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Phylogenetic Relationships in the Iguanid Lizard Genus Liolaemus

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Phylogenetic Relationships in the Iguanid Lizard Genus Liolaemus Biological Journal of the Linnean Society (2000), 69: 75±102. With 7 ®gures doi: 10.1006/bijl.1999.0346, available online at http://www.idealibrary.com on Phylogenetic relationships in the iguanid lizard genus Liolaemus: multiple origins of viviparous reproduction and evidence for recurring Andean vicariance and dispersal JAMES A. SCHULTE II1∗, J. ROBERT MACEY1, ROBERT E. ESPINOZA2 AND ALLAN LARSON1 1Department of Biology, Box 1137, Washington University, St. Louis, MO, USA 63130±4899. 2Ecology, Evolution and Conservation Biology/MS314, University of Nevada, Reno, NV, USA 89557 Received 2 March 1998; accepted for publication 15 January 1999 Phylogenetic relationships within the iguanid lizard genus Liolaemus are investigated using 1710 aligned base positions (785 phylogenetically informative) of mitochondrial DNA sequences, representing coding regions for eight tRNAs, ND2, and portions of ND1 and COI. Sixty new sequences ranging in length from 1736 to 1754 bases are compared with four previously reported sequences. Liolaemus species form two well-supported monophyletic groups of subgeneric status, Liolaemus and Eulaemus. These subgenera appear to have separated at least 12.6 million years ago based on the amount of molecular evolutionary divergence between them. Hypotheses that species occurring in the Andes, west of the Andes, and east of the Andes, each comprise distinct monophyletic groups are independently rejected statistically. The shortest estimate of phylogeny suggests that Liolaemus originated either in the Andes or the eastern lowlands. Numerous evolutionary shifts have occurred between the Andes, and the eastern and western lowlands, suggesting recurring vicariance and dispersal. Species occurring at high elevations or high latitudes usually have viviparous reproduction. Depending on whether parity mode is considered reversible in Liolaemus, the most parsimonious reconstruction supports at least six independent origins of viviparity or at least three gains followed by three losses of viviparity among the 60 Liolaemus lineages examined. 2000 The Linnean Society of London ADDITIONAL KEYWORDS:ÐReptilia ± Squamata ± Iguania ± Iguanidae ± Liolaemus ± phylogeny ± reproduction ± historical biogeography ± viviparity ± South America ± Andes. CONTENTS Introduction ....................... 76 Methods ........................ 79 ∗ Corresponding author. E-mail: [email protected] 75 0024±4066/00/010075+28 $35.00/0 2000 The Linnean Society of London 76 J. A. SCHULTE ET AL. Specimen information .................. 79 Laboratory protocols .................. 80 Phylogenetic analysis .................. 80 Results ........................ 81 Authentic mitochondrial DNA ............... 81 Assessment of homology and sequence alignment ......... 82 Genic variation .................... 82 Phylogenetic analyses .................. 83 Evaluating Andean vicariance ............... 87 Evolution of viviparity .................. 88 Discussion ....................... 89 Historical biogeography ................. 89 Dating phylogenetic divergence and vicariance .......... 91 Evolution of parity mode ................. 93 Phylogenetic relationships and taxonomy ............ 93 Acknowledgements .................... 95 References ....................... 95 Appendix 1 ....................... 98 Appendix 2 ....................... 99 Appendix 3 ....................... 101 INTRODUCTION The iguanid lizard genus Liolaemus contains over 160 species distributed in the Andes and adjacent lowlands of South America from Peru to Tierra del Fuego (Cei, 1986, 1993; Donoso-Barros, 1966; Etheridge, 1995). This genus has one of the largest latitudinal, elevational, and climatic distributions among lizards world-wide, with species found from sea level to over 5000 m (Cei, 1986, 1993; Donoso-Barros, 1966). Physiographic factors divide the distribution of Liolaemus into three major regions: (1) Andean highlands, (2) lowlands east of the Andes, and (3) lowlands west of the Andes. We test the hypothesis that the uplift of the Andes divided the ancestral Liolaemus into monophyletic groups corresponding to one or more of the three physiographic regions (Fig. 1). Alternatively, continual uplifting of the Andes over the last 25 million years (Norabuena et al., 1998) may have caused recurring episodes of vicariance superimposed on periodic dispersal events between the Andes, and the eastern and western lowlands. The latter hypothesis predicts that none of the three regions should comprise monophyletic groupings of Liolaemus species. The highest elevation of the Andean mountain chain currently extends up to 7000 m and presents a formidable barrier to dispersal for Liolaemus; however, numerous potential dispersal corridors occur under 5000 m. Because approximately half of the Liolaemus species are live-bearing, the phylo- genetic pattern of reproductive mode presents an interesting issue for investigation. Viviparity, the retention within the uterus of a developing neonate until development is complete, appears to have evolved frequently among squamate reptiles in cool environments at high latitudes and elevations (Guillette, 1993; Shine, 1985; Shine & Bull, 1979; Tinkle & Gibbons, 1977). Recent molecular phylogenetic work on iguanid lizards of the Sceloporus scalaris complex has demonstrated that viviparity evolved twice within that species group and possibly reversed to oviparous re- production once (Benabib, Kjer & Sites, 1997; Creer et al., 1997; Mink & Sites, 1996). An evolutionary analysis of reproductive modes within Liolaemus may reveal whether viviparity has evolved multiple times and potentially could reverse (Lee & Shine, 1998). LIOLAEMUS PHYLOGENETICS 77 Eastern and Western Andean A High-elevation species form a clade Andean and Western Eastern B Eastern lowland species form a clade Andean and Eastern Western C Western lowland species form a clade Figure 1. Hypotheses for the historical biogeography of Liolaemus. A possible outcome of the initial uplifting of the Andes is the geographic fragmentation of Liolaemus populations into major subgroups located in (A) the Andes, (B) the eastern lowlands and/or (C) the western lowlands (Table 1). If Liolaemus populations in these three regions formed a genetically homogeneous entity prior to the Andean uplift, and populations in one or more regions remained isolated following the initial uplifting, one to three major clades of Liolaemus corresponding to any or all of the geographic regions may result. If phylogenetic structure was present in Liolaemus prior to the Andean uplift, or if episodes of vicariance and dispersal between these three regions followed the initial uplift, one or more of the three major areas would contain a phylogenetically heterogeneous grouping of species. A well supported estimate of phylogeny is used to test these hypotheses of historical biogeography and evolution of viviparity. Samples of approximately one-third of the recognized Liolaemus species, including representatives occurring in all physiographic provinces and exhibiting both reproductive modes, are examined. These species represent the major groups from the most recent taxonomy of Liolaemus (Etheridge, 1995; Table 1). Sixty new mitochondrial DNA sequences are reported for the same region sequenced for a broad sampling of iguanid lizard taxa by Macey et al. (1997b). This sequence extends from the end of the gene encoding ND1 (NADH dehydrogenase 1) to the beginning of the gene encoding COI (cytochrome c oxidase I) and includes all of the ND2 gene, eight tRNA genes, and the origin for light- strand replication (OL). This same region of DNA sequenced for Liolaemus pictus (Macey et al., 1997b) is included in this analysis. Outgroups are based on the phylogenetic hypothesis of Schulte et al. (1998). In 78 J. A. SCHULTE ET AL. T 1. Taxa included in this study, by region of largest distribution, range in elevation (meters above sea level), and parity mode (O=oviparous, and V=viviparous) primarily based on museum specimens, Cei (1986, 1993), and Donoso-Barros (1966). Key references for parity mode are given to the right. Andean taxa occur above 2500 meters, whereas eastern and western taxa occur exclusively from sea level to 2500 meters on either side of the Andes. Museum catalogue numbers and localities are given in Appendix 1. Subgeneric designations are after Laurent (1984) and correspond to the phylogenetic results of this study. Species sections and series for the subgenus Eulaemus are largely after Etheridge (1995), and are amended to correspond with results of this study. Taxa denoted with a cross are members of the L. wiegmannii group of Etheridge (1995) and here are called the `sand-lizard clade' of the L. boulengeri series Taxon Region Elevation Parity Reference range mode Outgroup taxa 1. Oplurus cuvieri ÐÐ O 2. Phrynosoma douglassii ÐÐ V 3. Phymaturus palluma Andean 2500±4000 V Donoso-Barros (1966) 4. P. somuncurensis Eastern 1200 V Cei (1986) Subgenus Liolaemus 5. Liolaemus coeruleus Eastern 1500±1700 O Espinoza, unpubl. data 6. L. alticolor Andean 3000±3600 O Espinoza, unpubl. data 7. L. bitaeniatus Andean 700±2800 O Cei (1993) 8. L. robertmertensi Andean 690±2600 O Cei (1993) 9. L. bibronii Andean 0±3000 O Cei (1986) 10. L. gracilis Eastern 0±1380 O Cei (1986) 11. L. bellii Andean 2000±3200 V RamõÂrez Pinilla (1991a) 12. L. chiliensis Western 0±2100 O Donoso-Barros (1966) 13. L. cyanogaster Western 0±225 V Donoso-Barros (1966) 14. L. pictus ± NeuqueÂn Eastern & 10±1600 V Cei (1986) Western 15. L. pictus ± Rio Negro Eastern
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