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Molecular Tests of Phylogenetic Taxonomies: a General Procedure and Example Using Four Subfamilies of the Lizard Family Iguanidae James A

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Molecular Tests of Phylogenetic Taxonomies: a General Procedure and Example Using Four Subfamilies of the Lizard Family Iguanidae James A MOLECULAR PHYLOGENETICS AND EVOLUTION Vol. 10, No. 3, December, pp. 367–376, 1998 ARTICLE NO. FY980541 Molecular Tests of Phylogenetic Taxonomies: A General Procedure and Example Using Four Subfamilies of the Lizard Family Iguanidae James A. Schulte II,*,1 J. Robert Macey,* Allan Larson,* and Theodore J. Papenfuss† *Department of Biology, Box 1137, Washington University, St. Louis, Missouri 63130; and †Museum of Vertebrate Zoology, University of California, Berkeley, California 94720 Received September 19, 1997; revised April 8, 1998 Molecular phylogenetic analyses often are used to A general procedure is described for examining when examine monophyly of taxonomic groupings con- results of molecular phylogenetic analyses warrant structed from morphological characters. There is no formal revision of taxonomies constructed using mor- general procedure, however, for judging what consti- phological characters. We illustrate this procedure tutes sufficient evidence for monophyly of a taxonomic with tests of monophyly for four subfamilies in the grouping and what taxonomic procedure should be lizard family Iguanidae using 1561 aligned base posi- followed when results are ambiguous. We suggest a tions (838 phylogenetically informative) of mitochon- general method for evaluating support for monophyly drial DNA sequences, representing coding regions for eight tRNAs, ND2, and portions of ND1 and COI. Ten of taxonomic groupings and illustrate this procedure new sequences ranging in length from 1732 to 1751 with phylogenetic analyses of the iguanid lizard sub- bases are compared with 12 previously reported se- families Crotaphytinae, Iguaninae, Phrynosomatinae, quences and 67 morphological characters (54 phyloge- and Tropidurinae. This method uses statistical tests to netically informative) from the literature. New morpho- ask whether the molecular and morphological data logical character states are provided for Sator. analyzed separately and in combination can reject Phylogenies derived from the molecular and combined alternative hypotheses of either nonmonophyly or mono- data are in agreement but both conflict with phyloge- phyly for the taxa in question and whether these data netic inferences from the morphological data alone. partitions contain significant conflicts (Larson, 1994). Strong support is found for the monophyly of the Taxonomic groupings whose monophyly receives sup- subfamilies Crotaphytinae and Phrynosomatinae. port from analyses of the relevant data deserve formal Monophyly of the Iguaninae is weakly supported in taxonomic recognition. Taxonomic groupings for which each analysis. All analyses suggest that the Tropiduri- monophyly is not found but not statistically rejected nae is not monophyletic but the hypothesis of mono- can be recognized as metataxa (Estes et al., 1988; phyly cannot be rejected. A phylogenetic taxonomy is Gauthier et al., 1988) pending more definitive phyloge- proposed in which the Tropidurinae* is maintained as netic results. a metataxon (denoted with an asterisk), for which monophyly has not been demonstrated. Within the Phylogenetic relationships of iguanid lizards have Phrynosomatinae, the close relationship of Sator and been highly controversial. Frost and Etheridge (1989) Sceloporus is questioned and an alternative hypoth- divided the Iguanidae into eight new families corre- esis in which Sator is the sister taxon to a clade sponding to the eight monophyletic groups of Etheridge comprising Petrosaurus, Sceloporus, and Urosaurus is and de Queiroz (1988) because their analysis of morpho- presented. Statistical tests of monophyly provide a logical data could neither confirm nor reject monophyly powerful way to evaluate support for taxonomic group- of the Iguanidae (sensu lato). This taxonomy has been a ings. Use of the metataxon prevents premature taxo- topic of extensive controversy (for a review, see Schwenk, nomic rearrangements where support is lacking. ௠ 1998 1994). Recently, Macey et al. (1997c) presented data Academic Press supporting monophyly of the Iguanidae (sensu lato) Key Words: Reptilia; Squamata; Iguania; Iguanidae; and suggested a taxonomy recognizing the eight fami- Crotaphytinae; Iguaninae; Phrynosomatinae; Tropi- lies of Frost and Etheridge (1989) as subfamilies. durinae; Sator; mitochondrial DNA; phylogenetics; tax- However, monophyly of the eight iguanid subfamilies onomy; monophyly tests; metataxon. has never been tested rigorously. The eight iguanid subfamilies as proposed by Macey et al. (1997c) are the Corytophaninae, Crotaphytinae, 1 To whom correspondence should be addressed. Fax: (314) 935- Hoplocercinae, Iguaninae, Oplurinae, Phrynosomati- 4432. E-mail [email protected]. nae, Polychrinae, and Tropidurinae. Recently, molecu- 367 1055-7903/98 $25.00 Copyright ௠ 1998 by Academic Press All rights of reproduction in any form reserved. 368 SCHULTE ET AL. lar studies have investigated relationships within sev- Outgroups were selected from two separate lineages, eral iguanid subfamilies but have not adequately tested the Acrodonta, which is the sister taxon to the Iguani- monophyly of these subfamilies. The only subfamily dae (Macey et al., 1997c), and the Scleroglossa, which is that has been tested for monophyly using representa- the sister taxon to the Iguania (Estes et al., 1988; tives of all other subfamilies is the Crotaphytinae Macey et al., 1997a; Schwenk, 1988). Chamaeleo and (Crotaphytus and Gambelia; Macey et al., 1997c). Two Leiolepis were selected as representatives of the Acro- recent studies have addressed phylogenetic relation- donta, and Elgaria as a representative member of the ships of the Iguaninae but neither study included Scleroglossa using the previously published sequences representatives of more than three of the other iguanid of Macey et al. (1997c). subfamilies (Rassman, 1997; Sites et al., 1996). Molecu- lar phylogenetic studies within the Phrynosomatinae MATERIALS AND METHODS (Reeder, 1995; Reeder and Wiens, 1996) included repre- sentatives of four additional iguanid subfamilies as Specimen Information outgroups, but these taxa were used to construct a Museum numbers and localities for voucher speci- hypothetical ancestor based on the topologies identified mens from which DNA was obtained and GenBank in an analysis of morphological data by Frost and Accession Numbers are presented. Acronyms are MVZ Etheridge (1989). Macey et al. (1997c) showed that the for Museum of Vertebrate Zoology, University of Califor- morphological data of Frost and Etheridge (1989) have nia, Berkeley, and SDSU for San Diego State Univer- little phylogenetic information for resolving relation- sity, San Diego. The acronym followed by a dash RM ships between iguanid subfamilies. In an investigation represents the field number of the second author for an of the phylogenetic relationships of the Oplurinae, uncatalogued specimen being deposited in the Museum Titus and Frost (1996) included members of three other of Vertebrate Zoology. Iguaninae: Dipsosaurus dorsa- iguanid subfamilies as outgroups. While the Oplurinae lis, beach flats, Bahia de Los Angeles, Baja California was found to be monophyletic, the Tropidurinae was Norte, Mexico (MVZ 161172, AF049857). Phrynoso- not. Titus and Frost (1996) included members of two of matinae: Petrosaurus thalassinus, 32.2 miles north of the three groups of the Tropidurinae. The three groups Parador Punto Prieta, Mexico Highway 1, Baja Califor- of the Tropidurinae (sensu Macey et al., 1997c) were nia Norte, Mexico (MVZ 161010, AF049858); Sator recognized previously as subfamilies, the Liolaeminae, angustus, Baja California Sur, Mexico (MVZ 137666, Leiocephalinae, and Tropidurinae, by Frost and AF049859); Sceloporus graciosus, Mescalero Sands, Etheridge (1989). 37.5 miles east of Roswell on Highway 380, Chaves Here, hypotheses of monophyly are tested for four of County, New Mexico (MVZ 180319, AF049860); Uma the eight iguanid subfamilies, the Crotaphytinae, Igua- scoparia, 3.8 miles south of Parker on Highway 95, La ninae, Phrynosomatinae, and Tropidurinae. Ten new Paz County,Arizona (MVZ 182602, AF049861); Urosau- mitochondrial DNA sequences are reported for the rus graciosus, Kelso Dunes, approximately 4 miles same region sequenced by Macey et al. (1997c). This SSW of Kelso, San Bernardino County, California (MVZ- sequence extends from the end of the gene encoding RM3491, AF049862); Uta stansburiana, Mescalero ND1 to the beginning of the gene encoding COI and Sands, 37.5 miles east of Roswell on Highway 380, includes all of the ND2 and eight tRNA genes. Chaves County, New Mexico (MVZ 180323, AF049863). Mitochondrial DNA sequences for both genera of the Tropidurinae: Leiocephalus carinatus, Marsh Har- Crotaphytinae, Crotaphytus and Gambelia, were previ- bour, Abaco, Bahamas (no voucher, AF049864); Phyma- ously published by Macey et al. (1997c) and we further turus somuncurensis, Meseta Somuncura´, Dept. Rı´o test the monophyly of this subfamily with sequences Negro, Argentina (SDSU 1648, AF049865); Stenocercus from 10 additional iguanid genera. Within the Iguani- crasicaudatus, Machu Pichu Ruins, Dept. Cuzco, Peru nae, a basal taxon, Dipsosaurus, is compared with a (MVZ 199531, AF049866). representative member of the Iguanini (de Queiroz, The previously reported Liolaemus sequence (Macey 1987), Sauromalus, from Macey et al. (1997c). Mitochon- et al., 1997c) was misidentified as L. tenuis. The correct drial DNA sequences for all remaining major groups in information for this specimen is as follows: Liolaemus the Phrynosomatinae, Petrosaurus,
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