undergo sex-reversal
while growing up; (3) are these females actually
hermaphrodites that fertilize their own,. eggs; and
(4) do these females produce offspring from unfertilized eggs (Le., by true parthenogenesis)?
Rare examples for questions (1) through (3) were
PATTERNS OF INHERITANCE
The fact that unisexual species rep rod uce
parthenogenetically raises the question of
whether their offspring exhibit less variation than
do those of bisexual species. This requires understanding popUlation genetics both in bisexual and
unisexual species.
PopUlation genetics of bisexual species has
been studied extensively in lizards of the genera
Sceloporus (reviewed by Sites et al., 1992) and
Cnemidophorus (e.g., Dessauer and Cole, 1989,
1991). Patterns of inheritance of chromosomes occurring in heteromorphic pairs (e.g., sex
chrolnosomes and chromosomal aberrations) and
of proteins encoded by specific gene loci (including I-Iardy-Weinberg analyses of frequencies of
alternative alleles), show that bisexual lizards are
diploid outcrossing species with the same Mendelian inheritance that typifies other vertebrates,
such as birds and mammals (including humans)
Offspring resulting from different eggs and sperm
from the same parents (or different ones) exhibit
individual variation due to chromosomal crossing
over and random assortment and segregation in
meiosis, as well as rare mutationso
In contrast, females of unisexual species of
Cnemidophorus produce offspring that are ge-
Table 1.-Species of whiptail lizards (Cnemidophorus) in and
near the Madrean Archipelago (modified from Table 1 of
Dessauer and Cole, 1989, using some names from Wright,
1993).
SpeCies
C. burti
C. costatus
C. dixon;
C. exsanguis
C. fJagel/icaudus
C. grahamii
C. gu/aris
C. inornatus
C. /aredoensis
C. neomexicanus
C. opatae
C. scalaris
C. septemvittatus
C. sexlineatus
C. sonorae
C. tesse/atus
C. tigris
C. uniparens
C. ve/ox
Reproduction
bisexual
bisexual
unisexual
unisexual
unisexual
unisexual
bisexual
bisexual
unisexual
unisexual
unisexual
bisexual
bisexual
bisexual
unisexual
unisexual
bisexual
unisexual
unisexual
Ploidy
2n
2n
2n
3n
3n
2n
2n
2n
2n
2n
3n
2n
2n
2n
3n
3n
2n
3n
3n
0
268
netic ally identical to each other, to their mother,
grandmother, and so-on, excepting rare mutations. In other words, a lineage of these lizards is a
clone. This has been demonstrated by analyzing
patterns of inheritance at both the level of whole
chromosomes and individual gene products in
lineages of known ancestry raised through multiple generations in the laboratory (e.g., Cole, 1979;
Dessauer and Cole, 1984, 1986). In addition, some
of the unisexual species are triploid clones, each
individual possessing cells with three sets of functional chromosomes and genes instead of two
(e.g., C sonorae; for a review, see Dessauer and
Cole, 1989).
VEL
UNI
ORIGINS OF UNISEXUAL CLONES BY
HYBRIDIZATION
SON
TES
FLA
EXS
Figure 2.-Hypotheses of phylogenetic relationships of the bisexual
and unisexual species of Cnemldophorus occurring In and near
the Madrean Archipelago, modified from Dessauer and Cole,
1989, fig. 14. Each species Is indicated by the first three letters
of Its name (Table 1), except for 2X, which has not yet been
Identified In nature. Double lines to VEL and UNI Illustrate
multiple hybrid origins, based on mitochondrial DNA data
showing that 2X was formed by reciprocal crosses between INO
and BUR (Densmore et at, 1989b; Moritz et at, 1989b).
The comparative investigations in genetics of
Cnemidophorus indicated not only their patterns
of inheritance, but also hypotheses for the evolutionary relationships of the species. The evidence
from chromosomes, individual gene products
(with over three dozen independent loci analyzed
in the most recent studies), comparative anatomy,
geographic distribution, and habitat preferences
all demonstrate that the unisexual species in the
Madrean Archipelago arose as a consequence of
interspecific hybridization among the bisexual
species (e.g., Lowe and Wright, 1966; Neaves and
Gerald, 1968, 1969; Neaves, 1969; Parker and Selander, 1976, 1984; Dessauer and Cole, 1989).
A preliminary analysis of the relationships of
the bisexual Cnemidophorus from the Madrean
Archipelago was presented by Dessauer and Cole
(1989), who used UPGMA clustering of genetic
distance data based on about three dozen gene
loci. The same clustering of these species was obtained independently from mitochondrial DNA
(Moritz et al., 1992b). Currently this hypothesis is
being tested again by modern cladistic methods
(e.g., Hillis et al., 1994), and it will be modified if
appropriate. Meanwhile, we illustrate our hypothesis here in the form of a cladogram (fig. 2),
upon which we have also superimposed our preferred hypotheses for the hybrid origins of the
derived unisexual species (Dessauer and Cole,
1989).
The diploid unisexual species had one step of
hybridization involved in their origin. For example, the unisexual C neomexicanus (NEO in fig. 2)
resulted from hybridization between the bisexual
C. tigris (TIG in fig. 2) and C inornatus (INO in
fig. 2). The diploid clone of this hybrid is perpetu-
ated parthenogenetically today, as sterile male hybrids that may also have been produced originally
have died out (see below). We have no evidence
that new hybrids of this combination have been
produced in recent years (Cole et al., 1988).
Two steps of hybridization were involved in
the origin of the triploid unisexual species (fig. 2).
For example, the unisexual C grahamH (GRA in
fig. 2, using the name applied by Wright, 1993)
resulted from hybridization between the bisexual
C. tigris and C. septemvittatus (SEP in fig. 2;
Wright and Lowe, 1967; Neaves, 1969; Parker and
Selander, 1976; Dessauer and Cole, 1989). While
the resulting unisexual clone continues to perpetuate itself parthenogenetically, on at least one
occasion in the past a female of C grahamH mated
with a male of C. sexlineatus (SEX in fig. 2). The
spenn added a third set of chromosomes and
genes to the diploid egg cloned by the female and
produced a triploid hybrid. The triploid clone of
this hybrid is perpetuated parthenogenetically today as C tesselatus (TES in fig. 2). Thus, the
triploid C tesselatus is comprised of three haploid genomes ultimately inherited from three
different bisexual species, through two separate
events of hybridization (Neaves, 1969; Parker and
Selander, 1976; Dessauer and Cole, 1989). In addition, rare tetraploid hybrids are produced by
occasional mating between triploid clonal females
and males of bisexual species (e.g., Lowe et al.,
1970; Cole, 1979).
269
Several of the triploid unisexual species originated through an intermediary diploid clone
indicated as 2X in figure 2, which resulted from
hybridization between C inornatus and C burtl
This intermediary diploid clone has not been
identified with certainty in nature as yet, although
future research may reveal it among the C opatae
complex (Dessauer and Cole, 1989; Wright, 1993)
or C. innotatus (as that name is applied by Wright,
1993). Either hypothesis or both could be correct,
as various triploid clones and multiple hybridization events are involved (fig. 2).
INSTANTANEOUS SPECIATION
The process by which ancestral populations of
diploid bisexual species diverge over time and
prod uce one or more new species generally requires a minimum of hundreds, thousands, or
tens of thousands of generations to complete
through mutation and natural selection, particularly to the extent of developing reproductive
isolation. In stark contrast, all of the evidence suggests that parthenogenetic clones of hybrid origin
arise in a single generation (e.g., Cole, 1985).
In situations today where hybridization occurs
among bisexual populations distinguished by low
genetic differentiation, a hybrid zone of fertile hybrids is formed (e.g., Dessauer and Cole, 1991).
Panmixia is sufficiently extensive that.FI generation hybrids are rare or absent. All lizards in the
center of the hybrid zone are F2 and subsequent
generation hybrids or backcross hybrids with
various combinations of alleles from the parental
populations. This kind of hybrid swarm is not the
situation from which parthenogenetic cloning
emerges.
Parthenogens are derived from hybridization
among bisexual populations distinguished by
high genetic differentiation (but not so high as to
prevent development of viable hybrids; Dessauer
and Cole, 1989; Moritz et al., 1989a). The most detailed analyses of the combinations of genomes
and morphology in clonal lizards (Cnemidophorus and other genera as well) indicate that the
clone in each instance most likely arose instantaneously from a first-generation hybrid female.
This suggests that the PI hybrid males that might
have been produced were sterile and became extinct after contributing no genes to subsequent
generations while one or more PI hybrid females
perpetuated the PI state by parthenogenetic cloning. Given the number of independent cases
where hybridization has led to clones (e.g., fig. 2),
it seems unlikely that in each case the two rare
events of unusual hybridization and an even rarer
mutation conferring a new capacity for parthenogenesis on a hybrid female
occurred
simultaneously. Consequently, it seems likely that
there is a cause-and-effect relationship between
hybridization among well-differentiated populations and the origin of parthenogenesis, perhaps
through dysfunction in meiosis (e.g., Densmore et
al., 1989a; Moritz et al., 1989a, 1992b). It is a staggering thought that the
switch from
sperm-dependent to sperm-independent reproduction occurs in a single generation. Together
with Wade C. Sherbrooke at the Southwestern Research Station in the Chiricahua Mountains, we
are now conducting experiments to address this
question.
CLONAL DIVERSITY
Considering that the bisexual species of
Cnemidophorus show various differences in their
genetic material, it is clear that hybridization
among different combinations of bisexual species
results in various genetically distinct clones (fig.
2). There are other sources of clonal diversity also.
Comparative studies of individual gene products by protein electrophoresis have revealed two
or more minor genetic variants in otherwise similar clones within unisexual species (e.g.; C
tesselatus, see Parker and Selander, 1976; C
neonlexicanus, see Parker and Selander, 1984; and
C cryptus, see Cole and Dessauer, 1993). For the
cases cited, the allelic variants observed in the
unisexual species appeared also in one or the
other of the parental bisexual species. This suggests that the slightly different unisexual clones
arose from separate FI hybrids resulting from different combinations of eggs and sperm from the
parental species, even though in some cases the
same individual mother and father could have
been involved.
The laboratory of Wesley M. Brown at the University of Michigan has produced some elegant
work on comparative analyses of mitochondrial
DNA (mtDNA). The beauty of this is that mtDNA
is inherited in the cytoplasm of the egg, contributed by the mother and not the father.
Consequently, when the parental species of a
clont~ differ in mtDNA, identification of the
mtDNA in the unisexual clone determines which
parental species was the maternal ancestor of the
clont! (e.g., Brown and Wright, 1979). By such
analyses, Densmore et al. (1989b) and Moritz et al.
270
(1989b) determined that the diploid unisexual intermediary clone referred to as 2X in figure 2
probably was created by hybridization at least
twice, by reciprocal crosses (lNO female x BUR
male, and BUR female x INO male).
By conservative estimate, adding up the
strong indications for separate hybrid origins of
diploid unisexual species (Densmore et al., 1989a,
b; Dessauer and Cole, 1989; Moritz et al., 1989b,
1992a; Cole and Dessauer, 1993), parthenogenetic
cloning probably had at least 10 independent origins within Cnemidophol"US, but the actual
number may be considerably higher. The majority
of these occurred within or near the Madrean Archipelago, where there may have been more
separate origins of parthenogenetic lizards than in
any other comparable-sized area on Earth (but see
Moritz et al., 1989c, for data on unisexual lizards
in Australia). We suspect that the reason such diversity has arisen here hinges upon the diverse
native bisexual species, diverse habitats that have
shifted throughout the Pleistocene and Recent
(e.g., Lowe et al., 1970), and the fact that mating in
Cnemidophorus does not involve the more elaborate courtship-related behaviors seen in other
lizards. Thus, the local frequency of hybridization
is greater in Cnemidophorus than in other lizards,
and; as discussed above, there may be a causeand-effect relationship between hybridization and
the origin of parthenogenetic cloning.
Finally, genetic mutations can occur in lizards
of a clone, just as they can in bisexual species. If a
non-lethal mutation occurs within a clonal lizard,
both the original gene (still present in other individuals) and the derived mutant will be
perpetuated by parthenogenetic cloning (e.g.,
Parker and Selander, 1976). Examples of such
karyotypic clones were discussed in detail by Cole
(1979) and of an allelic clone at the transferrin locus by Dessauer in Cole et al. (1988). In the few
studies of geographic variation of clones within
unisexual Cnemidophorus (Parker and Selander,
1976, 1984; Dessauer and Cole, 1989), different
clones distinguished by allelic variation have been
found. In many cases, the source of this variation
(separate hybrid eggs or gene mutations in
parthenogenetic lineages?) remains unknown.
(1) As yet, we know nothing about the sections of
DN A that affect meiosis and cause parthenogenesis to occur in some hybrid females. With
a better understanding of the mechanics and
processes involved, it might become possible
to convert animals and plants of agricultural
importance to parthenogenetic reproduction.
This would greatly improve efficiency of production, as all normal individuals would bear
progeny of known qualities. Experimental
breeding, genetic engineering in other respects, and related activities would still be
important for improving stocks, but as desirable stocks were developed they could be
cloned. This might seem far-fetched if we
were not actually seeing this happen in vertebrates in nature.
(2) As yet, we do not know what activates cloned
eggs to initiate embryonic development in the
absence of sperm. All we do know about this
process is that the mature ovum, after meiosis, is genetically complete in the appropriate
environment (Cuellar, 1971), so there seems
to be no need to await fertilization. In fact, for
haploid, un-cloned ova of bisexual species,
do we know enough about the normal processes involved in their brief period of waiting
for fertilization before being shed through the
system?
(3) In general, we have a great deal to learn about
the effects of exposing wildlife and humans
to pathogens, pollutants, radiation, and
newly manufactured chemicals. In addition,
appropriate animals can be used for research
on the general phenomena of nutrition and
aging, as well as captive propagation of endangered species (e.g., Porter et al., in press).
Unisexual lizards are especially suited to such
research because all individuals are identical
within a clone and the affects of genetic variation are reasonably controlled (e.g., Cole and
Townsend, 1990).
(4) While a good start has been made (e.g., Schall,
1978; Price, 1992; various chapters in Wright
and Vitt, 1993; Walker et al., 1994), a great
deal remains to be learned about the biology
of Cnemidophorus, including the populations in and around the Sky Islands.
CURRENT AND FUTURE RESEARCH
MANAGEMENT CONSIDERATIONS
There are several areas of research and experimentation for which unisexual lizards and their
bisexual relatives are most suitable, including the
following:
Unisexual lizards and their bisexual relatives
are important biological resources with considerable potential for future, productive research, and
271
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as such they should be conserved. In most cases,
active conservation activities are not necessary because most species of these lizards are not
currently threatened in nature. However, these
lizards depend upon the continued existence of
their woodland, grassland, desert-grassland, and
desert environments (specific habitats and distribution depending on the species), and some
populations are quite locally restricted in geographic distribution.
Consequently, our main recommendation is to
keep avenues of communication open, as in the
spirit of this informative conference. Directors of
research stations and herpetologists should be involved as plans are developed to change land uses
in relevant areas that could severely impact the
lizards and/or scientists' long-term research programs.
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