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Unisexual Lizards (Genus Cnemidophorus) of the Madrean Archipelago

Charles J. Cole1 and Herbert C. Dessauer2

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 south­ ward 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). Figure 1.-Cnemldophorus sonorae, a triploid unisexual species (reproduced from Dessauer and Cole, 1989, fig. 2F; reptile Most species of whiptail are bisexual species specimen number 126976 of the American Museum of Natural (Le., populations consist of males and females in a History, New York). 50:50 sex ratio). In these, reproduction requires mating, and fertilization is internal (for the repro­ Approximately one-quarter of the species of ductive biology of a bisexual species, see Cnemidophorus, however, are unisexual species. Goldberg and Lowe, 1966). In these, only one sex exists; all individuals are females (Minton, 1959; Duellman and Zweifel, 1962; Maslin, 1962). 1Curator in Herpetology, American Museum of Naturel History, Cen­ The whiptail fauna of the Madrean Archipel­ tral Park West at 79 Street, New York, NY 10024-5192. ago includes approximately 20 species (Table 1), 2Professor Emeritus in Biochemistry and Molecular Biology, Louisi­ ana State University Medical Center, 1100 Florida Avenue, New of which about half are unisexual. This represents Orleans, LA 70119-2799. the largest concentration of all-female species and

267 their bisexual relatives found anywhere on Earth already under study for other vertebrates, particu­ (Wright and Lowe, 1968). For reviews of unisexual larly some fishes and salamanders (for reviews, lizards, including those in other genera, see Cole see Reinboth, 1975; Dawley and Bogart, 1989), but (1975) and Darevsky (1992). true parthenogenesis (development of eggs in the complete absence of sperm) waS not documented as the normal means of reproduction in any spe­ REPRODUCTION IN UNISEXUAL SPECIES cies of vertebrate prior to 1981. The best way to obtain controlled data on After realizing that certain population samples these questions was to establish colonies in the of Cnemidophorus consisted of females only, her­ laboratory and observe the development of multi­ petologists collected additional specimens in ple generations within individual family trees expectation of finding males. Nevertheless, males (lineages) of known ancestry and relationships. consistently failed to materialize for certain popu­ With this approach (for methods of maintaining lations. Consequently, several biologists began colonies see Townsend, 1979; Townsend and Cole, investigating reproduction of the all-female liz­ 1985), the following has been demonstrated about ards, particularly after seeing Darevsky's (1958) unisexual species: (1) their eggs develop in the intriguing pioneering studies of unisexual lizards absence of males; (2) all normal hatchlings are im­ (genus Lacerta) from Armenia, the first report of mature females that go through the same apparently normal unisexuality in reptiles. maturation process as the females of bisexual spe­ Anatomical and histological studies of field­ cies; (3) the lizards are not self-fertilizing captured lizards suggested that the reproductive hermaphrodites and completely lack testicular tis­ tracts in females of unisexual species were similar sue, spermatozoa, and males; and (4) to those in females of bisexual species (e.g., Cuel­ consequently, we must conclude that their eggs lar, 1968, 1970; Christiansen, 1971). However, develop parthenogenetically (Hardy and Cole, several questions concerning unisexual species 1981). 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 actu­ PATTERNS OF INHERITANCE ally begin life as males but undergo sex-reversal while growing up; (3) are these females actually The fact that unisexual species rep rod uce hermaphrodites that fertilize their own,. eggs; and parthenogenetically raises the question of (4) do these females produce offspring from un­ whether their offspring exhibit less variation than fertilized eggs (Le., by true parthenogenesis)? do those of bisexual species. This requires under­ Rare examples for questions (1) through (3) were standing popUlation genetics both in bisexual and unisexual species. PopUlation genetics of bisexual species has Table 1.-Species of whiptail lizards (Cnemidophorus) in and near the Madrean Archipelago (modified from Table 1 of been studied extensively in lizards of the genera Dessauer and Cole, 1989, using some names from Wright, Sceloporus (reviewed by Sites et al., 1992) and 1993). Cnemidophorus (e.g., Dessauer and Cole, 1989, SpeCies Reproduction Ploidy 1991). Patterns of inheritance of chromosomes oc­ C. burti bisexual 2n C. costatus bisexual 2n curring in heteromorphic pairs (e.g., sex C. dixon; unisexual 2n chrolnosomes and chromosomal aberrations) and C. exsanguis unisexual 3n of proteins encoded by specific gene loci (includ­ C. fJagel/icaudus unisexual 3n C. grahamii unisexual 2n ing I-Iardy-Weinberg analyses of frequencies of C. gu/aris bisexual 2n alternative alleles), show that bisexual lizards are C. inornatus bisexual 2n diploid outcrossing species with the same Mende­ C. /aredoensis unisexual 2n C. neomexicanus unisexual 2n lian inheritance that typifies other vertebrates,

C. opatae unisexual 3n such as birds and mammals (including humans) 0 C. scalaris bisexual 2n Offspring resulting from different eggs and sperm C. septemvittatus bisexual 2n C. sexlineatus bisexual 2n from the same parents (or different ones) exhibit C. sonorae unisexual 3n individual variation due to chromosomal crossing C. tesse/atus unisexual 3n over and random assortment and segregation in C. tigris bisexual 2n C. uniparens unisexual 3n meiosis, as well as rare mutationso C. ve/ox unisexual 3n In contrast, females of unisexual species of Cnemidophorus produce offspring that are ge-

268 VEL SON netically identical to each other, to their mother, UNI TES FLA EXS grandmother, and so-on, excepting rare muta­ tions. 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 multi­ ple 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 func­ tional chromosomes and genes instead of two (e.g., C sonorae; for a review, see Dessauer and Cole, 1989).

ORIGINS OF UNISEXUAL CLONES BY Figure 2.-Hypotheses of phylogenetic relationships of the bisexual HYBRIDIZATION 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 The comparative investigations in genetics of of Its name (Table 1), except for 2X, which has not yet been Cnemidophorus indicated not only their patterns Identified In nature. Double lines to VEL and UNI Illustrate of inheritance, but also hypotheses for the evolu­ multiple hybrid origins, based on mitochondrial DNA data showing that 2X was formed by reciprocal crosses between INO tionary relationships of the species. The evidence and BUR (Densmore et at, 1989b; Moritz et at, 1989b). from chromosomes, individual gene products (with over three dozen independent loci analyzed ated parthenogenetically today, as sterile male hy­ in the most recent studies), comparative anatomy, brids that may also have been produced originally geographic distribution, and habitat preferences have died out (see below). We have no evidence all demonstrate that the unisexual species in the that new hybrids of this combination have been Madrean Archipelago arose as a consequence of produced in recent years (Cole et al., 1988). interspecific hybridization among the bisexual Two steps of hybridization were involved in species (e.g., Lowe and Wright, 1966; Neaves and the origin of the triploid unisexual species (fig. 2). Gerald, 1968, 1969; Neaves, 1969; Parker and Se­ For example, the unisexual C grahamH (GRA in lander, 1976, 1984; Dessauer and Cole, 1989). fig. 2, using the name applied by Wright, 1993) A preliminary analysis of the relationships of resulted from hybridization between the bisexual the bisexual Cnemidophorus from the Madrean C. tigris and C. septemvittatus (SEP in fig. 2; Archipelago was presented by Dessauer and Cole Wright and Lowe, 1967; Neaves, 1969; Parker and (1989), who used UPGMA clustering of genetic Selander, 1976; Dessauer and Cole, 1989). While distance data based on about three dozen gene the resulting unisexual clone continues to per­ loci. The same clustering of these species was ob­ petuate itself parthenogenetically, on at least one tained independently from mitochondrial DNA occasion in the past a female of C grahamH mated (Moritz et al., 1992b). Currently this hypothesis is with a male of C. sexlineatus (SEX in fig. 2). The being tested again by modern cladistic methods spenn added a third set of chromosomes and (e.g., Hillis et al., 1994), and it will be modified if genes to the diploid egg cloned by the female and appropriate. Meanwhile, we illustrate our hy­ produced a triploid hybrid. The triploid clone of pothesis here in the form of a cladogram (fig. 2), this hybrid is perpetuated parthenogenetically to­ upon which we have also superimposed our pre­ day as C tesselatus (TES in fig. 2). Thus, the ferred hypotheses for the hybrid origins of the triploid C tesselatus is comprised of three hap­ derived unisexual species (Dessauer and Cole, loid genomes ultimately inherited from three 1989). different bisexual species, through two separate The diploid unisexual species had one step of events of hybridization (Neaves, 1969; Parker and hybridization involved in their origin. For exam­ Selander, 1976; Dessauer and Cole, 1989). In addi­ ple, the unisexual C neomexicanus (NEO in fig. 2) tion, rare tetraploid hybrids are produced by resulted from hybridization between the bisexual occasional mating between triploid clonal females C. tigris (TIG in fig. 2) and C inornatus (INO in and males of bisexual species (e.g., Lowe et al., fig. 2). The diploid clone of this hybrid is perpetu- 1970; Cole, 1979).

269 Several of the triploid unisexual species origi­ it seems unlikely that in each case the two rare nated through an intermediary diploid clone events of unusual hybridization and an even rarer indicated as 2X in figure 2, which resulted from mutation conferring a new capacity for partheno­ hybridization between C inornatus and C burtl genesis on a hybrid female occurred This intermediary diploid clone has not been simultaneously. Consequently, it seems likely that identified with certainty in nature as yet, although there is a cause-and-effect relationship between future research may reveal it among the C opatae hybridization among well-differentiated popula­ complex (Dessauer and Cole, 1989; Wright, 1993) tions and the origin of parthenogenesis, perhaps or C. innotatus (as that name is applied by Wright, through dysfunction in meiosis (e.g., Densmore et 1993). Either hypothesis or both could be correct, al., 1989a; Moritz et al., 1989a, 1992b). It is a stag­ as various triploid clones and multiple hybridiza­ gering thought that the switch from tion events are involved (fig. 2). sperm-dependent to sperm-independent repro­ duction occurs in a single generation. Together with Wade C. Sherbrooke at the Southwestern Re­ INSTANTANEOUS SPECIATION search Station in the Chiricahua Mountains, we are now conducting experiments to address this The process by which ancestral populations of question. diploid bisexual species diverge over time and prod uce one or more new species generally re­ quires a minimum of hundreds, thousands, or CLONAL DIVERSITY tens of thousands of generations to complete through mutation and natural selection, particu­ Considering that the bisexual species of larly to the extent of developing reproductive Cnemidophorus show various differences in their isolation. In stark contrast, all of the evidence sug­ genetic material, it is clear that hybridization gests that parthenogenetic clones of hybrid origin among different combinations of bisexual species arise in a single generation (e.g., Cole, 1985). results in various genetically distinct clones (fig. In situations today where hybridization occurs 2). There are other sources of clonal diversity also. among bisexual populations distinguished by low Comparative studies of individual gene prod­ genetic differentiation, a hybrid zone of fertile hy­ ucts by protein electrophoresis have revealed two brids is formed (e.g., Dessauer and Cole, 1991). or more minor genetic variants in otherwise simi­ Panmixia is sufficiently extensive that.FI genera­ lar clones within unisexual species (e.g.; C tion hybrids are rare or absent. All lizards in the tesselatus, see Parker and Selander, 1976; C center of the hybrid zone are F2 and subsequent neonlexicanus, see Parker and Selander, 1984; and generation hybrids or backcross hybrids with C cryptus, see Cole and Dessauer, 1993). For the various combinations of alleles from the parental cases cited, the allelic variants observed in the populations. This kind of hybrid swarm is not the unisexual species appeared also in one or the situation from which parthenogenetic cloning other of the parental bisexual species. This sug­ emerges. gests that the slightly different unisexual clones Parthenogens are derived from hybridization arose from separate FI hybrids resulting from dif­ among bisexual populations distinguished by ferent combinations of eggs and sperm from the high genetic differentiation (but not so high as to parental species, even though in some cases the prevent development of viable hybrids; Dessauer same individual mother and father could have and Cole, 1989; Moritz et al., 1989a). The most de­ been involved. tailed analyses of the combinations of genomes The laboratory of Wesley M. Brown at the Uni­ and morphology in clonal lizards (Cnemidopho­ versity of Michigan has produced some elegant rus and other genera as well) indicate that the work on comparative analyses of mitochondrial clone in each instance most likely arose instanta­ DNA (mtDNA). The beauty of this is that mtDNA neously from a first-generation hybrid female. is inherited in the cytoplasm of the egg, contrib­ This suggests that the PI hybrid males that might uted by the mother and not the father. have been produced were sterile and became ex­ Consequently, when the parental species of a tinct after contributing no genes to subsequent clont~ differ in mtDNA, identification of the generations while one or more PI hybrid females mtDNA in the unisexual clone determines which perpetuated the PI state by parthenogenetic clon­ parental species was the maternal ancestor of the ing. Given the number of independent cases clont! (e.g., Brown and Wright, 1979). By such where hybridization has led to clones (e.g., fig. 2), analyses, Densmore et al. (1989b) and Moritz et al.

270 (1989b) determined that the diploid unisexual in­ (1) As yet, we know nothing about the sections of termediary clone referred to as 2X in figure 2 DNA that affect meiosis and cause partheno­ probably was created by hybridization at least genesis to occur in some hybrid females. With twice, by reciprocal crosses (lNO female x BUR a better understanding of the mechanics and male, and BUR female x INO male). processes involved, it might become possible By conservative estimate, adding up the to convert animals and plants of agricultural strong indications for separate hybrid origins of importance to parthenogenetic reproduction. diploid unisexual species (Densmore et al., 1989a, This would greatly improve efficiency of pro­ b; Dessauer and Cole, 1989; Moritz et al., 1989b, duction, as all normal individuals would bear 1992a; Cole and Dessauer, 1993), parthenogenetic progeny of known qualities. Experimental cloning probably had at least 10 independent ori­ breeding, genetic engineering in other re­ gins within Cnemidophol"US, but the actual spects, and related activities would still be number may be considerably higher. The majority important for improving stocks, but as desir­ of these occurred within or near the Madrean Ar­ able stocks were developed they could be chipelago, where there may have been more cloned. This might seem far-fetched if we separate origins of parthenogenetic lizards than in were not actually seeing this happen in verte­ any other comparable-sized area on Earth (but see brates in nature. Moritz et al., 1989c, for data on unisexual lizards (2) As yet, we do not know what activates cloned in Australia). We suspect that the reason such di­ eggs to initiate embryonic development in the versity has arisen here hinges upon the diverse absence of sperm. All we do know about this native bisexual species, diverse habitats that have process is that the mature ovum, after meio­ shifted throughout the Pleistocene and Recent sis, is genetically complete in the appropriate (e.g., Lowe et al., 1970), and the fact that mating in environment (Cuellar, 1971), so there seems Cnemidophorus does not involve the more elabo­ to be no need to await fertilization. In fact, for rate courtship-related behaviors seen in other haploid, un-cloned ova of bisexual species, lizards. Thus, the local frequency of hybridization do we know enough about the normal proc­ is greater in Cnemidophorus than in other lizards, esses involved in their brief period of waiting and; as discussed above, there may be a cause­ for fertilization before being shed through the and-effect relationship between hybridization and system? the origin of parthenogenetic cloning. (3) In general, we have a great deal to learn about Finally, genetic mutations can occur in lizards the effects of exposing wildlife and humans of a clone, just as they can in bisexual species. If a to pathogens, pollutants, radiation, and non-lethal mutation occurs within a clonal lizard, newly manufactured chemicals. In addition, both the original gene (still present in other indi­ appropriate animals can be used for research viduals) and the derived mutant will be on the general phenomena of nutrition and perpetuated by parthenogenetic cloning (e.g., aging, as well as captive propagation of en­ Parker and Selander, 1976). Examples of such dangered species (e.g., Porter et al., in press). karyotypic clones were discussed in detail by Cole Unisexual lizards are especially suited to such (1979) and of an allelic clone at the transferrin lo­ research because all individuals are identical cus by Dessauer in Cole et al. (1988). In the few within a clone and the affects of genetic vari­ studies of geographic variation of clones within ation are reasonably controlled (e.g., Cole and unisexual Cnemidophorus (Parker and Selander, Townsend, 1990). 1976, 1984; Dessauer and Cole, 1989), different (4) While a good start has been made (e.g., Schall, clones distinguished by allelic variation have been 1978; Price, 1992; various chapters in Wright found. In many cases, the source of this variation and Vitt, 1993; Walker et al., 1994), a great (separate hybrid eggs or gene mutations in deal remains to be learned about the biology parthenogenetic lineages?) remains unknown. of Cnemidophorus, including the popula­ tions in and around the Sky Islands.

CURRENT AND FUTURE RESEARCH MANAGEMENT CONSIDERATIONS There are several areas of research and experi­ mentation for which unisexual lizards and their Unisexual lizards and their bisexual relatives bisexual relatives are most suitable, including the are important biological resources with consider­ following: able potential for future, productive research, and

271 as such they should be conserved. In most cases, Darevsky, I. S. 1958. Natural parthenogenesis in certain active conservation activities are not necessary be­ subspecies of rocky lizard, Lacerta saxicola Eversmann. cause most species of these lizards are not Transl. (English) of Doklady, Biol. Scis. Sect. 122:877-879 currently threatened in nature. However, these (pp. 730-732 in Russian). lizards depend upon the continued existence of --. 1992. Evolution and ecology of parthenogenesis in reptiles. Pages 21-39 in K. Adler, ed. Herpetology: Cur­ their woodland, grassland, desert-grassland, and rent research on the biology of amphibians and reptiles. desert environments (specific habitats and distri­ SSAR Contrib. Herpetol., no. 9. bution depending on the species), and some Dawley,R.M.,andJ.P. Bogart. 1989. Evolution and ecology populations are quite locally restricted in geo­ of unisexual vertebrates. Bull. 466, New York State graphic distribution. Mus., Albany. Consequently, our main recommendation is to Densmore, L. D., III,J. W. Wright, and W. M. Brown. 1989a. keep avenues of communication open, as in the Mitochondrial-DNA analyses and the origin and rela­ spirit of this informative conference. Directors of tive age of parthenogenetic lizards (genus research stations and herpetologists should be in­ Cllemidophorus).II. C. neomexicanus and the C. tesse­ volved as plans are developed to change land uses latuscomplex.Evolution43:943-957. in relevant areas that could severely impact the --, C. C. Moritz, J. W. Wright, and W. M. Brown. 1989b. lizards and/or scientists' long-term research pro­ Mitochondrial-DNA analyses and the origin and rela­ grams. tive age of parthenogenetic lizards (genus Q2emidophorus). IV. Nine sexlineatus-group unisexuals. Evolu tion 43:969-983. Dessauer, H. C.; and C. J. Cole. 1984. Influence of gene LITERATURE CITED dosage on electrophoretic phenotypes of proteins from lizards of the genus Cnemidophorus. Compo Biochem. 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