HERPETOLOGICAL JOURNAL, Vol. 11, pp. 137- 150 (2001)

A PHYLOGENETIC ANALYSIS OF LIZARDS OF THE LIOLAEMUS CHILIENSIS GROUP (IGUANIA: TROPIDURIDAE)

FERNANDO LOBO

Catedra de Anatomia Comparada - Facultad de Ciencias Naturales, Universidad Nacional de Salta, Argentina

The lizard genus Liolaemus includes over 160 species of which almost ha lf are in the c�iliensis group. Although some researchers have attempted to define smaller species groups within this_ large clade, the relationships among the taxa within the group as a whole remain enigmatic. The objectives of this study were to ( 1) identify characters that will be useful for present and futurephylogenetic studies of this group, and (2) generate preliminary phylogenetic hypotheses fortaxa within this large clade of liza rds. I examined more than 800 specimens of 73 taxa belonging to the chiliensis group from which I identified 55 phylogenetically informative morphological characters. Additional characters (6) were derived from published and unpublished data on chromosomes, life history, and ecology. Four species considered basal for the genus were taken as o�tg'.oups. A tree-building program (PAUP 4.0b2) recovered three trees of length 11.516(Retention index: 0.59). Differences found among these topologies were restricted to the relationships of species of the elongatus group, in which monophyly was recovered in only one tree . Results fr om PAUP's analysis support the monophyly of several previously proposed . species groups: alticolor, altissimus, gravenhorstii, hellmichi, kriegi, leopardinus, monlicola, nigromaculatus, nigroviridis, pie/us and tenuis. Interestingly, most of the groups indicated above are endemic to areas that have recently been described as areas of high endemism for southern South America. Key words: phylogeny, cladistics, iguanids, South American lizards

INTRODUCTION (Eulaemus) distributed on the western and eastern sides of the Cordillera de los Andes, respectively. Laurent Liolaemus is one of the most species-rich genera of 983a) also recognized the basal position of L. lizards. Currently, more than 160 taxa have been de­ (l archeforus, L. kingii, L. lineomaculatus, _ and L. scribed and many others await description (Etheridge & magellanicus and the relationship between the latter Espinoza, in review). Species belonging to Liolaemus - two species - with species described under the genus are distributed primarily throughout South America's Vilcunia (Donoso-Barros & Cei, 1971). Laurent (1983) southernportion, fromthe southerntip of the continent considered valid the subgenus Ortholaemus (Cei, in Tierra de! Fuego to central Peru. They are found on 1979). Laurent's 983a) proposal was amplified in a both the east and west sides of the Andes and are impor­ (l subsequent publication (Laurent, 1985) which also in­ tant vertebrate components of the Patagonian steppe, cluded a hypothesis concerning the main Liolaemus and the Monte, Prepuna, Puna and Andean ecosystems species groups. Despite the lack of a cladistic analysis, (Cabrera & Willink, 1980). Perhaps as a consequence Laurent's (1985) paper provided an important first step of their high species diversity, the intrageneric relation­ toward understanding the evolutionary history of the ships are largely unresolved. genus. The first comprehensive taxonomic treatments of Other subdivisions of the genus have been proposed Liolaemus were conducted by Ortiz (1981) and Laurent by Cei (1986, 1993): 28 species groups, 12 of which are ( 1983, 1984, 1985). Ortiz (1981) divided the species subsets of the chiliensis group (sensu Etheridge, 1995; then included in Liolaemus into 25 groups, (17 of Table 1). These proposed groupings were based on which are included in the chiliensis group [sensu combinations of characters used for identificationpur­ Etheridge 1995]; see Table I), but he did not propose poses (not apomorphies). Hence they may or may not any hypothesis concerning the relationships among represent natural groups. these groups. Ortiz (1981) also performed the first Laurent (1992) added to his previous morphometric cladistic analysis of members of the genus (the studies (Laurent, l 983a) other differences between the nigromaculatus group). Based on morphometric analy­ subgenera Liolaemus and Eulaemus: the position of the ses, and through examination of additional characters, nasal openings (lateral in the chileno group and latero­ Laurent (l 983a) defined two main groups which he dorsal in the argentino group), and the shape of the considered distinct subgenera: the "chileno group" supralabials - longer and flattened with the fourth one (Liolaemus sensu stricto) and the "argentino group" turned upward in the chileno group. According to Correspondence: F. Lobo, Catedra de Anatomia Comparada ­ Etheridge (1995), the upturned fourth supralabial is Facultad de Ciencias Naturales, Universidad Nacional de shared with magellanicus and the members of the Salta (UNSa),. Avda. Bolivia 5150, 4.400-Salta, Argentina. lineomaculatus group. Laurent ( 1992) also provided a E-mail: [email protected] 138 F. LOBO

list of the species of both subgenera, Liolaemus and Etheridge's skeleton collection and from alcohol pre­ Eulaemus. In this list, the chileno group included 68 served specimens. tax a. The majority of the characters used in this analysis Most recently, Etheridge (1995) re-examined the were taken fromthe externalmorphology, including 24 taxonomy of Liolaemus from a cladistic perspective. characters associated with squamation; 18 body pat­ He rejected or questioned the validity of the subgenera tern; two coloration; two neck-fold morphology; one Liolaemus, Eulaemus and Ortholaemus, as well as the neck fat pouches; two precloacal pores; one hemipenes, genera Rhytidodeira Girard 1858 (resurrected by three size and ratios; two tooth morphology; one oste­ Laurent, 1985), Phrynosaura Werner 1907, Vilcunia ology; one karyotype; and five physiology and Donoso-Barros & Cei 1971, Pelusaurus Donoso­ ecology. Apomorphic characters of the nitidus, Barros 1973b (previously assigned to subgenus lineomaculatus and chiliensis groups identified by Ortholaemus by Laurent [ l 983b]) , Velosaura and A bas Etheridge (1995) were included in this analysis. Char­ Nunez & Yanez 1984, and Ceiolaemus Laurent 1984, acter states 58 to 61 were kindly provided by Robert because each of these taxa exhibit the synapomorphies Espinoza (unpubl. data), taken mainly from dissec­ of Liolaemus and/or their monophyly was uncertain at tions. that time. Etheridge (1995) renamed the chileno group Although the taxonomic status of several members (Liolaemus sensu stricto, Laurent [ l 983a]) the of the chiliensis group has been controversial, I in­ chiliensis group, which he defined as those Liolaemus cluded each taxon (species and subspecies) belonging with a lower number ofprecloacal pores (fouror fewer) to the group (followingEtheridge, 1995) as a terminal and a fused Meckel's groove. Etheridge (1995) also OTU. Indeed, this analysis may provide reasons forre­ provided an indented taxonomy of currently valid visiting the taxonomic status of many forms. L. Liolaemus species and subspecies. The composition of kingii, archeforus, sarmientoi and lineomaculatus were his chiliensis group is coincident with that of the included as outgroups (following Etheridge, 1995). chileno group of Laurent (1992), with additions for Liolaemus kingii, L. archefo rus and L. sarmientoi were newly described species. However, Etheridge (1995) recently recognized as full species by Cei & Scolaro considered as valid or taxonomically uncertain L. (1996). Twelve taxa were represented by only one or lativittatus (considered a synonym of L. alticolor by two specimens (L. cristiani, L. curicensis, L. Donoso-Barros [1966]), and L. modestus (considered cyanogaster brattstroemi, L. monticola chillanensis, L. as Stenocercus by Laurent [1984], and later confirmed neuquensis, L. nigr oviridis nigroroseus, L. pictus by Ortiz [l 989a]). Also included in his chiliensis group argentinus, L. pictus talcanensis, L. sanjuanensis, L. is the problematic species L. chacoensis. According to tacnae, L. tenuis punctatissimus, L. variegatus). The Etheridge (in litt.), isabelae should have been placed in followingmembers of the chiliensis group were not in­ the chiliensis group, and not in the montanus group. cluded in this study: Liolaemus ceii, L. petrophilus, L. According to this last list (Etheridge; op.cit.), the lativittatus, L. modestus, L. nigroviridis minor, L. pictus chiliensis group has 74 species and subspecies. Two major. Most of the above were excluded because of thirds of these taxa are distributed in Chile, whilst the Jack of specimens for this study, and others because remaining third are from Argentina, Bolivia and Peru. their validity was uncertain (e.g. L. lativittatus and L. As a first attempt to resolve the phylogenetic rela­ modestus). tionships among members of the chiliensis group, I Binary characters that exhibited polymorphism were assembled data on most of the known species and sub­ coded using the frequency bins method (Wiens, 1993, species of this group. Data were taken from external 1995), with 25 character states (a-y). These characters morphology and anatomy, as well as ecological and cy­ were numbers 1, 3, 5-8, 12-13, 16, 18, 24, 28 and 31. togenetic data from the literature for use in this The gap weighting method of Thiele (1993) was ap­ preliminary phylogenetic analysis. plied forcharacters 2, 4, 9, 14, 19, 22-23, 47-48 and 50-52, which represent continuous characters with MATERIAL AND METHODS overlapping ranges - morphometrics or multistate Approximately 800 specimens were examined, rep­ polymorphics. The number of states were 25 (a-y) for resenting 77 species and subspecies of Liolaemus. The maintaining parity with the rest of the characters. Bi­ majority of the species studied (73) was from the nary characters not polymorphic were: 15, 21, 26-27, chiliensis group, (Etheridge, 1995). Most of the mor­ 29-30, 32-39, 41-43, 46, 49, 54-55 and 58. Multistate phological characters were taken from specimens characters not polymorphic were: 17, 25, 40, 44-45, 53, preserved in alcohol. Some characters were examined 56-57 and 59-61. Only characters 17, 20, 53 and 59 with the aid of a hand lens (x 10) or a binocular dissect­ were analysed as being unordered because no evident ing microscope (x 10-40). Measurements were taken series of change were observable. The other characters with electronic verniercalipers to ± 0.01 mm. Neck­ not coded using frequency bins or the gap weighting fold terminology follows Frost (1992). Hemipenes method were weighted by 24. The analysis was per­ were everted and studied following Bohme (1988). formed using PAUP* Version 4.0b2 for 32-bit Tooth morphology characters were taken fromRicha rd Microsoft Windows (Swofford, 1999), applying an PHYLOGENY OF LIOLAEMUS 139

.------4 kingi PAT archeforus PAT .------� sarmientoi PAT .------� constanzae PUN .------� tacnae PUN ------paulinae ATA sanjuanensis MON exploratorum PAT 121 lineomaculatus PAT chacoensis CHA fitzgeraldi AND 120 moradoensis AND altissimus AND araucanensis AND maldonadae AND 127 campanae VAC 119 lorenzmulleri AND nigroviridis AND hellmichi ATA velosoi coa ..------curicensis MAU speciesC PUN alticolor PUN walkeri PUN ---- lemniscatus VAC 11 118 gracilis MON ..------fu scus VAC --- pseudolemniscatus coa platei coa 126 kuhlmanni VAC silvai coa 113 sieversi coa ater coa nigromaculatus coa zapallarensis VA C bitaeniatus MON 151 130 MON 117 saxatilis 112 variegatu� PUN --- pagaouro1 PUN brattstroemi sev cyanogaster sev MAU sCh roederi MAU VAC gravenhorsti VAC chiliensis MAU _VAC nitidus COQ VAC robertmertensi MON bibroni MON PAT hemani AND MAU ramirezae MON donosoi ATA ATA 145 nigroroseus atacamensis ATA bisignatus. coa cop1apenS1s coa ch1llanensis AND monticola AND villaricensis AND argentinus sev chiloensis sev pictus SEV MAU talcanensis sev 147 neuquensis AND coeruleus AND pun�atissimus MAU tenu1s MAU austromendocinus MON cf.elo ngatus MON elongatus AND MON 150 capinitas cristiani AND ris AND ---��• cu isabelae ATA buergeri AND krieg1 AND valcfesianus AND leopardinus AND ra monensis AND

FIG. I. Cladogram of the chiliensis group, the result of a parsimony analysis using PAUP* Version 4.0b2. Considering Liolaemus kingii, archeforus, sarmientoi and lineomaculatus as outgroups (note the inclusion of lineomaculatus within the chiliensis group). Congruence values: Consistency index = 0.20; Retention index = 0.59. Abbreviations forspecies distribution are: AND- Andina; ATA- Atacama; CHA- Chaco; COQ- Coquimbo; MAU- Maulina; MON- Monte (western Argentina); PAT- Patagonia; PUN­ Puna; SEY- Selva Valdiviana; YAC- Valle Central. For more comments see the text. 140 F. LOBO

heuristic search with the tree bisection-reconnection Subclade 117 includes as most external group that (TBR) option for branch swapping. For each analysis, formed by bibroni, hernani and ramirezae (node 1 16); 1 OOO random addition sequence replicates were per­ subsequent sister taxa are curicensis, node 112 (which formed, saving 40 trees at each step. Liolaemus kingii, includes gravenhorstii group, the pair cyanogaster - archeforus, sarmientoi and lineomaculatus were· con­ brattstroemi, and the group formed by bitaeniatus, sidered outgroups following Etheridge (1995). saxatilis and variegatus) and finally, the terminal pair Bootstrap analysis (Felsenstein, 1985) was used to of sister taxa: the alticolor group (node 91) and node evaluate the support forinternal nodes (100 replicates). 101 (containing the nigromaculatus group at node 97). The list of characters is shown in Appendix 1. The content of different groups recovered in this analy­ sis are shown in Table 1. RESULTS After PAUP analysis, three trees were obtained with

a length of 11516 and Rl=0.59 (retention index, Farris, argentinus 133 1989). One of these trees is shown in Fig. 1. Differ­ chiloensis

ences among the three trees are related to the placement pictus of the clade including and 137 elongatus, cristiani capillitas talcanensis (nodes 141 and 139, Figs 2A and B respectively). In neuquensis Fig. 2A this clade is the sister taxon of another contain­ 136 coeruleus ing the pictus group (node I 33), the tenuis group (node 139 136) and the pair austromendocinus c.f. thermarum punctatissi mus (node 138). In Fig. 2B is shown other alternative rela­ tenuis 142 austromendocinus tionship found, in this tree the elongatus clade (node 138 139) is sister taxon only of the group including pictus d. elongatus � and tenuis groups (node 137). The tree shown in Fig. 1 elongatus 141 is the one in which the entire elongatus group is mono­ capillitas

phyletic. 144 cristiani Bootstraping was performed on this data set, but curis found almost no support in the results. The asymmetry 143 of this matrix - with more taxa than characters - prob­ A isabelae ably makes the deletion/resampling methods for yielding consistent results problematical. The best sup­ argentinus ported nodes from 100 replicates are: bisignatus - chiloensis copiapensis (94.9%); punctatissimus - tenuis (52.2%); pictus chillanensis - monticola - villaricensis (monticola 137 group, 47.5%); gravenhorstii - schroederi (46.8%); talcanensis austromendocinus c.f. thermarum (46.7%); neuquensis lineomaculatus - chacoensis (44.3%); nitidus group coeruleus 140 (lineomaculatus plus all chiliensis group species, punctatissimus

43.0%); capillitas - cristiani (42.1%) and hellmichi - tenuis

velosoi (40.7%). elongatus The topology .of the recovered phylogeny is shown 142 capillitas in Figs I and 2. The general structure of the trees show cristiani the leopardinus group as the sister taxon of all other austromendocinus species of the chiliensis group. This is a monophyletic 141 group including monticola, chillanensis and 144 d. elongatus

curis villaricensis. Subsequently, the kriegi group is the most 143

externalto node 145, which includes a clade (node 144, isabelae containingpictus, tenuis and elongatus groups) and the B remaining species of the chiliensis group. Node 130 in­ cludes the monticola group as a sister taxon of the remaining species. The next sister taxon is constanzae, FIG. 2. Two equally parsimonious trees different to that followedby the copiapensis group (5 spp.). Following shown in FIG. I. A, clade including elongatus, capillitas and the structure of the tree we have as subsequent sister cristiani (node 141) is sister taxon of the group containing taxa tacnae, paulinae, sanjuanensis and a node con­ both the tenuis-pictus groups and the species pair austromendocinus and cf. thermarum. Cladogram of the taining two big subclades (nodes 89 and 17). The first I chiliensis group based on a parsimony analysis considering subclade (89), includes altissimus, nigroviridis and all characters equally weighted (PAUP) rooting in Liolaemus hellmichi groups, and a small group formed by kingii. B, same clade (node 139), exclusively sister taxon of exploratorum, chacoensis and lineomaculatus. the pair tenuis-pictus groups. PHYLOGENY OF LIOLAEMUS 141

TABLE I. Comparisons of taxonomic arrangements proposed for species ofthe chiliensis group (sensu Etheridge, 1995). Groups in the third column are those recognized here, based on the results of the present analysis. Groups without equivalents in the third column did not have their monophyly supported in this analysis. Nine of the seventeen groups of Ortiz ( 1981) are monophyletic. *Groups proposed by Cei ( 1986, 1993) only included Argentine species, hence they may not contain all the species belonging to these groups. Cei ( 1986) proposed a bibronii group including L. bibronii, L. sanjuanensis and L. exploratorum and a gracilis only group forthis species. Later, Cei (1993) included L. gracilis in the bibronii group. ** The monophyly of the elongatus group is recovered in one of the three most parsimonious trees founded.

Ortiz(19 81) Cei (1986, 1993)* This study

1. elongatus-kriegi group: elongatus group: austromendocinus, **elongatus group: austromendocinus, buergeri, ceii, capil!itas, elongatus elongatus, austromendocinus, capil!itas, elongatus elongatus, elongatus elongatus petrophilus. cristiani, elongatus, c.f. elongatus. petrophilus, kriegi. kriegi group: buergeri, ceii, kriegi. kriegi group: buergeri, kriegi. 2. alticolor-walkeri group: alticolor group: alticolor alticolor, alticolor group: alticolor, walkeri, alticolor, walkeri, tacnae. alticolor walkeri. sp. nov. 3. constanzae-paulinae group: constanzae, paulinae. 4. /eopardinus group: leopardinus leopardinus group: leopardinus, leopardinus, leopardinus ramonensis, valdes ianus. ramonensis, leopardinus valdesianus 5. altissimus-fitzgeraldi group: altissimus group: altissimus altissimus group: altissimus, altissimus altissimus, altissimus {a ltissimus], fitzgeraldi. araucanensis, moradoensis, araucanensis, altissimus fitzgeraldi. moradensis, altissimus neuquensis, fitzgeraldi. 6. nigroviridis-lorenzmulleri group: nigroviridis group: nigroviridis, nigroviridis group: campanae, nigroviridis nigroviridis, constanzae. lorenzmulleri, maldonadae, nigroviridis nigroroseus, nigroviridis. lorenzmulleri. 8. pictus group: pictus argentinus, pictu group: pictus pictus, pictus pictus group: argentinus, pictus chiloensis, pictus pictus, argentinus. chiloensis, pictus, talcanensis. pictus major, pictus talcanensis. 9. tenuis group: tenuis tenuis, tenuis tenuis group: tenuis, coeruleus. tenuis group: coeruleus, neuquensis, punctatissimus. punctatissimus, tenuis. 10. gravenhorstii-schroederi group: gravenhorstii group: gravenhorstii, gravenhorstii group: chiliensis, gravenhorstii, schroederi. cyanogaster. gravenhorstii, nitidus, robermertensi, schroederi. 11. chiliensis-nitidus group: chiliensis group: chiliensis, chiliensis, nitidus. robermertensi. 12. monticola group: monticola monticola group: monticola, monticola, monticola chillanensis, chil/anensis, villaricensis. monticola vi!laricensis, curicensis. 13.f uscus-lemniscatus: group: /emniscatus group: lemniscatus. fu scus, lemniscatus. 14. hellmichi group: hellmichi. hellmichi group: hel/michi, velosoi. 15. donosoi group: donosoi. see below copiapensis group. 16. nigromaculatus group: nigromaculatus group: ater, bisignatus, copiapensis, kuhlmanni, kuhlmanni, nigromaculatus, platei, nigromaculatus, platei, sieversi, silvai, zapallarensis. zapallarensis zapallarensis, copiapensis group. atacamensis, zapallarensis ater, zapallarensis bisignatus, copiapensis, donosoi, sieversi, n. sp . I, n. sp. 2. nigroroseus. 17. modestus group: modestus. 18. bibronii group: bibronii, bitaeniatus, exploratorum, gracilis, sanjuanensis, saxatilis. 142 F. LOBO

DISCUSSION SPECIES GROUPS

TAXONOMIC STATUS OF TERMINAL TAXA Species belonging to the Liolaemus monticola In the chiliensis group, there are several taxa that group form a monophylethic group. There is no evi­ have proved to be taxonomically contentious. Many of dence of a relationship between these three species and curicensis as proposed by Ortiz (1981; see Table 1 ). these controversies are discussed in Nufiez & Jaksic (1992). These researchers proposed specific status for Navarro & Nufiez (1993) describe isabelae, which the three subspecies of leopardinus and they disagree they include in the nigroviridis group based on the fact with splitting the subspecies nigroviridis and tenuis. that these species plus maldonadae share some similar They also suggested conspecificity of pictus karyological features. In this analysis, these species talcanensis and pictus major. Following the observa­ were placed in different groups. PAUP analysis showed tions of Veloso et al. ( 1982), they also considered the (maldonadae (campanae (lorenzmulleri nigroviridis))) possible conspecificity of constanzae and donosoi. as the nigroviridis group. It is interesting to note that Ortiz (op. cit.) included lorenzmulleri in this group; Cei Nufiez & Jaksic (1992) included in their "nomina dubia" section L. hernani which they considered a pos­ (1993) did the same with constanzae (which is rejected sible synonym of L. curicensis. in this analysis) and Navarro & Nufiez( 1993) with mal­ According to the results obtained in these analysis, donadae. many taxa considered subspecies are independent line­ The Liolaemus altissimus group (Ortiz, 1981; Cei, ages that should be considered full species: 1986) is monophyletic, including moradoensis as a sis­ moradoensis (altissimus moradoensis), campanae ter taxon of the pair altissimus - araucanensis. The (nigroviridis campanae), ater (zapallarensis ater), form named neuquensis was excluded from this group, sieversi (zapallarensis sieversi), nigroroseus being related to the tenuis group. Liolaemus fitzgeraldi (nigroviridis nigroroseus), chillanensis (monticola is the sister taxon of the clade formedby moradoensis, chillanensis), argentinus (pictus argentinus), altissimus and araucanensis. The relationship of chiloensis (pictus chiloensis), neuquensis (altissimus fitzgeraldi with the altissimus group was postulated neuquensis), valdesianus (leopardinus valdesianus). previously by Ortiz (op. cit.) and Cei (op. cit.). The cladogram of Ortiz (op. cit, Fig. 28) for the SYSTEMATIC CONCLUSIONS nigromaculatus group differs mainly from those ob­ In the literature, there exist only a few proposals for tained here in that the pair of sister taxa copiapensis - grouping the species now included in the chiliensis bisignatus is nested within a group that also contains group (sensu Etheridge, 1995). Two authors presented zapallarensis, kuhlmanni and silvai. These last species, systematic arrangements in this sense: Ortiz ( 1981) and plus sieversi, ater and nigromaculatus form a mono­ Cei (1986, 1993). In both cases the definition of groups phyletic group and copiapensis and bisignatus forman were based on character combination instead of independent lineage, as can be seen in Fig. 1. In fact, in synapomorphies. Ortiz (1981) divided Liolaemus into his original description of silvai, Ortiz (l989)b notes 25 groups, 17 of them now should be included in the the proximity of this taxon to kuhlmanni and chiliensis group. Cei ( 1986, 1993) divided species in zapallarensis, and provides a rigorous comparisons be­ the chiliensis group into 12 more inclusive subgroups. tween them. Although the objective of this study was not to propose According to the results of this phylogenetic analy­ a new systematic rearrangement of the chiliensis group, sis, the nigromaculatus group should be considered as it is usefulto analyse the previous proposals and com­ consisting of the following species: nigromaculatus, pare them to the cladistic approach presented here. zapallarensis, ater, sieversi, silvai, kuhlmanni and Table 1 summarizes the systematic arrangements made platei. The other species previously considered belong­ by these two authors; there is a general overlap among ing to this group are not related and form an the two arrangements. The composition of the different independent clade (Fig. 1, node 125): (donosoi groups (previously recognized in the literature) that (nigroroseus (atacamensis (copiapensis bisignatus)))), were monophyletic in PAUP analysis are included in with the exception of velosoi which is the sister taxon of the third column of Table 1. hellmichi (Fig. 1, node 87). The interesting finding ofthis study is the inclusion Species belonging to the elongatus-kriegi group of lineomaculatus in the chiliensis group. The character (Ortiz, 1981) do not form a monophyletic group. Only apomorphic forthe chiliensis group which is the enclo­ as separate groups (Cei, 1986, 1993) is the elongatus sure of Meckel's groove is reverted in this taxon; the group monophyletic in one of three trees, and the kriegi other character described by Etheridge (op. cit) - lower group monophyletic in all trees. Videla & Cei (1996) number of precloacal pores - exhibits great variation: described a new species of the chiliensis group called evenmore precloacal pores are lost in cristiani, thermarum and they suggested that it is related to thermarum, neuquensis and coeruleus than in the neuquensis, coeruleus and cristiani because all these lineomaculatus group. The results of this analysis can lizards lack precloacal pores. In this analysis, charac­ be taken as preliminary, and more studies are needed to ters related to precloacal pores were included (numbers confirm or reject the hypothesis of the inclusion of 47-48), scoring the state "precloacal pores absent" for lineomaculatus in the chiliensis clade. these species (with the exception of thermarum for PHYLOGENY OF LIOLA EMUS 143 which we could not examine specimens for this study). Cordillera). Veloso & Navarro (1988; Fig. I), based on In Fig I these species are included in diffe rent and inde­ Di Castri ( 1968), described seven ecological areas of pendent lineages. It is, therefore, preferable not to distribution for the Chilean herpetofauna, adding one consider this grouping as valid until we have more evi­ area to the six described by Donoso-Barros ( 1966): dence supporting the hypothesis ofmonophyly. Desertica, Tropical, Mediterranea Arida, Mediterranea, Species belonging to Cei's bibronii group (Table I) Mediterranea Humeda, Oceanica and Andina. Veloso in this analysis do not fonna monophyletic group and & Navarro ( 1988) divided the Cordillera of Donoso­ are split into three independent lineages (nodes I 0 I, Barros ( 1966) into Tropical and Andina, Selva into I 12 and I 16). Mediterranea Humeda and Oceanica, but they did not Separate groupings of the chiliensis group and the recognize Patagonia. gravenhorsti group as were proposed (see Table I) are For assigning areas to terminal taxa in the not recovered. There is only the chiliensis group (sensu cladograms of Fig. I, I followed Hellmich (1952): Ortiz, I 98 I) plus robertmertensi. A broader, more in­ Atacama; Roig Juftent ( 1994): Coquimbo, Valle Cen­ clusive group is proposed here including species of tral, Maulina, Selva Valdiviana; Cabrera and Willink both groups previously proposed in the literature, con­ (1980): Chaco, Monte, Patagonia; Veloso and Navarro tammg: chiliensis, nitidus, robertmertensi, ( 1988): Andina; Morrone ( 1996): Puna. I preferthe di­ gravenhorstii and schroederi. (Table I). visions proposed by Roig Juftent (1994) and Morrone DISTRIBUTION ( 1996) because they applied a cladistic methodology for determining areas of endemism. The species of the chiliensis group are distributed Among the basic requirements needed today for over a wide latitudinal-elevational range. For example, cladistic biogeographic studies are: (I) the delimitation bisignatus lives in low-elevational coastal areas, of areas of endemism, and (2) the phylogenetic analysis whereas walkeri lives at elevations as high as 4800 m in of diffe rent groups of organisms (plants or/and ani­ the Peruvian Andes (Veloso & Navarro, 1988). They mals). In this manner, Roig Juftent(1 994) identified 12 occupy almost every type of habitat, from grasslands of areas of endemism for southern South America, based the Puna and other high elevation regions, to low eleva­ on overlaying the distribution of different groups of Ar­ tion habitats such as deserts and Nothofa gus forests. thropoda and plants. In that paper, the historical They can live in deserts (Atacama), going through the relationships between these areas, and New Zealand, central valleys of Chile to the southern Nothofa gus for­ New Caledonia, Australia and South Africa were ana­ ests, etc. Thus, almost every group of Liolaemus has lysed cladistically. liolaemus has representatives in representatives in these quite different areas. It is also every area. However those areas specially rich in spe­ valid to say that each region has generated sufficient cies of this genus are located in the western half of conditions forthe origin and development of groups of southern South America, including his Coquimbo, species (as we will see below). Valle Central, Maulina, Selva Valdiviana, Monte and The major clades discovered in this analysis have a Bosques Orientales areas and his three subdivisions of high geographic homogeneity. Species belonging to the Patagonia. The major groups identified in the chiliensis kriegi, leopardinus, monticola and altissimus groups all group seem to represent endemic areas of speciation in inhabit the Andina region. The majority of species of almost every one of the areas discovered by Roig the nigroviridis group are distributed in the Andina area Juftent (op. cit.). There are I I monophyletic groups, as well. The pictus group is distributed mainly in Selva eight of which exclusively inhabit the Puna area (one Valdiviana and Maulina areas (80% of the species). species group), Coquimbo area (one species group), The stem of the nigromaculatus group, comprising Valle Central and Maulina (one species group), Selva 71.4% of the species (5 spp.), is distributed in Valdiviana (one species group) or the Andean area Coquimbo area (two other species live in the Valle (four species groups). These main Liolaemus areas Central area 28.6%). Species belonging to the alticolor were previously drawn by Hellmich ( 1951; Fig I). group are all distributed in Puna. Species included in The species selected for rooting the analysis (kingii) the gravenhorstii group are distributed mainly (80% of and those most basal for the genus (archefo rus, the species) in Valle Central and Maulina and another lineomaculatus) are distributed mainly in Central lives in the Monte area (robertmertensi). Patagonia. The pictus group (foursubspecies) is found Hellmich (I95 1, 1952) compared the distribution of in the Selva Valdiviana. This area shows the climatic Liolaemus nigromaculatus and its races, the species liv­ and ecological characteristics of the Zona Mediterranea ing in central Chile, the Andes and the austral forests humeda and Zona Oceanica described by Veloso & with his own biogeographic regions (Atacama, Espinal, Navarro (I988). Liolaemus brattstroemi is another en­ de los Bosques, Andina). He compared his observations demic of that area. The Liolaemus gravenhorstii group with those for mammals and he divided the Puna and (five spp.) is present in Valle Central and Maulina the southern Argentine-Chilean Andes into diffe rent (Chile, between 32 and 38° of latitude) and in western areas. Later, Donoso-Barros (I 966; lam. lXXV) indi­ Argentina (L. robertmertensi). Other species are dis­ cated six ecological areas for Chile (Desiertos, tributed in Valle Central and/or Maulina (L.fuscus, L. Matorral, Centrochilena, Selva, Patagonia and lemniscatus, L. hernani, etc.). Another monophyletic 144 F. LOBO

group, the nigromacu/atus group (seven spp.) extends REFERENCES its distribution mainly through the Coquimbo area, an Aiassa, D., Gorla, N., Avila, L. J. & Martori, R. (1998). area between 32 and 27° of latitude. The Andean areas: Citogenetica de Liolaemus (Grupo chiliensis) con Puna and southern Chilean Andes of moderate to high recopilaci6n de los cariotipos reportados y definici6n elevations, exhibit their own endemisms. The Puna re­ de Liolaemus fi tzgeraldi. Resumenes de la XIII gion has the a/tico/or group (three spp.) and the Andes Reunion de Com. Herp. Arg. 2. of southern Chile and Argentina have the a/tissimus Bohme, W. ( 1988). Zur genitalmorphologie der Sauria: group (fourspp.), kriegi group (two spp.), /eopardinus funktionelle und stammeschichtliche aspekte. Bonner group (three spp.), montico/a group (three spp) and Zoologische Monographien, N°27, 176 pp. nigroviridis group (three out of fourspp.). Cabrera, A. L. & Willink, A. (1980). Biogeografia de The Puna province extends across north-western America Latina. Departamento de Asuntos Cientificos Argentina, north-eastern Chile, western Bolivia and y tecnol6gicos de la Sec. Grat. de la Organizaci6n de south-western Peru (Morrone, 1996). The equivalent Estados Americanos (OEA). Serie de Biologia, zones of Veloso Navarro (op. cit.) are Zona Andina & Mo nog. 13, 1-122. and Tropical (Puna). The individual areas of distribu­ Cei, J. M. ( 1979). A reassessment of the genus tion and the ecological regions of the species of the Ctenoblepharis (Reptilia, Sauria, Iguanidae) with chi/iensis group can be traced from Donoso-Barros description of a new subspecies of Liolaemus (1966), Donoso-Barros (I 973a) and Veloso Navarro & multimacu/atus from western Argentina. J. Herpetol. (1988), but only for Chilean species. Data on the Ar­ 13, 297-302. gentine species can be found in Cei (1986, 1993). Cei, J. M. (1986). Reptiles del centro, centro-oeste y sur The results presented here represent the first de la Argentina. Mus. reg. Sci. nat. Torino Monogr. 4, cladistical approach to the analysis of the chiliensis 527 pp. group of Lio/aemus. New observations and characters Cei, J. M. ( 1993 ). Reptiles del noroeste, nordeste y este de are been studied at this time that hopefully will bring la Argentina. Mus. reg. Sci. nat. Torino, Monogr. 14, new evidence for a better understanding of the 949 pp. phylogenetic relationships within this large clade of Cei, J. M. & Scolaro, J. A. (1996). A new species of Lio/aemus. Liolaemus of the archeforus group from the precordilleran valley of the Zeballos river, Santa Cruz ACKNOWLEDGEMENTS province, Argentina (Reptilia, Tropiduridae). Boll. I thank J. Wiens, S. Poe, R. Espinoza, R. Laurent, R. Mus. reg. Sci. nat. Torino 14, 389-401. Etheridge and H. Nufiezfor valuable comments on the Di Castri, F. (1968). Esquisse Ecologique du Chili. In: manuscript. I thank B. Hollingsworth for his advise on Biol. de 1 'Amerique Australe. Delamare Debouteville performing PAUP analysis. R. Laurent and E. Lavilla C.I. et E. Rapaport. eds. (FML), H. Nunez (MNHN), J. C. Ortiz (MZUC), J. Donoso-Barros, R. (1966). Reptiles de Chile. Ediciones Cadle and E. Williams (MCZ), C. Myers and D. Frost de la Universidad de Chile, 458 pp. (AMNH), E. Censky and J. Wiens (CMNH), R. Donoso-Barros, R. (I 973a). Catalogo herpetol6gico Etheridge and T. Reeder (SDSU), R. Heyer (USNM), chileno. Bo/. Mus. Nac. Hist. Nat. Chile 31, 49-124. G. Carrizo and J. Faivovich (MACN), R. Martori Donoso-Barros, R. (I 973b). Un nuevo saurio de Bolivia (UNRC), and J. Williams (MLP) forallowing the study (Lacertilla lguanide). Fae. Ciencias Nat. Mus. La of materials under their care. I received much help Plata 19, 133-134. fromR. Espinoza, E. Teisaire, F. Cruz, G. Scrocchi, E. Donoso-Barros, R. & Cei, J. M. (1971). New lizard from LaviIIa, M. Halloy, R. Martori, L. Avila, M. Arnold, J. the volcanic patagonian plateau of Argentina. J. C. Moreta, S. Torres, C. Abdala, V. Abdala and R. Herpetol. 5, 89-95. Montero. This study was supported by CONICET Espinoza, N. D. & Formas, J. R. (1976). Karyological (Consejo Nacional de Investigaciones Cientificas y pattern of two Chilean lizard species of the genus Tecnologicas) and a grant of the Agencia Nacional de Liolaemus (Sauria: Iguanidae). Experientia 32, 299- Promoci6n Cientifica y Tecnica (PICT98 N° O 1- 301. 04637). Visits to some US museums were supported by Etheridge, R. ( 1995). Redescription of Ctenoblepharys an ErnstMayr Grant (MCZ), a Collection Study Grant adspersa Tschudi, 1845, and the taxonomy of (AMNH), and a Collection Study Grant in Herpetology Liolaeminae (Reptilia: Squamata: Tropiduridae). (CMNH). Visits to the Buenos Aires, Santiago and Amer. Mus. Nat. Hist. Novitates 3142, 1-34. Concepci6n museums (MNHNC and MZUC, respec­ Etheridge, R. and R. E. Espinoza. A semi-annotated tively) were made possible by R. Laurent's CONICET bibliography and taxonomy of the Liolaeminae program (PIP-CONICET), and E. Teisaire's UNT (Squamata: Iguania: Tropiduridae). Smithsonian project (CIUNT). Fundaci6n Miguel Lillo and Herpetological Information Service (in review). d CRILAR (CONICET) provided lab facilities and ac­ Farris, J. S. ( 1989). The retention in ex and the rescaled cess to their extensive collections. consistency index. C/adistics 5, 417-419. PHYLOGENY OF LIOLAEMUS 145

Felsenstein, J. (1985). Confidence limits on phylogenies: an Leyton C., V., Miranda A., E., & Bustos Obreg6n, E. approach using the bootstrap. Evolution 39, 783-791. ( 1980). Gestational chronology in the viviparous Frost, D. R. (1992). Phylogenetic analysis and taxonomy lizard Liolaemus gravenhorsti (Gray) with remarks on of the Tropidurus group of lizards (lguania: ovarian and reproductive activity. Arch. Biol. Tropiduridae). Amer. Mus. Nat. Hist. Novitates 3033, (Bruxelles) 91, 34 7-361. 1-68. Leyton, V., Veloso, A. & Bustos Obreg6n, E. (1982). Girard, C. ( 1858). Descriptions of some new reptiles Modalidad reproductiva y actividad ciclica gonadal en collected by the United States exploring expedition, lagartos iguanidos de distintos pisos altitudinales de! under the command of Capt. Charles Wilkes, U.S.N. interior de Arica (Lat. 18-10' S), 293-301. In: Veloso, Fourth Part. Including the species of saurians exotic to A. & Bustos Obreg6n, E. (Eds.). El Ho mbre y /as North America. Proc. Acad. Nat. Sci., Philadelphia 9, Ecosistemas de Montana I: La Ve getaci6n y . /as 195-199. Vertebrados Ectotermicos de/ Transecto Arica-Lago Hellmich, W. (1934). Die Eidechsen Chiles, insbesondere Chungara. Volumen de Sintesis, Proyecto MAB-6 die Gattung Liolaemus. Nach den Sammlungen Unep/Unesco 1105-77-01. Montevideo, Uruguay, 327 Goetsch-Hellmich. Abh. Bayer. Ak. Wiss. 24, 1-140. pp. Hellmich, W. ( 1951). On ecotypic and autotypic Lobo, F. & Espinoza, R. E. ( 1999). Two new cryptic characters, a contribution to the knowledge of the species of Liolaemus (lguania: Tropiduridae) from evolution of the genus Liolaemus (Iguanidae). Northwestern Argentina: resolution of the purported Evolution 5, 359-369. reproductive bimodality of Liolaemus alticolor. Hellmich, W. ( 1952). Contribuci6n al conocimiento de la Copeia 1999, 122-140. sistematica y evoluci6n de! genero Liolaemus. Invest. Morrone, J. J. ( 1996). The biogeographical Andean Zoo/. Chi/. 1, 7-15. subregions: a proposal exemplified by arthropod taxa lturra, P., Veloso, A., Espejo, P., & Navarro, J. (1994). (Arachnida, Crustacea, and Hexapoda). Neotropica Karyotypic and meiotic evidence for a robertsonian 42, 107-108. chromosome polymorphism in the lizard Liolaemus Navarro Baron, J. (1992). Cariotipos de trece especies de fu scus (Tropiduridae, Sauria). Rev. Brasil. Genet. 17, lagartijas de! noroeste argentino de los grupos 171-174. Liolaemus, Eulaemus y Ortholaemus. Acta zoo/. Lamborot, M. ( 1991 ). Karyotypic variation among Lilloana 41, 225-230. populations of Liolaemus monticola (Tropiduridae) Navarro, J. & Nui'iez,H. ( 1992). Acerca de la ausencia de separated by riverine barriers in the Andean Range. poros precloacales en Liolaemus cristiani nominaci6n Copeia 1991, 1044-1059. del alotipo y cariotipo de la especie. Not. Me ns. Mus. Lamborot, M. & Alvarez-Sarret, E. ( 1989). Karyotypic Nac. Hist. Nat. Chile 323, 35-38. characterization of some Liolaemus lizards in Chile Navarro, J. & Nui'iez, H. (1993). Liolaemus (Iguanidae). Genome 32, 393-403. patriciaiturrae y Liolaemus isabelae, dos nuevas Lamborot, M., Espinoza, A. & Alvarez, E. E. (1979). especies de lagartijas para el norte de chile. Aspectos Karyotypic variation in Chilean lizards of the genus biogeograficos y citotaxon6micos (Squamata, Liolaemus (Iguanidae). Experientia 35, 593-594. Tropiduridae). Bal. Mus. Nac. Hist. Nat. Chile 44, 99- Lamborot, M., Alvarez, E., Campos, I. & Espinoza, A. 113. ( 1981 ). Karyotypic characterization of three Chilean Navarro, J., Sallaberry, M., Veloso, A. & Valencia, J. subspecies of Liolaemus monticola. J. Heredity 72, ( 1981 ). Diversidad cromos6mica en lagartos 328-334. (Squamata-Sauria). I. Avances citotaxon6micos. Laurent, R. F. (1983a). Contribuci6n al conocimiento de Perspectivas de estudios evolutivos en Iguanidae. la estructura taxon6mica de! genero Liolaemus Me dia Ambiente 5, 23-38. Wiegmann (Iguanidae). Bal. Asoc. Herpetol. Arg. 1, Navarro, J., Veloso, A., Valencia, J. & Sallaberry, M. 16-18. (1979). Diversidad de los cariotipos de las lagartijas Laurent, R. F. (1983b). Sinonimia del genero Pelusaurus de! genero Liolaemus (lguanidae) de la zona central de Donoso-Barros con Liolaemus (Sauria, lguanidae). Chile. Arch. Biol. Me d. Exper. 12, 222. Bal. Asoc. Herpetol. Arg. 1, 9-10. Nunez, H. & Yai'iez, J. (1984). Abas y Ve losaura nuevos Laurent, R. F. (1984). On some iguanid genera related to generos de lagartos Iguanidae y proposiciones or previously confused with Liolaemus Wiegmann. J. sistematicas respecto de los generos aliados (Reptilia: Herpetol. 18, 357-373. Squamata). Bal. Mus. Nac. Hist. Nat. Chile 40, 97-105. Laurent, R. F. ( 1985). Segunda contribuci6n al Nui'iez, H. & Jaksic, F. ( 1992). Lista comentada de los conocimiento de la estructura taxon6mica del genero reptiles terrestres de Chile continental. Bal. Mus. Nac. Liolaemus Wiegmann (Iguanidae). Cuadernos de Hist. Nat. Chile 43, 63-91. Herpetologia 1, 1-37. Ortiz, J. C. ( 1981). Revision taxonomique et biologique Laurent, R. F. (1992). On some overlooked species of the des Liolaemus du groupe nigromaculatus (Squamata, genus Liolaemus Wiegmann (Reptilia Tropidurinae) Iguanidae). These Doct. d'Etat Sci. Nat. Univ. Paris fromPeru. Breviora 494, 1-33. VII, 438 pp. 146 F. LOBO

Ortiz, J. C. (1989a). Catalogue des types du Musee APPENDIX I d'Histoire Naturelle de Neuchatel. III. Sauriens. Extrait du Bulletin de la Societe Neuchateloise des LIST OF CHARACTERS Sciences Naturelles 112, 47-64. Sq uamation. A total of 24 characters were scored: Ortiz, J. C. (1989b). Descripci6n de Liolaemus si/:;1ai sp. I. Nasal-rostral contact (Fig. 3): (0) absent; (1) present. nov. (Sauria, Iguanidae) du "Norte Chico" du Chili. FREQ. BINS. Bull. Mus. Natn. Hist. Nat. Paris, 4e ser., 11, sec. A, 1, 2. Width of the nasal at the mid-point of the external 247-252. nares I width of the scale in contact with the rostral Quatrini, R., Bunge, M. M. & Albino A. (1997). Cariotipo (Fig. 3 ): ranging from a mean of 18.2 to 1.6. GAP de Liolaemus elongatus (Sauria: Tropiduridae) del WEIGHTING METHOD. noroeste patag6nico. Resumenes de/ Ill Congreso 3. Number of scales between canthal and nasal (Fig. 4): Argentina de Herpetologia. Pp. 75. (0) two scales; (!) one scale. FREQ. BINS. Ramirez Pinilla, M. P. ( 1991) . Estudio histol6gico de los 4. Dorsal head scales (rostral to occiput): ranging from tractos reproductivos y actividad ciclica anual a mean 16.0 to 10.5. GAP WEIGHTING METHOD. reproductiva de machos y hem bras de dos especies del 5. Neck scales (along the longitudinal fold where genero Liolaemus (Reptilia: Sauria: Iguanidae). Tesis present, or mid-distance between auditory meatus Doctoral, Universidad Nacional de Tucuman, and shoulder): (0) granular, hemispherical; (19) Argentina. laminar (flattened). FREQ. BINS. Roig Junent, S. ( 1994). Historia biogeografica de 6. Neck scales II: (0) smooth; (2) keeled. FREQ. BINS. America de! Sur Austral. Multequina 3, 167-203. 7. Dorsal head surface: (0) smooth; (!) rugose. FREQ. Sallaberry, M., Nunez, H. & Yanez, J. (1982). Liolaemus BINS. hernani n. sp. de Iguanidae de la Zona Central de 8. Temporal surface: (0) smooth; (!) keeled. FREQ. Chile. Bo/. Mus. Nac. Hist. Nat. Chile, Santiago 39, BINS. 93-99. 9. No. of temporals in a vertical count (counted at the Swofford, D. L. (1999). PAUP*: Phylogenetic Analysis mid-distance between subocular and auditory Using Parsimony*, Version 4.0b2 for 32-bit Microsoft meatus from the oral commisure upwardly to the Windows. Sinauer Associates, Sunderland, level of supraciliars): means ranging from 12.0 to Massachusetts, USA. 5.5. GAP WEIGHTING METHOD. Thiele, K. ( 1993 ). The biological grail of the perfect JO. Number of scales in contact with the interparietal: character: the cladistic treatment of morphometric (0) 8 scales; (I) 7 scales; (2) 6 scales; (3) 5 scales. data. Cladistics 9, 275-304. MAJORITY RULE. Valencia, J., Veloso, A. & Sallaberry, M. (1975). Analisis 11. Number of enlarged supraoculars: (0) 6 scales; (I) biometrico y cromos6mico en poblaciones de 5 scales; (2) 4 scales; (3) 3 scales. MAJORITY Liolaemus nigroviridis MUiler y Hellmich (Squamata, RULE. Iguanidae). Arch. Biol. Me d. Exper. 12, 209-220. 12. Posterior circumorbital scales: (0) forming a com­ Veloso, A. & Navarro, J. (1988). Lista sistematica y plete row of scales; (I) formingan interrupted row of distribuci6n geografica de anfibios y reptiles de Chile. scales. FREQ. BINS. Boll. Mus. reg. Sci. nat. Torino 6, 48 1-539. 13. Contact between 4th supralabial and subocular (Fig. Veloso, A., Sallaberry, M., Navarro, J., Iturra, P., 5): (0) no contact; (I) contact. FREQ. BINS. Valencia, J., Penna, M. & Diaz, N. (1982). 14. Number of Iorilabials: means ranging from 9 to 5. Contribuci6n sistematica al conocimiento de la GAP WEIGHTING METHOD. herpetofaunade! extremo norte de Chile, 135-268. In: 15. Height of supralabials: (0) wide and short with the "El hombre y los ecosistemas de montafza" . Off. Reg. fourth scale not differentiated; (I) slender with the Cien. Tee. Unesco para Amer. Lat. Carib. Montevideo. fourthusually showing its posterior tip encurved up­ Videla, F. & Cei, J. M. (1996). A new peculiar Liolaemus wardly. This character is the synapomorphy of species of the "chiliensis" phyletic group from the Etheridge's (1995) nitidus group. BINARY NOT volcanic cordilleran landscapes of southern Mendoza POLYMORPHIC. province, Argentina (Iguania, Lacertilia, Reptilia). 16. Auricular scale (Fig. 6): (0) not differentiated; (I) Boll. Mus. reg. Sci. nat. Torino 14, 505-516. differentiated. FREQ. BINS. Werner, F. (1907). Estudios sobre reptiles chilenos. 17. Scales along the anterior border of the auditory Anales Univ. Chile 121, 147-155. meatus (Fig. 6): (0) no enlarged scales at the anterior Wiens, J.J. ( 1993). Phylogenetic systematics of the tree margin of the auditory meatus. ( 1) one or two small Urosaurus). Herpetologica 49, lizards (Genus 399- laminar to granular scales differentiated slightly pro­ 420. jecting on the anterior margin; (2) one enlar�ed Wiens, J. J. ( 1995). Polymorphic characters in laminar scale; (3) two to four enlarged lam mar Syst. Biol. 44, phylogenetic systematics. 482-500. scales; (4) two to four enlarged lobulate scales. MULTISTATE NOT POLYMORPHIC. UNOR­ Accepted: 11.4.01 DERED. PHYLOGENY OF LIOLAEMUS 147

18. Separation of second chinshields (Fig. 7): (0) sec­ ond chinshields always separated one fromthe other by one or two scales; (I) second chinshields in con­ tact. In copiapensis and bisignatus more than 90% of individuals have these scales in contact. In other spe­ cies it is less common (silvai, platei, nigromaculatus, hellmichi, zapallarensis, sieversi). All the remaining species of the chiliensis group ex­ hibit the first condition. FREQ. BINS.

A canthal

A

anterior

B

FIG. 4. A, Liolaemus capillitas (FML 1229). Character 3, state 0: canthal separated from nasal by two scales. B, B Liolaemus bitaeniatus (FML 2918). Character 3, state I: canthal separated from nasal by one scale. Drawings made at nasal different scales.

19. Number of chinshields (Fig. 7): means ranging from 5.6 to 3.0. GAP WEIGHTING METHOD. 20. Shape of dorsal body scales: (0) with the posterior margin rounded; (I) rhomboidal; (2) lanceolate. � MAJORITY RULE 21. Keels of dorsal body scales: (0) not forming a pro­ jecting spine at the median posterior margin (mucrone); (I) forminga mucrone. BINARY NOT POLYMORPHIC. 22. Number ofmidbody scales (mean value): from 99.5 to 32. GAP WEIGHTING METHOD. 23. lnfradigital scales of fourthfinger (counted over the entire finger): means ranging from 24.4 to 15.4. GAP WEIGHTING METHOD.

Body patterns. A total of 18 characters were scored: 24. Subocular distinct from the general coloration of FIG. 3. A, Liolaemus pagaburoi (FML 2248). Character I, the head: (0) subocular not distinct; (I) subocular state I (nasal-rostral contact present); character 2 (broad white distinct. FREQ. BINS. contact between nasal and rostral scales). B, Liolaemus 25. Ventral melanism (belly plus abdomen): (0) im- ramirezae (FML 2940). Character I, state I (nasal-rostral maculate white. (1) spotted. (2) black. contact present); character 2 (slight contact between these scales). C, Liolaemus capillitas (FML 1229). Character I, MUL TISTA TE NOT POLYMORPHIC. state O (nasal-rostral contact absent). Drawings made at 26. Prescapular spot: (0) absent; (I) present. BINARY different scales. NOT POLYMORPHIC. 148 F. LOBO

anterior

A

subocular

D

anterior

B 4th supralabial

FIG. 5. A, Liolaemus pagaburoi (FML 2248). Character 13, state 0: fourth supralabial and subocular scales separated one from the other. B, Liolaemus n.sp. (FML 1761 ). Character 13, state I: fourthsupralabial and subocular scales in contact. Drawings made at different scales.

27. Postcapular spot: (0) absent; (1) present. BINARY FIG. 6. A, Liolaemus alticolor (AMNH 16904). Character NOT POLYMORPHIC. 16, state 0: auricular scale not differentiated; character 17, state 0: auditory meatus without enlarged scales on anterior 28. Paravertebral markings: (0) present; (1) absent. bordering. B, Liolaemus gravenhorsti (AMNH 80054). Paravertebral markings are those symmetrically po­ Character 16, state 0: auricular scale not differentiated; sitioned markings in the dorsal field of many character 17, state 3: auditory meatus with one enlarged members of the chiliensis group (see also Lobo and laminar scale. C, Liolaemusfuscus (AMNH 131833) and D, Espinoza, in review). Although these markings ex­ Liolaemus lemniscatus (AMNH 21145). Character 16, state I: auricular scale differentiated plus two other enlarged hibit variation in shape and number, at this point, I scales (character 17, state 2). Notice the elongated auricular only considered their presence. Paravertebral mark­ scale of lemniscatus reaching at least half the length of the ings can be shaped subquadrate (for example auditive meatus height. E, Liolaemus zapallarensis (AMNH /emniscatus, walkeri, etc.), slender transversal 37574). Character 16, state I: auricular present plus three stripes (as in a/tissimus), subtriangular (pictus enlarged lobed scales (character 17, state 4) which in this case, sometimes almost completely enclose the meatus. group), etc. FREQ. BINS. Drawings made at different scales. 29. Throat in males: (0) spotted; (1) immaculate. BI­ NARY NOT POLYMORPHIC. the head. Cei (1993) used the name "bandas 30. Throat II (females): (0) spotted; (1) immaculate. BI­ dorsolaterales." Lobo & Espinoza (1999) provide a NARY NOT POLYMORPHIC. figure and detailed descriptions of dorsal patterns 31. Vertebral stripe: (0) present (in some individuals and their variation among species of the altico/or fragmented); (1) absent. "Vertebrallinie" of group. BINARY NOT POLYMORPHIC. Hellmich (1934). FREQ. BINS. 33. Dorsolateral stripes II: (0) uniformlyslender exhib­ 32. Dorsolateral stripes: (0) absent; (1) present; (2) iting the same width all along their extension. (1) present only in females. Thesestripes were termed Slender over the neck and shoulders and becoming "parietalband" by Hellmich (1934; Abb. 2). wider posteriorly. BINARY NOT POLYMORPHIC. Donoso-Barros (1966) referred to them as "bandas 34. Subtriangular paravertebral markings in zigzag pat­ supraoculares" because they initiate fromthis area of tern: (0) absent; (1) present. This pattern is distinct PHYLOGENY OF LIOLA EMUS 149

40. Melanism on flanks: (0) absent; (I) present as a variegated pattern of large, fused spots; (2) uni­ formly black. State I is typical (with some variation) in monticola subspecies. State 2 is exhibited by cristiani and maldonadae. MUL TISTA TE NOT POLYMORPHIC. 41. Metallic or irridescent scales on the belly or flanks: (0) B absent; (I) present. Distinct in chi/ iensis, and A present, but less evident in fitzgeraldi, gravenhorsti FIG. 7. A, Liolaemus donosoi (FML 1340). Character 18, and robertmertensi. BINARY NOT POL YMOR­ state 0: second chinshields separated one from the other by PHIC. two scales; character 19 (number of chinshields). B, Liolaemus hellmichi (FML 1339). Character 18, state I: second chinshields in contact; character 19 (number of Colours. Two characters were scored: chinshields). Drawings made at different scales. 42. Pregnancy colour restricted to cloaca) and adjacent areas: (0) absent; (I) present. This colour is bright in members of the pictus group, having subtriangular red, strongly marked on the cloaca) region, proximal markings at each side of the vertebral band or field part of ventral surfaces of thighs and posterior ex­ (vertebral line is absent in these taxa), alternately treme of the abdomen. BINARY NOT positioned on either side. Liolaemus fitzgeraldi has POLYMORPHIC. similar pattern, but almost no vertebral band, and 43. Sexual dichromatism showing a dense pattern of these markings (left and right sides) are in contact ligth blue to green or turquoise scales scattered on with the vertebral line; this was not considered ho­ flanks and dorsum of males: (0) absent; (I) present. mologous in this analysis. BINARY NOT BINARY NOT POLYMORPHIC. POLYMORPHIC. 35. Paravertebral markings transversely elongated: (0) Neck-folds . Two characters were scored: absent; present. This pattern, very often, is more (I) 44. Lateral neck-folding (rictal, postauricular and lon­ evident in femalesthan males. gitudinal): (0) absent; (I) poorly developed 36. Occellations over the dorsum: (0) absent; (1) (foldings slightly projecting over the lateral wall of present. These markings are big and black and re­ the neck); (2) well developed (foldingsstrongly pro­ semble the skin pattern of a leopard. This pattern is jected over the lateral wall of the neck). The folds present in the three forms ofthe group leopardinus identified in this case are equivalent to those de­ with varying degrees of distinctness. BINARY NOT scribed by Frost ( 1992). Rictal, postauricular and POLYMORPHIC. longitudinal foldsappears always to exhibit the same 37. Irregularly fine "spotted" pattern on dorsum in degree of development. The antegular fold appears males: (0) absent; (I) present. BINARY NOT to change independently of the others. POLYMORPHIC. MULTISTATE NOT POLYMORPHIC. 38. Same pattern in females:(0) absent; (1) present. BI­ 45. Antegular fold: (0)present as a deep pocket; (1) not NARY NOT POLYMORPHIC. forming a pocket (evident because of diffe rences in 39. Dorsal pattern formed by scattered longitudinal the size of the scales); (2) absent (no pocket and all dark markings, like very short segments irregularly scales between ear and shoulder identical). located: (0) absent; (I) present. Originally this char­ MULTISTA TE NOT POLYMORPHIC. acter was drawn by Cei (1986, Fig. 50) for exploratorum, bibroni, sarljuanensis. Fat pouches. Only one character scored: 46. Fat pouches prominent on the sides of the neck: (0) present; (1) absent. BINARY NOT POL YMOR­ PHIC.

Precloacals pores. Two characters were scored: 47. Number of precloacal pores in males: means rang­ 8 c ing from 8.0 to 0.0. GAP WEIGHTING METHOD. 48. Precloacal pores in females: means ranging from 4.0 to 0.0 GAP WEIGHTING METHOD. FIG. 8. A Lio/aemus kriegi (REE 2412). Character 53, state Liolaemus O: maxill�ry teeth crowns expanded, tricuspid. B, . bibroni (REE 2305). Character 53, state l: max11l�ry teeth Hemipenis. Only one character scored: crowns slender, untapering, cusps reduced. C, Lzola�mus 49. Hemipenis ornamentation: (0) with calices re­ copiapensis (REE 2560). Characte� 53, state 2: maxillary stricted to the base of apical lobes, up to the level of teeth with crowns broad and untapermg, almost round, cusps the sulcus spermaticus bifurcation; (1) calices ex­ slightly differentiated or absent. Drawings made at different scales. tended below that level. 150 F. LOBO

en from Lamborot, Alvarez, Campos & Espinoza Size and ratios. Three characters were scored: (1981). Data for karyotypes were taken from Valen­ 50. Snout-vent length (taken from adult specimens cia, Veloso & Sallaberry (1975); Espinoza & Formas only): means from 92.0 to 41.5 mm. GAP WEIGHT­ (1976); Lamborot, Espinoza & Alvarez (1979); Na­ ING METHOD. varro, Veloso, Valencia & Sallaberry ( 1979); 51. Tail length I Snout-vent length ratio (tail length Lamborot et al. (1981 ), Navarro, Sallaberry, Veloso measured on apparently non-regenerated tails): & Valencia (1981); Sallaberry, Nunez & Yanez ranging from means of 1.0 to 2.1. GAP WEIGHT­ (1982); Veloso, Sallaberry, Navarro, Iturra, Valen­ ING METHOD. cia, Penna & Diaz (1982); Lamborot & 52. Subocular length I eye diameter (eye diametertaken Alvarez-Sarret (1989); Lamborot (1991); Navarro & between both angles formed by upper and lower Nunez (1992, 1993); Navarro (1992); Iturra, Veloso, ciliar scales): ranging frommeans of 1.1 to 1.7. GAP Espejo & Navarro ( 1994); Quatrini, Bunge & Albino WEIGHTING METHOD. (1997); Aiassa, Garia, Avila & Martori ( 1998). MUL TISTA TE NOT POLYMORPHIC. Te eth and lower jaw. Three characters were scored: 53. Maxillary teeth crowns (Fig. 8): (0) expanded and Biology and ecology. A total of five characters were tricuspid; (I) slender, untapering, anterior and poste­ scored: rior cusps reduced; (2) broad and untapering, crown 57. Maximum number ofyolked-follicles: (0) 4; (I) 5; almost round, cusps slightly differentiated or absent. (2) 6; (3) 7; (4) 8; (5) 9; (6) 10; (7) 11; (8) 12; (9) 13; Only mid-maxillary teeth were considered in this (10) 14; (1 1) 15. Data were taken from Ortiz (1981), analysis. MULTISTA TE NOT POLYMORPHIC. Leyton, Miranda & Bustos Obregon (1980), Leyton, UNORDERED. Veloso & Bustos Obregon (1982) and Ramirez 54. Heterodonty (cusped posterior maxillary teeth be­ Pinilla (1991). No raw data available to analyzing coming uncusped anteriorly): (0) absent (all using the Gap Weighting Method. MUL TIST A TE maxillary teeth have the same cusp morphology); (I) NOT POLYMORPHIC. present (anterior maxillary teeth become uncusped 58. Reproductive mode: (0) viviparous; (I) oviparous. and subconically shaped). BINARY NOT POLY­ Robert Espinoza pers. obs. BINARY NOT POLY­ MORPHIC. MORPHIC. 55. Meckel's groove: (0) open; (I) enclosed. The sec­ 59. Life style I: (0) saxicolous; (I) terrestrial; (2) ond condition is the synapomorphy uniting the psamophilous. Robert Espinoza pers. abs. MULTI­ chiliensis group (Etheridge, 1995). BINARY NOT STA TE NOT POLYMORPHIC. UNORDERED. POLYMORPHIC. 60. Life style II: (0) not arboreal; (!) terrestrial with ar­ boreal tendencies; (2) arboreal. Those scored 1 were Karyotype. Only one character was scored: coded terrestrial (I) for character 52. 56. Number ofmacrochromosomes: (0) 12 macrochro­ MUL TISTATE NOT POLYMORPHIC. mosomes; (!) 14 macrochromosomes; (2) 15 61. Diet: (0) insectivorous; (I) omnivorous; (2) her- macrochromosomes; (3) 16 macrochromosomes; (4) bivorous. Robert Espinoza pers. abs. 18 macrochromosomes; (5) 20 macrochromosomes; MUL TISTATE NOT POLYMORPHIC. (6) 22 macrochromosomes; (7) 24 macrochromo­ Data matrix and information on specimens studied is somes. Liolaemus monticola was scored available at: http://www.unsa.edu/ar/acunsa/ polymorphic (14/15/16 at its type locality) data tak- index02.html