teiidae_cnemidophorus phylogeny

7/22/2019 Teiidae_Cnemidophorus Phylogeny

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Copyright American Museum of Natural History 2002 ISSN 0003-0082

P U B L I S H E D B Y T H E A M E R I C A N M U S E U M O F N A T U R A L H I S T O R Y

CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024Number 3365, 61 pp., 7 figures, 3 tables May 17, 2002

Phylogenetic Relationships of Whiptail Lizards of

the Genus Cnemidophorus (Squamata: Teiidae): ATest of Monophyly, Reevaluation of Karyotypic

Evolution, and Review of Hybrid Origins

TOD W. REEDER,1 CHARLES J. COLE,2 AND HERBERT C. DESSAUER3

CONTENTS

Abstract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

CnemidophorusBackground and Classification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3Higher-Level Relationships and Cnemidophorus Monophyly . . . . . . . . . . . . . . . . . . . . . . . 4Objectives of the Present Study . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

Materials and Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7Choice of Taxa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7Molecular Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7DNA Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

Allozyme Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8Morphological Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8Phylogenetic Analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

1 Research Associate, Division of Vertebrate Zoology (Herpetology), American Museum of Natural History; As-sistant Professor, Department of Biology, San Diego State University, San Diego, CA 921824614; e-mail: [email protected].

2 Curator, Division of Vertebrate Zoology (Herpetology), American Museum of Natural History; e-mail: [email protected].

3 Research Associate, Division of Vertebrate Zoology (Herpetology), American Museum of Natural History; Pro-fessor Emeritus, Department of Biochemistry and Molecular Biology, Louisiana State University Medical Center,New Orleans, LA 70119-2799.


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2 NO. 3365AMERICAN MUSEUM NOVITATES

Uniformly Weighted Analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10Successive Approximations Analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11Effects of Initial Starting Tree in Successive Approximations . . . . . . . . . . . . . . . . . . . . . 13Phylogenetic Placement of Cnemidophorus murinus and Cnemidophorus ocellifer . . . 13

Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14Cnemidophorus Phylogeny . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14Cnemidophorus Paraphyly . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14Cnemidophorus lemniscatus Group . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14North American Cnemidophorus Clade . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18Ameiva Phylogeny . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20Evolution of Tongue Characters Traditionally Used in Cnemidophorine Systematics 20Taxonomic Implications and Nomenclatural Recommendations . . . . . . . . . . . . . . . . . . . . 21AspidoscelisFitzinger, 1843 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 22Maternal Ancestor of Kentropyx borckiana . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 24Unisexual Species: An Overview . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25Teioid Unisexual Species . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25

Knowing Ancestors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28Extent and Origin of Parthenogenetic Cloning in Vertebrates . . . . . . . . . . . . . . . . . . . . . . 29Successive Approximations and Initial Starting Trees . . . . . . . . . . . . . . . . . . . . . . . . . . . . 29Karyotype Evolution Revisited . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30

Summary and Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 34Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 36Appendix 1: Specimens Examined . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 41Appendix 2: Mitochondrial DNA Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 45Appendix 3: Allozyme Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60Appendix 4: Morphological Data . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 61


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2002 3REEDER ET AL.: PHYLOGENETIC RELATIONSHIPS OF CNEMIDOPHORUS

ABSTRACT

Phylogenetic relationships of the whiptail lizards of the genus Cnemidophorus are inferredbased on a combined analysis of mitochondrial DNA, morphology, and allozymes. Within theTeiini, Teius and Dicrodon are the most basal lineages, and these two taxa form a graded

series leading to a cnemidophorine clade containing Ameiva, Cnemidophorus, and Kentropyx.Cnemidophorus monophyly is not supported, with members of the neotropical C. lemnis-catus species group (except C. longicaudus) being more closely related to species in otherneotropical cnemidophorine taxa (Ameiva and Kentropyx). Ameiva is also paraphyletic.

The Cnemidophorus lemniscatus species group is also paraphyletic, with a C.murinus C. lemniscatus complex clade being more closely related to Kentropyx than to C.lacertoides, C. longicaudus, and/or C. ocellifer. Although the C. lemniscatus speciesgroup is paraphyletic, the three remaining bisexual Cnemidophorus species groups (deppii,sexlineatus, and tigris species groups) are each monophyletic. Together, these three groupsform a clade ( North American Cnemidophorus clade), with the deppii and tigris speciesgroups being sister taxa. Within the Cnemidophorus deppii species group, the Baja Cali-fornia C. hyperythrus is the sister species to a more exclusive mainland Mexico cladecontaining C. deppii and C. guttatus. Except for a C. inornatus C. sexlineatus

clade and a monophyletic C. gularis complex, the inferred inter- and intraspecific relation-ships within the sexlineatus species group are weakly supported. In none of the inferred phy-logenies are the C. costatus populations (C. c. costatus and C. c. griseocephalus)represented as each others closest relatives.

Because ofCnemidophorus paraphyly, nomenclatural changes are recommended. Aspidos-celisFitzinger, 1843, is resurrected for the North American Cnemidophorus clade containingthedeppii,sexlineatus, and tigris species groups (and the unisexual taxa associated with them).Lizards of the genusAspidoscelisdiffer from all other cnemidophorine lizards by the combinedattributes of absence of basal tongue sheath, posterior portion of tongue clearly forked, smoothventral scutes, eight rows of ventral scutes at midbody, absence of anal spurs in males, me-soptychial scales abruptly enlarged over scales of gular fold (more anterior mesoptychialsbecoming smaller), three parietal scales, and three or four supraocular scales on each side.

Previous studies using morphology and allozymes have determined that the unisexual Ken-tropyx borckiana originated from a historical hybridization event between the bisexual speciesK. calcarata and K. striata. In this study mitochondrial DNA confirms K. striata as the ma-ternal ancestor ofK. borckiana.

A review of our current knowledge of teioid unisexuals and their hybrid origins is provided.Also, a reevaluation of teiine chromosomal evolution is presented from a phylogenetic per-spective. These reviews elucidate the paradox that the capability of instantly producing par-thenogenetic clones through one generation of hybridization has existed for approximately 200million years, yet the extant unisexual taxa are of very recent origins. Consequently, theselineages must be ephemeral compared to those of bisexual taxa.

INTRODUCTION

CNEMIDOPHORUSBACKGROUND ANDCLASSIFICATION

Teiid whiptail lizards of the genus Cnem-idophorus range widely in the New World,extending from the northern United Statessouthward to Argentina, and occupy manydiverse ecological communities. However,while exhibiting this extensive distribution,their greatest diversity occurs in NorthAmerica, where they are a conspicuous com-

ponent of the herpetofauna of the arid andsemiarid regions of the southwestern U.S.and Mexico. By conservative count, there are

approximately 50 species known (for recentsummaries see Maslin and Secoy, 1986;Wright, 1993), with new species continuingto be found (e.g., Markezich et al., 1997; Ro-cha et al., 1997, 2000).

Because of their abundance and conspic-uous nature, whiptails are an ecologically im-portant squamate lizard clade, which is re-flected by the great number of ecological andlife history studies conducted on this group(reviewed in Wright and Vitt, 1993). Cnem-idophorushas been (and continues to be) one

of the most extensively studied genera of liz-ards, third only to Sceloporus and Anolis(Dunham et al., 1988). Besides their abun-


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TABLE 1

Cnemidophorus Species Groupsa

dance and geographic proximity to NorthAmerican biologists, one of the reasonswhiptails have been so intensively studied isthe occurrence of parthenogenetic all-femalespecies (of interspecific hybrid origin; seebelow) within this diverse clade. Approxi-mately one-third of the described species areunisexual, with the majority of these all-fe-male species occurring in the southwesternU.S. and northern Mexico (Wright, 1993).Diploid and triploid unisexual species have

evolved many times in Cnemidophorus, ineach instance the switch from sperm-depen-dent to sperm-independent reproduction oc-curring in one generation in an F1 interspe-cific hybrid (for reviews, see Darevsky et al.,1985; Dessauer and Cole, 1989; Moritz et al.,1989a, 1992a; Darevsky, 1992; Cole andDessauer, 1995), and dynamic hybridizationpresently occurs in nature (e.g., Walker et al.,1989; Dessauer et al., 2000; Taylor et al.,2001). Consequently, whiptail lizards areused broadly in research, particularly in re-

productive biology, population genetics,physiological ecology, and evolutionary bi-ology, often with emphasis on the instanta-neous, multiple and independent origins ofparthenogenetic cloning.

The species of Cnemidophorus are cur-rently allocated to six species groups (table1). Based on external morphology and kar-yology, these groups were erected by Loweet al. (1970), who modified Burts (1931) ar-rangement. All except the lemniscatus group

are confined to North and Central America.The lemniscatus group is largely a SouthAmerican radiation, with only a single spe-

cies (C. lemniscatus) extending into CentralAmerica. Two of the northern Cnemidopho-rus species groups (cozumelaandtesselatus)are composed entirely of parthenogeneticspecies. The origins of the unisexual speciesin both of these groups involve hybridizationbetween bisexual species from different spe-cies groups (i.e., sexlineatus group deppiigroup cozumela group; sexlineatus group tigris group tesselatusgroup). The lem-niscatusand sexlineatus groups each possess

bisexual and unisexual species. However, un-like the aforementioned completely unisex-ual groups, the unisexuals in the lemniscatusandsexlineatusgroups are derived exclusive-ly from hybridizations between species with-in their respective groups (intragroup hybrid-izations).

HIGHER-LEVEL RELATIONSHIPS ANDCNEMIDOPHORUSMONOPHYLY

WhileCnemidophorushas been extensive-

ly studied and much is known about its bi-ology, ecology, and natural history, the spe-cific phylogenetic placement of Cnemido-phorus within the Teiidae, as well as thehigher-level relationships within Cnemido-phorus, has received little attention. Presch(1974) provided osteological evidence thatthe macroteiids consisted of two majorgroups: Teiini (including Ameiva, Cnemido-phorus,Dicrodon,Kentropyx, andTeius) andTupinambini (including Callopistes, Crocod-

ilurus, Dracaena, and Tupinambis). Withinthe Teiini, Ameiva, Cnemidophorus, andKentropyxshared the most similarities, lead-


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Fig. 1. Previous phylogenetic hypotheses ofhigher-level relationships within Cnemidophorus.A. Modified hypothesis of Burt (1931). B. Mod-ified hypothesis of Lowe et al. (1970).

ing Presch to hypothesize that these threetaxa were more closely related to each otherthan any were to Dicrodon or Teius. How-ever, there were no derived osteological char-acters provided to resolve the relationshipsamongAmeiva,Cnemidophorus, andKentro-pyx. Informally we refer to these three verysimilar taxa as the cnemidophorines.

Using external morphology and intuition,Burt (1931) was the first to hypothesize high-er-level relationships within Cnemidophorus(fig. 1A). Because members of the SouthAmerican lemniscatus group shared somecharacteristics with other South American te-iids (e.g., Ameiva), Burt (1931) postulatedthat the lemniscatus group was the most

primitive lineage within Cnemidophorus.The ancestor of the North American groupswas hypothesized to have been derived fromthe lemniscatus group, with this lineage giv-ing rise to the deppii (excluding C. hypery-thrus) and sexlineatus groups. Burt (1931)also proposed that his tesselatus group (in-cluding the as-yet-to-be-described tigrisgroup) and hyperythrus groups were derivedfrom the sexlineatus group.

Based on karyology, external morphology,

and knowledge of the existence of unisexualspecies, Lowe et al. (1970) modified thehigher-level classification and hypothesizedrelationships within Cnemidophorus. Theevolutionary scenario (fig. 1B) proposed byLowe et al. (1970) was largely influenced bytheir assumption that the chromosomes ofvertebrates evolve primarily by means ofRobertsonian centric fusion, thus resulting inthe reduction of diploid chromosome num-ber. Members of the deppiigroup possess thehighest diploid number (2n 52) within

Cnemidophorus. Given this, Lowe et al.(1970) suggested that the deppii group (in-cluding the cozumela group) represented themost primitive lineage within Cnemido-phorus, possessing a karyotype essentiallyidentical to that of the hypothesized ancestorof Cnemidophorus. Such a conclusion dif-fered from Burt (1931), who suggested thatthe lemniscatus group was ancestral to theremaining Cnemidophorus species groups.Lowe et al. (1970) postulated that the lem-

niscatus group evolved from a deppii-likeancestor, requiring only a single centric fu-sion to derive the lemniscatus group karyo-

type (2n 50) from the deppii group/ances-tral karyotype. The sexlineatus and tigrisgroups were proposed to be sister taxa, with

their common ancestor being derived from adeppii-like ancestor (via three centric fu-sions).


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Based on mitochondrial DNA restrictionsite data, Moritz et al. (1992a) provided thefirst explicit phylogenetic analysis of higher-level relationships within Cnemidophorus. Inthat study, C. lemniscatus was used to rootthe resulting phylogeny. This outgroupchoice was based on Burt (1931) and the factthat the greatest observed genetic distanceswere between C. lemniscatus and the re-maining Cnemidophorus species (see alsoDessauer and Cole, 1989). Moritz et al.(1992a) provided strong support for a sistergroup relationship between the sexlineatusand tigris groups, corroborating the hypoth-esis of Lowe et al. (1970). These mitochon-drial data also supported the placement of the

deppii group as the sister taxon to the sexli-neatus group tigris group clade. Mono-phyly of the deppii and sexlineatus groupswas also supported by Moritz et al. (1992a).However, because of the limited sampling,these conclusions could only be consideredpreliminary. Even so, the relatively large es-timated sequence divergences between C.lemniscatus and the remaining Cnemidopho-russpecies are suggestive of a relatively bas-al position for the lemniscatus group. How-

ever, this study cannot be viewed as a rig-orous test of the basal relationships withinCnemidophorus (e.g., hypotheses of Burt,1931 vs. Lowe et al., 1970). Such a testwould require the inclusion of other closelyrelated teiine taxa (e.g., Ameiva, Kentropyx)as outgroups.

While there have been previous attemptsto organize Cnemidophorus into speciesgroups and hypothesize on the interrelation-ships of these groups, there has never been arigorous attempt to demonstrate the mono-

phyly of this group of lizards. All previousstudies generally assumed that Cnemidopho-rus was monophyletic, based on the pheneticsimilarity between Cnemidophorusand otherSouth American teiid lizards (i.e., Ameiva,Dicrodon, Kentropyx, and Teius). Historical-ly, Cnemidophorus has been defined by theabsence of presumably derived characterstates exhibited by these other South Amer-ican genera (i.e., laterally compressed teethin Dicrodon and Teius, keeled ventral scales

in Kentropyx, basal tongue sheath in Amei-va). The long recognition that Cnemidopho-rus lacked apomorphies, and earlier hypoth-

eses suggesting that various lineages ofCnemidophorus were independently derivedfrom ancestral South American stocks(e.g., Burt, 1931; Lowe et al., 1970) suggestthat Cnemidophorus monophyly is in ques-tion and should be rigorously tested. Al-though taxon sampling was limited (ingrouptaxa three Cnemidophorus species groups,Ameiva, and Kentropyx), a phylogeneticstudy using allozymes by Dessauer and Cole(1989) provided support for Cnemidophorusparaphyly, with the lemniscatus group hy-pothesized to be more closely related to Ken-tropyx than to a clade containing the sexli-neatus and tigris groups.

OBJECTIVES OF THE PRESENT STUDY

As the use ofCnemidophorus increases inresearch and the literature mushrooms, it be-comes increasingly important to establish thevalidity of this taxon as a monophyleticgroup, if indeed it is. Dessauer and Cole(1989) provided preliminary evidence sug-gestingCnemidophorus paraphyly. However,their taxon sampling was limited and/or in-complete (e.g., absence of the deppii group

and other critical cnemidophorine lineages).Thus, it is timely to more rigorously examinethe phylogenetic relationships betweenCnemidophorusand other teiine taxa (Amei-va, Dicrodon, Kentropyx, and Teius), partic-ularly now that the necessary samples areavailable. The inferred phylogenetic relation-ships presented below are based on diversetypes of data. The bulk of these data are de-rived from mitochondrial ribosomal RNA(rRNA) genes, but these data are augmentedwith previously published allozyme data

(Dessauer and Cole, 1989; Cole and Des-sauer, 1993; Cole et al., 1995; Markezich etal., 1997) and morphological characters tra-ditionally used in Cnemidophorus systemat-ics.

The following questions are addressed inthis paper: (1) Is Cnemidophorus a mono-phyletic group? (2) If not, what nomencla-tural changes are needed and appropriate atthis time? (3) What are the relationships be-tween Cnemidophorus and the other teiinine

genera? (4) Are the traditionally recognizedbisexual species groups within Cnemidopho-rus monophyletic, and what is their relation-


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ship to each other? Finally, (5) Do the newlyinferred higher-level relationships require re-examination of past hypotheses of chromo-somal evolution within Cnemidophorus? Inaddition we comment briefly on the reticulatephylogeny of unisexual clones of hybrid or-igin and determination of the maternal an-cestor of Kentropyx borckiana, a unisexualspecies of hybrid origin.

MATERIALS AND METHODS

CHOICE OF TAXA

Twenty-seven recognized Cnemidophorustaxa were included in the present study, rep-resenting all currently recognized bisexualspecies groups (deppii, lemniscatus, sexli-neatus, and tigris species groups; Wright,1993). This sample allows a preliminary testof the monophyly of these groups. Also, sev-eral additional non-Cnemidophorus teiinespecies were included in order to test Cnem-idophorusmonophyly. In all, 41 ingroup taxa( Ameiva, Cnemidophorus, Dicrodon, Ken-tropyx, and Teius) were included (appendix1).

The following five outgroup taxa (succes-

sively more distant) were included also: Tup-inambis (Teiidae), Pholidobolus (Gymnoph-thalmidae), Acanthodactylus and Lacerta(Lacertidae), and Eumeces (Scincidae). Therelationships of these outgroups to the in-group are fairly well understood (Estes et al.,1988; Lee, 1998). However, to minimize out-group assumptions, a global parsimony root-ing approach was taken (Maddison et al.,1984), with Eumeces (assumed to be themost distantly related outgroup) being usedto root the overall resulting tree(s).

MOLECULAR DATA

DNA DATA: Total genomic DNA was iso-lated from small amounts of liver or eryth-rocytes (100 mg) following the phenol-chloroform extraction protocol of Hillis et al.(1996). Two portions of the mitochondrialgenome were amplified using the polymerasechain reaction (PCR) in Perkin-Elmer 2400or Ericomp TwinBlock thermocyclers. One

PCR product was a

380 bp fragment fromthe 12S ribosomal RNA (rRNA) gene. Theother PCR product was a 500 bp fragment

from the 16S rRNA gene. The primers andPCR parameters used to amplify these frag-ments are described in Reeder (1995). Puri-fication of amplified DNA and automatedDNA sequencing were performed followingmethods described in Wiens and Reeder(1997). The DNA sequences for Acantho-dactylus cantorisand Lacerta agiliswere ob-tained from GenBank (accession numbersAF080298, AF080300, AF080344, andAF080346).

The mitochondrial rDNA sequences (ap-pendix 2) were aligned under varying gapcosts (opening gap cost of 6, 9, and 12) usingthe multiple sequence alignment programClustal W (Thompson et al., 1994). Sequence

alignment procedures and parameters are de-scribed in Wiens and Reeder (1997). It hasbeen demonstrated that rRNA secondarystructure models can be useful in the align-ment of these gene sequences (Kjer, 1995;Titus and Frost, 1996). Following the pro-cedure outlined in Wiens and Reeder (1997),rRNA secondary structure information wasused to assist in DNA sequence alignment.Regions of sequence were considered align-ment-ambiguous if nucleotide positional ho-

mologies differed among the different gapcost alignments (Gatesy et al., 1993). Am-biguously aligned regions were excludedfrom phylogenetic analysis. In all, 1072 nu-cleotide positions were aligned (491 12S and581 16S; appendix 2), with 61 positions (2512S and 36 16S) excluded from phylogeneticanalysis. Gaps ( insertion/deletion events)were coded as a fifth character state, as de-scribed in Wiens and Reeder (1997). AllDNA sequences are deposited in GenBank(accession numbers AY046420AY046503,

AF080344, AF080346, AF080298, andAF080300). Upon request, the PAUP* ma-trix is available from one of us (T.W.R.).

We followed Dessauer et al. (1996) in us-ing allele-specific oligonucleotide probes toscreen multiple individuals of Kentropyxborckianato determine the maternal ancestorof this unisexual species.

ALLOZYME DATA: Data on 31 phylogenet-ically informative protein loci ( characters)were scored for 19 taxa of teiid lizards. The

entire allozyme database was produced inone laboratory (H.C.D.s), so there is com-plete internal consistency across the data set.


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Data are the alleles detected at individualgene loci. For phylogenetic analysis, each lo-cus was interpreted as the character and thealleles present in a taxon as character states

(Buth, 1984). All allozyme characters wereanalyzed unordered.The gene loci and codes for phylogenetic

analysis of the allozymes are presented in ap-pendix 3. The data were published previous-ly in the following reports: Dessauer andCole, 1989 (Ameiva, Cnemidophorus, Ken-tropyx, and Tupinambis); Cole and Dessauer,1993 (South American Cnemidophorus);Cole et al., 1995 (Kentropyx); and Markezichet al., 1997 (South American Cnemidopho-

rus). However, this is the first report in whichall of these data have been cross-correlated,so the individual alleles as specified in thisreport (appendix 3) will not necessarily bearthe same letter designation as in those orig-inal papers, some of which were alphabetizedonly on the basis of the alleles being com-pared within the individual report.

Methods of collecting, preparing, and stor-ing tissue samples, and methods of conduct-ing protein electrophoresis, identifying loci,

and determining allele products present inthe various species are detailed in the paperscited above and relevant references therein(also see Dessauer et al., 2000). The data areof discrete characters that could be scored

unambiguously. Although most loci for each

taxon show no intraspecific variation or poly-

morphism, some do. In cases where two or

more alleles were recorded for a taxon, each

allele was recorded as present at that locus

for that taxon. We did not attempt to use fre-

quency data (we used only presence or ab-sence of allele character states) because de-gree of variability varies widely among loci,

it can vary geographically, and because sam-

ple sizes vary widely among the taxa. For

example, we examined only one specimen of

Tupinambis teguixin and more than 35 of

Cnemidophorus inornatus. The problems as-

sociated with geographic variation and sam-

ple size are illustrated by Dessauer et al.

(2000), who examined more than 650 indi-

viduals of Cnemidophorus tigris. We did nottry to integrate all of their data on rare allelesinto this report.

MORPHOLOGICAL DATA

Data on the 10 morphological characterswere recorded for 42 taxa of teioid lizards(includingPholidobolusand two populations

of Kentropyx altamazonica). These taxa in-clude all of the teiids for which DNA se-quence data were analyzed. Because of prob-lems with homology assessment, morpholog-ical data were not coded for any of the non-teioid taxa. Data were recorded frommuseum specimens, which are specified inappendix 1 (Specimens Examined).

These characters have historically beenuseful in recognizing generic and subgenericspecies groups within the Teiidae, as sug-

gested by previous authors (Burt, 1931;Lowe et al., 1970; Peters and Donoso-Barros,1970; Hoogmoed, 1973). While not a largeset of characters, we felt it was better to in-clude these traditional characters than to ex-clude them. It has been demonstrated thateven a small number of morphological char-acters (within the context of a large com-bined data set largely consisting of molecularcharacters) can have an effect on a phylo-genetic analysis (e.g., Titus and Larson,1996). The character descriptions, coding,

and matrix are presented in appendix 4. Allwere discrete characters that could be scoredunambiguously and for which there was littleintraspecific variation.

PHYLOGENETICANALYSIS

The mtDNA, allozymic, and morphologi-cal data were combined into a single datamatrix for phylogenetic analysis. Taxa miss-ing a particular subset of the total data (e.g.,allozymes) were coded as missing (?) those

data. Phylogenetic analyses were performedwith PAUP* 4.0b2 (Swofford, 1999). Theheuristic tree search routine was used (withTBR branch swapping and 100 random taxonadditions). When multiple shortest trees werediscovered, the trees were summarized witha strict consensus tree (Sokal and Rohlf,1981), thus depicting only those relationshipsshared among all shortest trees. A characterstate change was considered to unambigu-ously support a clade if it was placed along

a branch by both ACCTRAN (Farris, 1970)and DELTRAN (Swofford and Maddison,1987) optimizations.


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Initial phylogenetic analyses were per-formed with uniformly weighted characters(i.e., all character state transformations had aweight of 1, irrespective of data type). How-ever, it is fairly well understood that verte-brate mtDNA exhibits substitution biases(e.g., transitions occurring more rapidly thantransversions), and different sites or regions(e.g., third codon positions, stem vs. loop re-gions) evolve at different rates. Thus, differ-ential weighting of nucleotide substitutionsand/or sites may be warranted. Seemingly re-alistic and justifiable weighting schemes canbe devised for the DNA data at hand (e.g.,Arevalo et al., 1994; Cunningham, 1997;Wiens et al., 1999). However, philosophical

and methodological difficulties arise withinthe context of a combined phylogenetic anal-ysis (e.g., what weight is applied to morpho-logical characters vs. the differentiallyweighted nucleotide substitutions?). Also,different genes within a combined analysismay have different substitution properties(e.g., are the best character state transfor-mations of gene A equivalent to those ofgene B?). An objective way to differentiallyweight characters within the context of a

combined analysis is to use the a posteriorimethod of successive approximations (Farris,1969; Carpenter, 1988). Such a weightingstrategy differentially weights all the char-acters based on their relative degrees of ho-moplasy. Those characters most consistentwith the initial starting tree are given thegreatest weights, regardless of data partition(i.e., DNA, allozymes, morphology). In ourstudy, the initial tree(s) for successiveweighting was that inferred from a uniformlyweighted combined data analysis. Reweight-

ing characters was performed in PAUP*, us-ing the maximum rescaled consistency index(rci; Farris, 1989) (base weight 100;weights truncated instead of being rounded[as in Hennig86]).

While originally envisioning means of ob-jectively determi ning character wei ghts,Kluge (1997a, 1997b) has recently arguedthat all character weighting (a priori and aposteriori) should be rejected. Kluge statesthat all forms of differential character

weighting invoke additional backgroundknowledge about biological processes thatare untestable. While such an affirmation re-

garding the use of biological processes ormodels of evolution are debated (e.g., Swof-ford et al., 1996), one should always be cau-tious of the assumptions that are being madein any phylogenetic analysis. In our study weuse successive approximations to test thesensitivity of the most parsimonious un-weighted trees(s) to differential characterweighting based on inferred levels of ho-moplasy (Farris, 1969; Kluge, 1997a). Cladestability during successive approximations( clades congruent with tree(s) based onuniform weighting) instills us with additionalconfidence for those relationships inferred inthe uniformly weighted analysis (Carpenteret al., 1993).

A common criticism or concern of succes-sive approximations is that the final inferredtree may be largely dependent on the initialstarting tree from which weights were deter-mined (Swofford et al., 1996). To test howrobust inferred clades were to initial startingtrees, we generated 20 random trees inMacClade v3.07 (Maddison and Maddison,1992) and performed successive approxima-tions on each of the random trees. Congru-ence among the final trees from the 20 com-

pleted successive approximation analyseswas summarized with a 50% majority-ruleconsensus tree.

The number of taxa scored for the mtDNA(n 44) and morphological (n 43) datafar exceeded the number available for the al-lozyme (n 19) data. Thus, some taxa areincomplete for a subset of the total combineddata. However, these incomplete taxa (miss-ing 8% of informative characters) were stillincluded in the phylogenetic analyses (seeWiens and Reeder, 1995; Reeder and Wiens,

1996). Also, two taxa (Cnemidophorus mu-rinus and C. ocellifer) were coded for onlythe 10 morphological characters (represent-ing 3% of the total informative characters),since we lacked tissue samples for molecularanalysis. While these highly incomplete taxa(missing 97% of informative characters)were included in certain phylogenetic anal-yses, their impact on tree stability was as-sessed by bootstrapping (see below) the com-bined data with and without these two spe-

cies. The phylogenetic placement of C. mu-rinus is of special significance because it isthe type species ofCnemidophorus.


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Support for individual clades was assessedby nonparametric bootstrapping (Felsenstein,1985). Bootstrap analyses were based on 500heuristic tree searches (with TBR branchswapping). Because of computational con-straints, only three random taxon additionsper pseudoreplicate were performed in eachof the heuristic tree searches. Bootstrappingwas performed in both the uniformly weight-ed and successive approximation analyses.Sullivan et al. (1997) have noted that weight-ed parsimony analyses often significantly in-crease bootstrap values (relative to their val-ues in uniformly weighted analyses of thesame data). However, because of the inherentproperties of parsimony, the elevated boot-

strap values in weighted parsimony analysesprobably represent overestimates of theamount of support for the inferred clades(Yang et al., 1995; Sullivan et al., 1997).Therefore, we cautiously interpret the boot-strap results of the successively weighteddata, and base most of our conclusions ofrelative support from the unweighted boot-strap analysis. For the uniformly weighteddata, clades with bootstrap values of 70%were considered strongly supported (follow-

ing Hillis and Bull, 1993).

RESULTS

UNIFORMLY WEIGHTED ANALYSIS

Phylogenetic analysis of the 317 uniform-ly weighted phylogenetically informativecharacters (235 informative charactersamong teiine taxa) resulted in four shortesttrees (L 1539; CI 0.39; RI 0.61). Thestrict consensus of these four trees is shownin figure 2A. The numbers of unambiguous

synapomorphies supporting the unambigu-ously resolved branches of the strict consen-sus tree are given in table 2. All inferred tei-ine clades were supported by unambiguouslyplaced synapomorphies. However, the vastmajority of the clades were supported onlyby mtDNA character state transformations.In all, only four of the 36 teiine clades wereunambiguously supported by mtDNA, mor-phological, and allozymic synapomorphies(table 2), possibly because allozyme data

were coded for only 19 taxa.Monophyly of the Teiidae (excludingGymnophthalmidae) is not supported by this

analysis. However, teiid paraphyly is onlyweakly supported, with the gymnophthalmid( microteiid) Pholidobolus being placedwith Tupinambis (bootstrap 57%). Teiini(Clade 1) monophyly is strongly supported(80%) by 11 synapomorphies, withTeiusandDicrodon representing the most basal line-ages. Within the teiine clade, 18 of the 34unambiguously resolved clades are stronglysupported (bootstraps 70%) by the com-bined data. Within the Teiini, the cnemido-phorine taxa are also supported as a clade(Clade 3). However, cnemidophorine mono-phyly is only weakly supported (70%).

While cnemidophorine monophyly is sup-ported, monophyly ofCnemidophorus is re-

jected. All of the South American Cnemi-dophorusspecies (exceptC. longicaudus) aremore closely related to species of other gen-era of Central and South American cnemi-dophorines (i.e.,Ameivaand Kentropyx) thanto the North American species ofCnemido-phorus. However, this neotropical clade(Clade 4) is only weakly supported by thesedata. Within Clade 4C. lacertoidesis weaklyplaced as the sister species of the remainingtaxa. Monophyly of the lemniscatuscomplex

(i.e., C. arenivagus, C. gramivagus, and C.lemniscatus; Clade 10) is strongly supported(100%), with this clade being placed as thesister taxon of a strongly supported Kentro-pyx (100%; Clade 13). In addition to 12mtDNA synapomorphies, the lemniscatuscomplex is also supported by one morpho-logical synapomorphy (basal tongue sheathabsent [character state 1.b]). Kentropyxmonophyly is supported by 19 synapomor-phies: 12 mtDNA, four morphological(keeled ventral scutes [3.b], 14 rows of ven-

tral scutes [4.c], two enlarged anal spurs perside in males [6.c], abruptly enlarged mesop-tychial scales [8.c]), and three allozymes.Within Kentropyx, it is equally parsimoniousto place K. calcarata as the sister taxon ofall remaining Kentropyx, or as the sister spe-cies to the K. altamazonica K. pelvicepsclade.

Analysis of these data also rejects themonophyly of Ameiva. Within Clade 4, A.undulata is more closely related to the lem-

niscatusgroup

Kentropyxclade than to thesmall clade containing A. ameiva, A. bifron-tata, andA. quadrilineata. Also, the West In-


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dian species (A. auberi and A. chrysolaema)are strongly supported as a clade (98%), butthey are distantly related to mainland Amei-va. The West Indian clade is weakly placed(55%) as the sister taxon to a large clade con-taining all of the North American Cnemido-phorus (Clade 20) and the South AmericanC. longicaudus.

The monophyly of a large North Americanclade of Cnemidophorus (Clade 20) isstrongly supported (84%) in this analysis by10 mtDNA synapomorphies. This clade con-tains the bisexual deppii, sexlineatus, and ti-gris groups, each of whose monophyly isstrongly supported (89%, 80%, and 100%,respectively). Within the North American

clade, the deppii group and tigris group arestrongly supported (85%) as sister taxa(Clade 21). While deppii group (Clade 22)monophyly is well supported, the inferred re-lationships within this group are weak, withthe Baja California C. hyperythrus beingplaced as the sister species of the C. deppii C. guttatusclade of mainland Mexico. Thephylogenetic relationships within the tigrisgroup (Clade 24) are well supported, exceptfor the interrelationships among the follow-

ing three taxa: C. tigris punctilinealis, C. t.aethiops, and the C. t. septentrionalis C.t. tigris clade.

The monophyly of the sexlineatus group(Clade 29) is strongly supported by eightsynapomorphies: six mtDNA, one morpho-logical (enlarged postantebranchial scales[7.c]), and one allozyme. Only two of theseven resolved clades within the sexlineatusgroup are strongly supported by this analysis.One of these is the clade containing C. gu-laris gularis, C. g. scalaris, and C. g. sep-

temvittatus(85%; Clade 31), which is weaklyplaced as the sister taxon to C. costatus cos-tatus. The other strongly supported clade isthe sister group relationship between C. in-ornatus andC. sexlineatus. The C. inornatus C. sexlineatus clade is supported by 18 or20 synapomorphies (depending on resolutionofC. burti taxa): 13 or 15 mtDNA, one mor-phological (slightly enlarged postantebrachi-al scales [7.b]), and four allozymes. The onlyambiguity within the sexlineatusgroup is the

phylogenetic affinity ofC. burti burti andC.b. stictogrammus (fig. 2A, B). Both of thesetaxa are weakly placed in a clade containing

C. costatus griseocephalus,C. inornatus, andC. sexlineatus. However, it is equally parsi-monious to place C. b. burti and C. b. stic-togrammus as sister taxa, or to place C. b.burtias the most basal taxon within its clade.And finally, the two C. costatus taxa includ-ed (C. c. costatus and C. c. griseocephalus)are not supported as each others closest rel-ative.

SUCCESSIVE APPROXIMATIONS ANALYSIS

Phylogenetic analysis of the 317 succes-sively weighted phylogenetically informativecharacters (235 informative charactersamong teiine taxa) resulted in a single short-

est tree (fig. 3; L 43,281) with a CI of0.61 and RI of 0.79. The numbers of unam-biguous synapomorphies supporting the un-ambiguously resolved branches of the strictconsensus tree are given in table 3. As in theuniformly weighted analysis, all clades aresupported by unambiguous synapomorphies,with most clades being unambiguously sup-ported only by mtDNA character state trans-formations.

Successive weighting (based on the four

fundamental phylogenies from the unweight-ed analysis; two iterations) of these data re-sulted in a phylogeny that is very similar tothe phylogenies inferred in the uniformlyweighted analysis, with Cnemidophorus andAmeiva both being paraphyletic. Besidesgreater resolution in the successive approxi-mations analysis, the only differences be-tween the unweighted and the successive ap-proximations analyses involve the followingrelationships: (1) Dicrodon and Teius haveswitched positions, withDicrodonnow being

the sister taxon to the remaining teiines; and(2) interrelationships within the sexlineatusgroup of North America. Within the sexli-neatus group, the C. inornatus C. sexli-neatus clade is now the sister taxon to theremaining sexlineatus group species. Whilethe C. inornatus C. sexlineatus clade stillappears to be strongly supported, the numberof unambiguously placed synapomorphiessupporting this group is about half of thatfrom the uniformly weighted analysis (11 vs.

20). Also, the single morphological synapo-morphy (i.e., slightly enlarged postantebra-chial scales [7.b]) in the uniformly weighted


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Fig. 2. Teiini phylogeny inferred from the uniformly weighted combined analysis of the mtDNA,morphological, and allozymic data. A. Strict consensus of four equally parsimonious shortest phyloge-nies (L 1542, CI 0.39, RI 0.61). The phylogenetic placements of Cnemidophorus ocelliferand

C. murinus (based on morphology only) are indicated by arrows. The numbers above the branchesdenote the different clades of the strict consensus tree. The numbers below the branches are bootstrapvalues. Branches without bootstrap values were supported in 50% of the pseudoreplicates. Number of


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synapomorphies supporting inferred clades is given in table 2. B. The two equally parsimonious ar-rangements of taxa within the sexlineatus group.

analysis no longer diagnoses theC. inornatus C. sexlineatus clade, but instead becomesa synapomorphy of the sexlineatus group asa whole. In the unweighted analysis, en-larged postantebrachial scales (7.c) was asexlineatus group synapomorphy, with a re-versal to slightly enlarged postantebrachialscales (7.b) diagnosing theC. inornatus C.sexlineatus clade. The two C. burti taxa arenow unambiguously supported as sister taxaby a single mtDNA synapomorphy. And fi-nally, while the specific placement ofC. cos-tatus griseocephalus has changed relative tothe unweighted analysis (figs. 2, 3), this tax-on andC. c. costatusare still not each othersclosest relatives.

Bootstrap analysis resulted in 25 teiineclades with bootstrap values 70% (com-pared to only 18 clades in the unweightedanalysis) (fig. 2 vs. fig. 3). The increase inbootstrap support in the successively weight-ed analysis is consistent with the results fromother recent empirical studies (see Phyloge-netic Analysis under Materials and Meth-ods). Ten inferred clades remain weakly sup-ported (bootstrap 70%) in the weightedanalysis. These clades may represent the

poorest supported relationships of the study.And finally, the level of support for the sex-lineatus group (bootstrap 65%) appears tohave decreased in the weighted analysis, rel-ative to its strong support (80%) in the un-weighted analysis.

EFFECTS OF INITIAL STARTING TREE INSUCCESSIVE APPROXIMATIONS

Twenty random trees were generated,which were 1432 steps longer than the orig-

inal four equally parsimonious unweightedtrees. Application of successive approxima-tions on these random trees indicated that theinitial starting tree did influence the final in-ferred tree. None of these analyses on ran-dom trees resulted in a phylogeny completelycongruent with our preferred successive ap-proximations phylogeny (fig. 3). However,when the results of the 20 successive ap-

proximation analyses are summarized with amajority-rule consensus tree (fig. 4), it isclear that most of the inferred relationshipsin figure 3 are being recovered through suc-cessive approximations, regardless of thestarting tree. Twenty-six clades were recov-ered in 90% of the random tree analyses,and these clades are supported in the pre-ferred successive approximations analysis.

PHYLOGENETICPLACEMENT OFCNEMIDOPHORUS MURINUS AND

CNEMIDOPHORUS OCELLIFER

Because of the lack of tissue, Cnemido-phorus murinus and C. ocellifer were codedfor only the 10 morphological characters.

However, while lacking 97% (307 of 317) ofthe phylogenetically informative characters,analysis of the complete data set containingC. murinus and C. ocellifer unambiguouslyplaces these two species within the teiinephylogeny (figs. 2A, 3). The inclusion ofthese two species did not alter the previouslyinferred interrelationships among the otherteiine species. Also, the placement of thesetwo species is identical in the uniformly andsuccessively weighted analyses. The mostparsimonious placement ofC. ocellifer is as

the sister species of the large clade (Clade 3;figs. 2A, 3) containing all the remainingcnemidophorines.Cnemidophorus murinusisnested further in the cnemidophorine clade,being placed as the sister species of the lem-niscatus complex (Clade 10; figs. 2A, 3).While C. murinus and C. ocellifer are un-ambiguously placed by the morphologicaldata, these specific placements are weaklysupported. In fact, the relative supportthroughout the phylogeny generally decreas-

es when these taxa are included in a boot-strap analysis. The decrease in tree supportis attributed to the largely incomplete natureof the data for C. murinus and C. ocellifer.

DISCUSSION

CNEMIDOPHORUS PHYLOGENY

CNEMIDOPHORUS PARAPHYLY: One of theprimary goals of this study was to rigorously


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TABLE 2

Number of Unambiguously PlacedSynapomorphies Supporting the Clades of theTeiine Phylogeny Inferred from the Uniformly

Weighted Phylogenetic Analysis

testCnemidophorusmonophyly and infer the

interrelationships among the bisexual speciesgroups. Equal weighting of the combinedmtDNA, allozymic, and morphological data

resulted in four equally parsimonious phy-logenies (strict consensus in fig. 2), and suc-cessive weighting resulted in a completelyresolved phylogenetic hypothesis (fig. 3) forteiine lizards. The higher-level teiine rela-tionships inferred in these two analyses areessentially identical, with these data not sup-porting Cnemidophorus monophyly. Such aconclusion should come as no surprise.While Cnemidophorus monophyly has longbeen assumed, no apomorphies have everbeen proposed, and its monophyly has neverbeen explicitly tested. In fact, Cnemidopho-rus (we use quotation marks in reference tothe broader paraphyletic group) has histori-cally been defined by the absence of presum-

ably derived character states exhibited by theother teiine teiids (Ameiva, Dicrodon, Ken-tropyx, and Teius). Our data support at leastfour distinct clades or lineages of Cnemi-dophorus: (1) North American Cnemido-phorus clade (deppii, sexlineatus, andtigrisspecies groups) C. longicaudus; (2)C.lacertoides; (3) C.lemniscatuscom-plex C.murinus; and (4) C.ocellifer.

CNEM IDO PHO RUS LEMNISCATUS GROUP:Except for Cnemidophorus longicaudus

and C. ocellifer(placement based on mor-phology only), all members of the traditionallemniscatusgroup are more closely related toother neotropical cnemidophorines (i.e.,Ameiva and Kentropyx) than they are to theNorth American Cnemidophorus. Such aconclusion is consistent with the hypothesisput forth by Burt (1931), who proposed thatthe lemniscatus group was derived from anAmeiva-like Cnemidophorus ancestor, al-though he visualized the lemniscatus groupsubsequently giving rise to the ancestor of

the North American Cnemidophorus.Specifically, Cnemidophorus lacerto-

ides and the C. lemniscatus complex(Clade 10) are placed within a more inclusiveclade (Clade 4; figs. 2A, 3) that containsKentropyxand mainland neotropicalAmeiva.However, even within this neotropical clade,the lemniscatus complex does not form aclade with C. lacertoides. The combineddata strongly support a clade containingthose lemniscatus group species (i.e., C.

arenivagus, C. gramivagus, C. lemnis-catus, C. murinus) that possess anal spurs,and this clade is placed as the sister taxon to


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Fig. 3. Teiini phylogeny inferred from the successively weighted combined analysis of the mtDNA,morphological, and allozymic data (L 43,489, CI 0.61, RI 0.79). The phylogenetic placementsof Cnemidophorus ocellifer and C. murinus (based on morphology only) are indicated by arrows. Thenumbers above the branches denote the different clades. The numbers below the branches are bootstrapvalues. Branches without bootstrap values were supported in 50% of the pseudoreplicates. Number ofsynapomorphies supporting inferred clades (and branch lengths) is given in table 3.


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TABLE 3

Number of Unambiguously Placed Synapomorphies Supporting the Clades of the Teiine Phylogeny

Inferred from the Successively Weighted Phylogenetic Analysis

Kentropyx. Traditionally C. lacertoideshas been included as a member of the lem-

niscatusgroup (Wright, 1993). However, ourdata do not support a close relationship be-tween these taxa. In fact, the generic assign-

ment of C. lacertoides has been contro-versial (Cole et al., 1979), as the species has

been alternatively placed in Ameiva (Vanzo-lini and Valencia, 1966). Note also that ouranalyses place C. lemniscatus splendidus


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Fig. 4. Majority-rule consensus tree depicting shared clades from the 20 random-tree successive

approximation analyses. Numbers along the branches denote the percentage a given clade was recoveredin the analyses.


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and C. arenivagus as sister taxa (figs. 2A,3), suggesting that the specific status of C.lemniscatus splendidus merits reevaluation(Markezich et al., 1997).

Two additional species that have tradition-ally been placed in the lemniscatusgroupare Cnemidophorus longicaudus andC.ocellifer(Wright, 1993). Our combinedanalysis places C. longicaudus as the sis-ter species of the North American Cnemi-dophorus clade. While we find this possiblerelationship perplexing considering thatC. longicaudus is found in south-centralSouth America, our current analysis suggeststhis inferred relationship is weakly support-ed. Cnemidophorus ocellifer was scored

only for the 10 morphological characters, butit is unambiguously placed as the sister spe-cies to all remaining cnemidophorines (Clade3; figs. 2A, 3). However, like the placementof C. longicaudus, this specific placementof C. ocellifer is very weakly supported.Therefore, we do not have great confidencein the placement of these two species, andtheir inferred relationships will likely changewith the addition of new data (Bell andReeder, unpubl. data).

NORTH AMERICAN CNE MIDO PH OR USCLADE: Our current study strongly supportsthe monophyly of a group of North Ameri-can Cnemidophorus, composed of thedeppii, sexlineatus, and tigris species groups(each of which is also strongly supported).Such a hypothesis is consistent with Burt(1931), although he had also postulated thatthe neotropical lemniscatus group gaverise to the ancestor of the North AmericanCnemidophorus. Within this clade thereappears to be relatively strong support for a

sister group relationship between the deppiiandtigrisspecies groups. Such a relationshiphas not been previously proposed. Lowe etal. (1970) hypothesized that the sexlineatusand tigris groups (each of which possessesuniquely derived karyotypes; see KaryotypeEvolution Revisited below) were each othersclosest relatives, with this clade potentiallysupported by a single centric fusion. A sex-lineatus group tigris group relationshipwas also strongly supported by mitochondri-

al restriction site data in Moritz et al.(1992a). Thus, there appears to be strongconflict between our mitochondrial rDNA se-

quences and the mitochondrial restriction sitedata of Moritz et al. (1992a). Since the mi-tochondrial genome is inherited as a single,nonrecombining unit (Brown, 1981, 1983),these two mtDNA data sets might be ex-pected to yield the same result. Nevertheless,the nature of the restriction sites and the nu-cleotide gene sequences are quite differentdata sets, based on different details in themtDNA.

Based on shared identical karyotypes,Lowe et al. (1970) and Robinson (1973) pro-posed that the Baja California Cnemidopho-rus ceralbensis and C. hyperythrus(sen-su lato; see Grismer, 1999) were closely re-lated to the mainland Mexico deppii group

(C. deppii, C. guttatus, and C. li-neatissimus). However, since Lowe et al.(1970) also hypothesized that the deppiigroup possessed the ancestral karyotype ofCnemidophorus, it was possible that theBaja taxa were being placed within the dep-piigroup by the possession of a shared prim-itive trait. Also, members of the C. hy-perythruscomplex (Grismer, 1999) and C.ceralbensis share a uniquely derived feature(i.e., undivided frontoparietal scale; Walker

et al., 1966; Walker and Taylor, 1968), butevidence supporting a specific relationship ofthe Baja clade to the remaining deppii grouptaxa has been lacking. The results of our cur-rent study corroborate and strongly supporta close relationship between the Baja Cali-fornia C. hyperythrus and the mainlandMexico deppii group, with these data sup-porting the placement of C. hyperythrusas the sister taxon to the C.deppii C.guttatus clade.

Species limits within the tigris group are

controversial, with recent checklists recog-nizing anywhere from a single, widespreadpolytypic species (Wright, 1993) to eightspecies (Maslin and Secoy, 1986). Also, thephylogenetic relationships among the 20named taxa (i.e., subspecies and species) arelargely unknown, with only the recent mo-lecular study by Radtkey et al. (1997) pro-viding a preliminary hypothesis of relation-ships for the Baja taxa. The goal of our studywas not to rigorously evaluate the relation-

ships within the tigris group. However, evenwith this limited sampling, significant pre-liminary results are evident. Cnemidopho-


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rus tigris maximus (C. maximusof Mas-lin and Secoy [1986]) of the Cape Region ofBaja California is placed as the sister taxonof all remaining tigris group taxa in ourstudy. This finding is consistent with Radt-key et al. (1997), whose mitochondrial cy-tochrome b data suggested that a clade ofsouthern Baja California C. tigris popu-lations (including C. t. maximus) was thesister taxon to a clade containing the northernBaja taxa and the few non-Baja Californiapopulations they studied. Our data alsostrongly support the placement of C. t.marmoratus as the sister taxon to the re-maining western U.S. C. tigris taxa. Sucha finding is significant, because it demon-

strates that the ongoing and evidently unre-stricted hybridization between the geograph-ically proximate C. t. marmoratus andC. t. punctilinealis (see Dessauer et al.,2000) is between relatively distantly relatedC. tigris lineages.

With 20 recognized species, the sexli-neatus group is the largest species groupwithin the North American Cnemidopho-rus clade. While we excluded the unisexualtaxa and included only seven bisexual spe-

cies in our study (thus limiting what can behypothesized regarding sexlineatus groupevolution), our results are reasonably congru-ent with some past hypotheses ofsexlineatusgroup relationships. Our data strongly sup-port a clade containing C. inornatus andC. sexlineatus. However, the placement ofthis clade within thesexlineatusgroup is am-biguous. The uniformly weighted analysisweakly supported its placement within aclade containing C. burti and C. cos-tatus griseocephalus (fig. 2), whereas the

successively weighted analysis placed theC. inornatus C. sexlineatus clade asthe sister taxon to all remaining sexlineatusgroup taxa (fig. 3). Moritz et al. (1992a) hy-pothesized a relationship similar to that in-ferred in the successive weighted analysis,with the C. inornatus C. sexlineatusclade being relatively basal within the sexli-neatus group.

Much taxonomic confusion exists withinthe Cnemidophorus gularis complex.

Walker (1981a, 1981b) concluded that C.septemvittatus and C. scalaris were con-specific (but heterosubspecific) with C.

gularis. More recently, Wright (1993) (with-out comment) elevated C. g. gularis tospecific status and treated C. scalaris as asubspecies of C. septemvittatus (seeCrother et al., 2001, regarding taxonomic un-certainty as to correct specific epithet forC. scalaris/septemvittatus). While oursampling is inadequate to address the specieslimits problems within the C. gulariscomplex, the results of our data analysis areconsistent with these three taxa being veryclosely related. For now, we have followedthe taxonomic recommendation of Walker(1981a, 1981b), but acknowledge that addi-tional work is needed in this group.

Within the sexlineatus species group, the

species complex involving the polytypicCnemidophorus burti and C. costatushas also bewildered past Cnemidophorussystematists. While we made no rigorous at-tempt to thoroughly resolve these uncertain-ties, our data provide new insight into thepotential magnitude of the problem. For ex-ample, our data do not support the suppos-edly conspecific C. costatus costatus andC. c. griseocephalus as being each othersclosest relatives. The placement of C. c.

costatus as being closely related to the C.gularis complex (figs. 2A, 3) is consistentwith the findings of Duellman and Zweifel(1962). Duellman and Zweifel (1962) com-mented on southern Mexico populations ten-tatively assigned to C. costatus. They not-ed that these populations were similar toC. c. costatus, but also had attributes lik-ening them to C. septemvittatus. As forC. c. griseocephalus, Dessauer and Cole(1989) provided evidence (allozymes) thatthis taxon was genetically more similar to

C. burti than to C. c. costatus (mis-identified as C. deppii in Dessauer andCole, 1989). Without comment, Wright(1993) considered C. c. griseocephalus tobe conspecific with C. burti (his C.burti griseocephalus), an action possiblyprompted by the data of Dessauer and Cole(1989). The results of this phylogenetic anal-ysis do not support a particularly close rela-tionship of this taxon to C. burti or C.c. costatus (figs. 2, 3). Our study further re-

inforces the complexity of the problemswithin the C. burti/costatus complex, andsuggests that future endeavors to resolve


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their species limits may require the consid-eration of the C. gularis complex as well.

AMEIVA PHYLOGENY

Compared to Cnemidophorus, our tax-on sampling within Ameiva was not exten-sive, with two species from each of the fol-lowing areas: West Indies (A. auberi, A.chrysolaema), Central America (A. quadrili-neata, A. undulata), and South America (A.ameiva,A. bifrontata). Even with this limitedsampling, our data show that Ameiva is par-aphyletic. The West Indian clade is placed asthe sister taxon of the clade containing C.longicaudus and the Nor th Ame rica n

Cnemidophorus. The other Ameivaspecies are more closely related to the neo-tropical C. lemniscatusgroup (sensu stric-to) and Kentropyx. However, most of theseinferred relationships for Ameiva areweakly supported, with strong support foronly two small clades: A. auberi A.chrysolaema and A. ameiva A. bif-rontata. While Ameiva phylogeny was notone of the main foci of this study, it is evi-dent that additional phylogenetic studies ofAmeiva are needed.

EVOLUTION OF TONGUE CHARACTERSTRADITIONALLY USED IN CNEMIDOPHORINE

SYSTEMATICS

Historically, finding characters to diagnoseCnemidophorus from Ameiva has beenproblematic. Burt (1931) used attributes ofthe tongue as the only real basis for differ-entiating these genera: (1) Ameiva pos-sesses a sheath at the base of the tongue (vis-ibly separating it from the glottis) and has

the posterior margin of the tongue not forked(or only slightly so); and (2) Cnemidopho-rus lacks a basal tongue sheath and has theposterior margin of the tongue clearly forked(possessing an arrowhead- or heart-shapedtongue, according to Burt [1931]). However,not all species have perfectly fit this scheme,with C. lacertoidesbeing a species of tax-onomic instability. Without comment, Burt(1931) transferred this species to Ameiva(leaving one to assume that this species pos-

sessed the two lingual characteristics ofAmeiva). Milstead (1961) and Presch(1971) noted that this species exhibited the

Cnemidophorus tongue type and recom-mended that this species be placed back inCnemidophorus, whereas Vanzolini andValencia (1966) believed the tongue structurewas more similar to Ameiva. The confu-sion largely stems from the fact that C.lacertoides does not perfectly fit the diag-nosis developed by Burt (1931). Cnemido-phorus lacertoides possesses a distinctlyforked posterior edge of the tongue (as inother Cnemidophorus), but also exhibitsthe tongue sheath characteristic of Amei-va. The results of our phylogenetic analysisshed some light on the evolution of thesetongue characters in teiines and help deter-mine which teiines can be diagnosed by de-

rived character states.The absence of a tongue sheath appears to

be the ancestral condition for teiines (absentin the most recent common ancestor of Tei-ini; Clade 1 of figs. 2, 3). However, the an-cestral condition for cnemidophorines (Clade3 of figs. 2, 3) is ambiguous, with each ofthe following evolutionary scenarios beingequally parsimonious: (1) The absence of atongue sheath is ancestral for cnemidophor-ines, with independent origins of a tongue

sheath in the ancestor of the neotropicalclade (Clade 4 of figs. 2, 3; reversal inCnemidophorus lemniscatus complex)and the West Indian Ameiva (Clade 18 offig. 2; Clade 19 of fig. 3); or (2) presence oftongue sheath is a synapomorphy of cnemi-dophorines, with independent losses in theC. lemniscatuscomplex and the C.lon-gicaudus North American Cnemidopho-rus clade (Clade 19 of fig. 2 or Clade 20of fig. 3). While the evolution of this char-acter among cnemidophorines is largely am-

biguous, under both scenarios the C. lem-niscatus complex has secondarily lost thetongue sheath.

A distinctly forked posterior edge of thetongue is the ancestral condition for Teiini,as well as the cnemidophorines. The derivedloss of the forking occurred independently atleast twice among cnemidophorines: (1)Once in the West Indian Ameiva (Clade18 of fig. 2; Clade 19 of fig. 3); and (2) oneor two times among the neotropical cnemi-

dophorines. Within the neotropical cnemi-dophorine clade, the distinctive forking ofthe posterior edge of the tongue was either


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lost once in the ancestor of Clade 5 (figs. 2,3) or lost twice (independently in Clade 6and A. undulata). If the forking was lostonly once among the neotropical cnemido-phorines, then a reversal must have occurredin the ancestor of the Cnemidophoruslem-niscatus complex Kentropyx clade (Clade9 of figs. 2, 3). Under any of the above evo-lutionary scenarios, it is apparent that thediagnostic distinctly forked posterior edgeof the tongue is the plesiomorphic conditionfor all Cnemidophorus. Unfortunately, thebasal teiine and cnemidophorine relation-ships are weakly supported, with some ofthese currently inferred relationships likely tochange with the addition of more data (e.g.,

placement of C. longicaudusand the WestIndian Ameiva; see Taxonomic Implica-tions and Nomenclatural Recommendations).Thus, any future phylogenetic rearrange-ments will likely require a reassessment ofthe evolution of these two tongue charactersthat historically have played an importantpart in cnemidophorine systematics.

TAXONOMIC IMPLICATIONS ANDNOMENCLATURALRECOMMENDATIONS

One of the main goals of this study wasto test Cnemidophorus monophyly, aswell as the monophyly of the currently rec-ognized bisexual Cnemidophorus speciesgroups. Our study demonstrates that Cnem-idophorus is paraphyletic with respect toAmeiva and Kentropyx. Given this result,nomenclatural changes are needed in order tomaintain a classification that more accuratelyreflects the evolutionary relationships withinthe cnemidophorine clade (Clade 3; figs. 2,

3). Within this large assemblage exists astrongly supported clade that has informallybeen referred to as the North AmericanCnemidophorus clade (Clade 20 of fig. 2;Clade 21 of fig. 3). This clade contains themonophyletic deppii, sexlineatus, and tigrisspecies groups and their associated unisexualtaxa. Except for C. longicaudus and C.ocellifer, all other species of the Cnemido-phorus lemniscatus group (i.e., the C.lemniscatus complex, C. murinus, and

C. lacertoides) are more closely related toCentral and South American Ameiva andKentropyx than to members of the North

American Cnemidophorus clade. Cnem-idophorus ocellifer was weakly placed asthe sister species to the large clade contain-ing Ameiva, Kentropyx, and all otherCnemidophorus, and C. longicauduswas weakly placed as the sister species of theNorth American Cnemidophorus clade.

If our goal is to recognize monophyleticgroups, then widespread nomenclaturalchange is required. One option would be toclassify all cnemidophorine species of Clade3 (figs. 2, 3) into a single large taxon. In thiscase, Ameiva Meyer, 1795, would have pri-ority over CnemidophorusWagler, 1830, andKentropyx Spix, 1825. A second optionwould be to name the more exclusive well

supported cnemidophorine clades (withinClade 3) that are morphologically distinctand/or geographically coherent. We do notfavor the first alternative for two reasons.First, this former option would subsumelong-recognized and morphologically dis-tinctive groups (e.g., Kentropyx) under a sin-gle name. Second, we feel that the recogni-tion of a single taxon (i.e., an expandedAmeiva) would obscure the true phyletic di-versity within this large and diverse assem-

blage. Given this, we find it necessary to res-urrect Aspidoscelis as the available genericname for species of the North AmericanCnemidophorus clade (Clade 20 of fig. 2;Clade 21 of fig. 3). As the type species ofCnemidophorusis C. murinus, that gener-ic name remains with the South Americantaxa (see additional details below).

AspidoscelisFitzinger, 1843

Aspidoscelis Fitzinger, 1843: 20.

VerticariaCope, 1870: 158 (type species, Cnem-idophorus hyperythrus Cope).

TYPE SPECIES: Lacerta sexlineata Linnae-us, 1758, is the nominal type species.

ETYMOLOGY: Aspidoscelis was first namedby Fitzinger (1843). He merely listed it as asubgenus ofCnemidophorus, with the com-ment that the type species is Lacerta 6-linea-ta Linnaeus ( Cnemidophorus sexlineatus).No etymology was presented.

The name probably was derived from two

Greek nouns, aspido, meaning shield, andscelis, meaning rib or leg. This seemsappropriate, because it could refer to the


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large scales on the legs and has a meaningsimilar to that ofCnemidophorus: equippedwith leggings.

According to the International Code ofZoological Nomenclature (1999, art. 30),gender of a compound word is that of thefinal component if it is a noun, so Aspidos-celisis feminine, although Cnemidophorusismasculine. Consequently, in the list of taxabelow, we emend the specific and subspecificepithets for agreement with the femininegender (ICZN, 1999, art. 31.2). Specialthanks are due to Darrel Frost for providingthese emendations.

CONTENT: The genus Aspidosceliscontainsat least 87 currently recognized bisexual and

unisexual taxa. The following list of taxa isa blend of those recognized by Grismer,1999; Maslin and Secoy, 1986; Taylor andWalker, 1996; Walker, 1981a, 1981b; Walkeret al., 1997; Wright, 1993; and Wright andLowe, 1993. Given the complex nature of theinterrelationships among the described taxaof the A. burti, A. costata, and A. gulariscomplexes, many additional evolutionaryspecies may exist withinAspidoscelis. We re-alize that no two individuals or teams of her-

petologists would independently come upwith the same list of species and subspeciesrecognized these days for such a large andcomplex genus (especially given the insularforms), but this is our best working hypoth-esis for now.

The Aspidoscelis cozumela Group: A. coz-umela; A. maslini; A. rodecki.

The Aspidoscelis deppii Group: A. car-menensis; A. ceralbensis; A. danheimae; A.deppii; A. d. deppii; A. d. infernalis; A. d.schizophora;A. espiritensis;A. franciscensis;

A. guttata; A. g. guttata; A. g. immutabilis;A. g. flavilineata; A. hyperythra; A. h. hyper-ythra; A. h. beldingi; A. lineatissima; A. l.lineatissima; A. l. duodecemlineata; A. l. ex-orista; A. l. livida; A. picta.

The Aspidoscelis sexlineata Group: A. an-gusticeps;A. a. angusticeps;A. a. petenensis;A. burti; A. b. burti; A. b. stictogramma; A.b. xanthonota; A. calidipes; A. communis; A.c. communis; A. c. mariarum; A. costata; A.c. costata; A. c. barrancorum; A. c. griseo-

cephala; A. c. huico; A. c. mazatlanensis; A.c. nigrigularis; A. c. occidentalis; A. c. zwei-feli; A. exsanguis; A. flagellicauda; A. gular-

is; A. g. gularis;A. g. colossus;A. g. pallida;A. g. scalaris; A. g. septemvittata; A. g. sem-ifasciata; A. g. semiannulata; A. innotata; A.inornata; A. i. inornata; A. i. arizonae; A. i.cienegae; A. i. chihuahuae; A. i. gypsi; A. i.heptagramma; A. i. juniperus; A. i. llanuras;A. i. octolineata; A. i. pai; A. i. paulula; A.labialis; A. laredoensis; A. mexicana; A. mo-taguae; A. opatae; A. parvisocia;A. sacki;A.s. sacki; A. s. gigas; A. sexlineata; A. s. sex-lineata; A. s. viridis; A. sonorae; A. unipar-ens; A. velox.

The Aspidoscelis tesselata Group: A. dix-oni; A. neomexicana; A. neotesselata; A. tes-selata.

TheAspidoscelis tigris Group:A. tigris;A.

t. tigris; A. t. aethiops; A. t. disparilis; A. t.marmorata; A. t. maxima; A. t. multiscutata;A. t. pulchra;A. t. punctilinealis;A. t. rubida;A. t. septentrionalis; A. t. stejnegeri;A. t. un-dulata; A. t. variolosa.

DEFINITION AND DIAGNOSIS: Tongue mor-phology: Basal tongue sheath absent and pos-terior portion of tongue clearly forked. Scu-tellation: Smooth ventral scutes; eight rowsof ventral scutes across midbody; granulardorsal scales; anal spurs in males absent; me-

soptychial scales abruptly enlarged overscales in gular fold, more anterior ones be-coming smaller; three parietal scales; three orfour supraocular scales on each side.

The above combination of traits distin-guishes Aspidoscelis from all other cnemi-dophorine teiid genera. Aspidoscelis differsfrom Kentropyx by the absence of keeledventral scutes and the absence of enlargedanal spurs in males (presence of keeled ven-tral scutes in Kentropyx is unique among te-iids). Aspidoscelis can also be differentiated

from all species currently placed in Amei-va by the absence of a basal tongue sheath(present in Ameiva) and the possession ofa distinctly forked posterior portion of thetongue (not clearly forked in Ameiva).

Species of Aspidoscelis are easily distin-guished from Cnemidophorus murinus andthe C. lemniscatus complex by the followingattributes: (1) lack of anal spurs in males(present inC. murinusand theC. lemniscatuscomplex); (2) presence of abruptly enlarged

mesoptychial scales, with more anteriorscales becoming smaller (somewhat enlargedin C. murinus and the C. lemniscatus com-


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plex, with more anterior mesoptychials be-coming abruptly enlarged); and (3) presenceof three parietal scales (five in C. murinusand the C. lemniscatus complex).

Aspidoscelis differs from Cnemidopho-rus ocelliferby the presence of three pari-etal scales (five in C. ocellifer). Also,most species ofAspidoscelis possess slightlyto greatly enlarged postantebrachial scales(most species within the A. sexlineatagroup), whereas the postantebrachials aregranular in C. ocellifer. Species of Aspi-dosceliscan be differentiated from C.lac-ertoides by the following traits: (1) absenceof a basal tongue sheath (present in C.lacertoides); (2) eight rows of ventral scutes

across midbody (1012 in C.lacertoides);and (3) presence of three parietal scales (fivein C. lacertoides). Also, as in C. ocel-lifer, C. lacertoides possesses granularpostantebrachial scales. And finally,Aspidos-celis can be distinguished from C. longi-caudusby the presence of eight rows of ven-tral scales across midbody (1012 in C.longicaudus) and abruptly enlarged meso-ptychial scales over the gular fold scales(somewhat enlarged in C. longicaudus).

Some populations of A. tigris have second-arily reduced mesoptychials, thus resemblingC.longicaudus. However, allA. tigristyp-ically have only eight ventral scutes acrossthe midbody.

DISTRIBUTION: Aspidoscelis occursthroughout most of North America (exceptCanada), reaching the East and West Coastsof the United States, and ranging souththrough all of Mexico into Central America.Its southern limit is in extreme northwesternCosta Rica. Range maps for the species

groups are provided in Wright (1993).COMMENT: Our data place the South Amer-

ican Cnemidophorus longicaudus as thesister species of Aspidoscelis, and its inclu-sion inAspidosceliswould be consistent withthe phylogeny (figs. 2, 3). However, thisplacement of C. longicaudus is veryweakly supported. We suspect that the trueaffinities of C. longicaudus lie with theother lemniscatus group species andAmeiva in South America. Preliminary se-

quence data from additional mitochondrialgenes (Bell and Reeder, unpubl. data) lendsupport to this suspicion. Therefore, the ex-

clusion of C. longicaudus from Aspidos-celisin this paper probably prevents the dem-onstration of paraphyly ofAspidoscelisin fu-ture studies. As currently defined, Aspidos-celis is a strongly supported andgeographically coherent clade. Within Aspi-doscelis, there is strong support for themonophyly of the deppii, sexlineata, and ti-gris species groups; thus, we advocate thecontinued recognition of these informal su-praspecific groups formerly associated withCnemidophorus. While our present phy-logenetic analysis did not include all of thedescribed bisexual species of the aforemen-tioned species groups, we are confident oftheir proposed group membership (based

largely on karyotypic data; see KaryotypeEvolution Revisited), and strongly doubt thattheir inclusion in future phylogenetic studieswill renderAspidoscelisparaphyletic. And fi-nally, the species of the unisexual cozumelaand tesselata species groups are also includ-ed in the genus Aspidoscelis, as these uni-sexuals are derived from hybridization eventswithin Aspidoscelis.

The removal of all of the North Americantaxa from Cnemidophorus leaves only the

lemniscatus group species withinCnemi-dophorus (sensu stricto). However, the rec-ognition ofAspidoscelis still does not makeCnemidophorusmonophyletic (due to lem-niscatus group paraphyly). Within Clade 3(figs. 2, 3) there exists a strongly supportedclade that corresponds to the C. lemnis-catus complex (Clade 10). Based on onlymorphological data, C. murinus is placedas the sister species of the lemniscatus com-plex. Also, all males of this clade (C. mu-rinus lemniscatus complex) possess two

anal spurs (one per side), while all remainingspecies of the lemniscatusgroup lack analspurs. Since the type species of Cnemido-phorus is C. murinus, Cnemidophorus couldbe made monophyletic by restricting thisname to the strongly supported and morpho-logically distinct clade containingC. murinusand the C. lemniscatus complex. However,that still leaves us with the problem of whatto do with the remaining lemniscatusgroup species lacking anal spurs (i.e., C.

lacertoides, C. longicaudus, and the C. ocel-lifer complex). To maintain Cnemidophorusmonophyly, each of these taxa would have


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to be removed from Cnemidophorus andplaced into other taxa (e.g., Ameiva).

The phylogenetic placements of Cnemi-dophorus longicaudus, C. lacertoides, andC.ocellifer suggest erecting monotypic generafor each species. Cnemidophorus ocelliferwas originally described and placed inTeius.However, because of the pentadactyl condi-tion of the hind foot of C. ocellifer and itsresemblance to Cnemidophorus, Burt (1931)transferred this species to Cnemidophorus.Our current data do not support a close re-lationship between C. ocellifer and Teius;thus, a new generic name is needed for C.ocellifer (and probably to include the othermembers of theC. ocellifercomplex; see Ro-

cha et al., 1997, 2000). Cnemidophorus lon-gicaudus was originally placed in Ameiva,and C. lacertoides has had an unstable tax-onomic history, withC. lacertoidesbeing re-peatedly shifted between Cnemidophorusand Ameiva (Burt, 1931; Vanzolini and Va-lencia, 1966; Cole et al., 1979). Initially, itmay appear that the appropriate action wouldbe to return C. longicaudus and C. lacerto-ides to Ameiva. However, these two speciesare not closely related, nor are they closely

related to any Ameiva. Furthermore, Ameivais also paraphyletic, so no benefit would re-sult by moving these two Cnemidophorusspecies from one paraphyletic taxon to an-other.

As previously mentioned, the phylogeneticplacements ofC. longicaudus, C. lacertoidesand C. ocelliferare weakly supported. Giventhis, we prefer to tentatively leave these threespecies within Cnemidophorus, even thoughsuch an action renders Cnemidophorus par-aphyletic. We feel that a better understanding

of the phylogenetic relationships among theSouth American Cnemidophorus speciesis needed before additional taxonomic chang-es (e.g., transfer of taxa to existing generaand/or the proposal of new genera) should bemade. Ultimately, we suspect that Cnemido-phoruswill be restricted to those species pos-sessing anal spurs in males (i.e., C. murinusand the C. lemniscatus complex). However,such a conclusion requires that additionaldata and taxa (i.e., C. ocellifercomplex spe-

cies and additional species ofAmeiva) be in-cluded in future studies before final taxo-nomic recommendations are proposed.

MATERNAL ANCESTOR OF KENTROPYXBORCKIANA

As Kentropyx borckiana was known onlyfrom female specimens, Hoogmoed (1973)and Gallagher and Dixon (1992) were thefirst to suggest that it was yet another uni-sexual teiid species. Gallagher and Dixon(1992) hypothesized that K. borckiana (likeother unisexual teiids) was of hybrid origin,with the bisexual K. calcarata andK. striatabeing the ancestor species. Based upon anextensive analysis of morphology and allo-zymes, Cole et al. (1995) confirmed that K.borckiana was of hybrid origin involving K.calcarata and K. striata. Cole et al. (1995)

were also able to exclude K. altamazonica (athird bisexual species occurring near K.borckiana) of any involvement in the hybrid-ization event giving rise to K. borckiana.While both ancestral species had been deter-mined with confidence, it was not knownwhich of the two bisexual species had beenthe maternal ancestor.

Karyological (e.g., Cole, 1979) and allo-zymic (e.g., Cole et al., 1988; Dessauer andCole, 1989) studies have been successful in

determining the ancestral species involved inthe hybrid origins of many unisexual lizards.However, such methods could not elucidatewhich was the maternal and which was thepaternal ancestor. With the advent of meth-ods to effectively assay mitochondrial DNA,this maternally inherited molecular markerhas been instrumental in elucidating the ma-ternal ancestral species in numerous unisex-ual teiid species (e.g., Brown and Wright,1979; Densmore et al., 1989a, 1989b; Moritz

et al., 1989b). In our phylogenetic study, theKentropyx borckiana mtDNA stronglygrouped (bootstrap 97100%) with K. stria-ta. Overall, the single K. borckiana mtDNAsequence differed from theK. striatamtDNAby only 0.9%. Using allele-specific oligonu-cleotides (see Dessauer et al., 1996) designedfor the detection of K. calcarata and K. stri-ata 12S mtDNA, we determined that an ad-ditional K. borckiana individual also pos-sesses K. striata-like mtDNA (fig. 5). Thus,

we provide strong evidence implicating K.striata as the maternal ancestor of the uni-sexual K. borckiana.


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Fig. 5. Dot-blot illustrating specificity of theallele-specific oligonucleotide probes (ASOs).DNA samples from 16 lizards of the genus Ken-tropyx from Ecuador, Guyana, Surinam, and Ven-

ezuela were applied in rows A and B of a strip ofnitrocellulose paper. After heat denaturation, theblot was hybridized successively with the STR-ASO probe (specific forK. striata;left), and, afterstripping, with the CAL-ASO probe (specific forK. calcarata; right). Lizards in row A, positions16 were specimens of K. striata, and lizards inrow A, positions 7 and 8 were specimens of K.borckiana, showing that the probe binds with themtDNA of these two species (i.e., the mtDNA ofthe unisexual K. borckiana is similar to that ofK.striata). Lizards in row B, positions 15 werespecimens ofK. calcarata; row B, positions 6 and

7 were specimens ofK. altamazonica; and row B,position 8 was a specimen of K. pelviceps. Notethat only individuals ofK. calcarata bind with theCAL-ASO probe, and in particular, individuals ofthe unisexual K. borckiana do not. See Dessaueret al. (1996) for details on the ASO methodology.

UNISEXUAL SPECIES: AN OVERVIEW

TEIOID UNISEXUAL SPECIES: There are nu-merous unisexual species within the Teiidae,

and two or more occur among their closestrelatives, the microteiids or Gymnophthal-midae. All of the unisexual taxa that have

been studied in detail consist of parthenogenswith a clonal pattern of inheritance, and theyhad a hybrid origin. Figure 6 illustrates thereticulate phylogeny of the teioid unisexualspecies, in which the numbered nodes indi-cate the following:

1. The Gymnophthalmidae is a diverse andunderstudied neotropical group. To date, oneconfirmed and two apparent unisexual line-ages have been discovered. In the northernpart of its range, Gymnophthalmus under-woodi is a diploid clonal parthenogen of hy-brid origin (Cole et al., 1990, 1993; Kizirianand Cole, 1999). However, some Brazilianpopulations assigned to G. underwoodi aremorphologically and genetically distinct and

apparently represent a different lineage(Yonenaga-Yassuda et al., 1995), which re-quires additional research. In addition, Le-posoma percarinatum probably is at leastone unisexual lineage also (Uzzell and Barry,1971; Hoogmoed, 1973; Avila-Pires, 1995).

2. Teius suquiensis is known on the basisof more than 160 specimens, all females(Avila and Martori, 1991). No genetic dataare available for comparing this taxon withbisexual species ofTeius.

3. Cnemidophorus cryptus is a diploidclonal parthenogen of hybrid origin (Des-sauer and Cole, 1989; Sites et al., 1990). Twoclones probably originated from separate F1hybrid zygotes (Cole and Dessauer, 1993),although it is not known whether these wereproduced by the same individual parents orin the same clutch of eggs. The current work-ing hypothesis is that C. gramivagus andC. lemniscatus are the two ancestral spe-cies (Cole and Dessauer, 1993).

4. Cnemidophorus pseudolemniscatus

is a triploid clonal parthenogen of hybrid or-igin, which is hypothesized to have beenC. cryptus C. lemniscatus (Dessauerand Cole, 1989; Cole and Dessauer, 1993).

5. Kentropyx borckiana is a diploid clonalparthenogen of hybrid origin (Hoogmoed,1973; Cole et al., 1995). In this study wehave determined that K. striata was the ma-ternal ancestor (see above).

6. Aspidoscelis rodecki and the A. cozu-mela complex are diploid unisexuals of the

cozumelaspecies group. Both taxa are of hy-brid origin, withA. deppiiand A. angusticepsbeing the probable bisexual ancestors (Fritts,


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Fig. 6. Phylogeny depicting the hybrid origins of teiid unisexual species. Dashed lines indicate thatnot all relevant taxa are included in the given phylogeny. The solid square denotes the true Cnemi-dophorus clade (those taxa possessing anal spurs in males; see text).


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teiidae_cnemidophorus phylogeny

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