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Evolution of Galapagos Island Lava Lizards (Iguania: Tropiduridae: Microlophus)

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Evolution of Galapagos Island Lava Lizards (Iguania: Tropiduridae: Microlophus) MOLECULAR PHYLOGENETICS AND EVOLUTION Molecular Phylogenetics and Evolution 32 (2004) 761–769 www.elsevier.com/locate/ympev Evolution of Galapagos Island Lava Lizards (Iguania: Tropiduridae: Microlophus) David Kizirian,a,b,* Adrienne Trager,c Maureen A. Donnelly,b and John W. Wrightd a Department of Organismic Biology, Ecology and Evolution, University of California–Los Angeles, Los Angeles, CA 90095-1606, USA b Department of Biological Sciences, Florida International University, Miami, FL 33199, USA c Moorpark College, 7075 Campus Road, Moorpark, CA 93021, USA d Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, CA 90007, USA Received 18 June 2003; revised 24 March 2004 Available online 2 June 2004 Abstract Nucleotide sequences of mitochondrial genes (ND1, ND2, COI, and tRNAs) were determined for 38 samples representing 15 taxa of tropidurid lizards from the Galapagos Islands and mainland South America. Phylogenetically informative characters (759 of 1956) were analyzed under Bayesian, maximum likelihood, and parsimony frameworks. This study supports the hypothesis that tropidurid lizards dispersed to the Galapagos on at least two separate occasions. One dispersal event involved an eastern Galapagos clade (Microlophus habelii and M. bivittatus, on Marchena and San Cristobal islands, respectively) the sister taxon of which is M. occipitalis from coastal Ecuador and Peru; the closest mainland relative of the western Galapagos clade was not unambiguously identified. The wide-ranging M. albemarlensis is revealed to be a complex of weakly divergent lineages that is paraphyletic with respect to the insular species M. duncanensis, M. grayii, and M. pacificus. Ó 2004 Elsevier Inc. All rights reserved. Keywords: Biogeography; Galapagos; Microlophus; Phylogeography; Tropiduridae; Tropidurus 1. Introduction named and unnamed lineages but has not been widely accepted. Central to the disagreement about Lava Liz- Despite more than a century of intensive study there ard diversity is the status of the populations of M. al- are still many unanswered questions regarding the evo- bemarlensis, which occur on four major and at least six lutionary history of organisms inhabiting the Galapagos satellite islands. In addition to addressing species di- Islands (e.g., Grehan, 2001). A fundamental issue ad- versity we also address the biogeographic history of dressed herein is the number of species of the conspic- Lava Lizards. Previous biogeographic hypotheses in- uous and abundant Lava Lizards (Microlophus; auct. ferred from the electrophoretic migration rates of allo- Tropidurus) occurring on the islands. Based on an zymes (Wright, 1983, 1984) and micro-complement analysis of morphological variation, Van Denburgh and fixation of albumins (Lopez et al., 1992) indicated that Slevin (1913) recognized seven species of Lava Lizards at least two independent dispersal events from the in the archipelago, an arrangement that has been fol- mainland to the archipelago were required to explain lowed by most (e.g., Lopez et al., 1992; Wright, 1983). Lava Lizards diversity. Herein, we revisit hypotheses An alternative arrangement (Lanza, 1974, 1980; Talurri about the diversity and biogeography of Galapagoan et al., 1982) based on geographic distribution and be- Microlophus in light of nucleotide sequence data ana- havioral data (Carpenter, 1966, 1970) recognized 17 lyzed in a phylogenetic context and broader taxonomic sampling than previous studies. At the same time, we evaluate hypotheses of monophyly for the M. occipitalis * Corresponding author. and M. peruvianus groups (Dixon and Wright, 1975) and E-mail address: [email protected] (D. Kizirian). the genus Microlophus (Frost et al., 2001; Harvey and 1055-7903/$ - see front matter Ó 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2004.04.004 762 D. Kizirian et al. / Molecular Phylogenetics and Evolution 32 (2004) 761–769 Gutberlet, 2000). Lastly, we employ the principles of NADH 1 and CO1, and the intervening tRNAs were phylogenetic classification (de Queiroz and Gauthier, amplified using the primers in Macey et al. (1997a,b) and 1990) to represent nested diversity at the species level. Jackman et al. (1999) as well as [50] taarataagtcattttggg [30], which was designed for use with some light strand primers from those studies. 2. Materials and methods Some fragments were amplified using a capillary thermal-cycler (Rapidcycler) and DNA amplification 2.1. Taxon sampling and data kits available from Idaho Technology (Salt Lake City, Utah). PCR cocktails comprised water (25 ll), 10 X Exemplars for this study include some of the tissue buffer (20, 30, or 40 mM MgCl2, 5.0 ll), dNTPs (2 mM samples used by Wright (1983) and Lopez et al. (1992) each; 5.0 ll), bovine serum albumin (2.5 mg/ml; 5.0 ll), as well as additional samples of mainland species not light and heavy strand primers (10 mM; 2.5 ll each), Taq previously examined (Table 1). Genomic DNA was ex- polymerase (ProMega; 0.3 ll), and template DNA (0.7– tracted from frozen tissues (1–25 mg) using the DNEasy 1.0 ll). Reactions were subjected to an initial heating Tissue Kits (Qiagen-Operon Catalog # 69504, 69506). (15 s, 94 °C), then 40–42 cycles of denaturation (15 s, Nucleotide sequence data were collected using poly- 94 °C), annealing (15 s, 53 °C), and extension (35 s, merase chain reaction (PCR) and automated DNA se- 71 °C), and then a final extension (60 s, 71 °C). quencing technology. Approximately 2 kb of the Most fragments were amplified using a block ther- mitochondrial genome, including NADH 2, portions of mal-cycler (Perkin–Elmer 9700) and AmpliTaq Gold Table 1 Samples of Microlophus and Tropidurus used in this study Species Voucher # (Tissue #) Locality M. albemarlensis LACM 106273 (G302) Galapagos: Baltra M. albemarlensis LACM 106267 (G216) Galapagos: Bartolome M. albemarlensis LACM 106268 (G217) Galapagos: Bartolome M. albemarlensis LACM 106288 (G327) Galapagos: Daphne M. albemarlensis LACM 106282 (G321) Galapagos: Daphne M. albemarlensis LACM 106254 (G150B) Galapagos: Fernandina: Punta Espinosa M. albemarlensis LACM 106244 (G142) Galapagos: Fernandina: Punta Espinosa M. albemarlensis LACM 106193 (G170) Galapagos: Isabela: Black Cove M. albemarlensis LACM 106185 (G162) Galapagos: Isabela: Black Cove M. albemarlensis LACM 106205 (G280B) Galapagos: Isabela: Cartago Bay M. albemarlensis LACM 106217 (G341) Galapagos: Santiago: James Bay M. albemarlensis LACM 106207 (G232) Galapagos: Santiago: Sullivan Bay M. albemarlensis LACM 106206 (G231) Galapagos: Santiago: Sullivan Bay M. albemarlensis LACM 106181 (G290) Galapagos: Santa Cruz: Conway Bay M. albemarlensis LACM 106162 (G11) Galapagos: Santa Cruz: Academy Bay M. albemarlensis LACM 106168 (G17) Galapagos: Santa Cruz: Academy Bay M. bivitattus LACM 106298 (G43) Galapagos: San Cristobal: Wreck Bay M. bivitattus LACM 106303 (G49) Galapagos: San Cristobal: Wreck Bay M. delanonis LACM 106327 (G104) Galapagos: Espanola: Gardner Bay M. delanonis LACM 106314 (G92) Galapagos: Gardner: near Espanola M. delanonis LACM 106315 (G93) Galapagos: Gardner: near Espanola M. duncanensis LACM 106340 (G261) Galapagos: Duncan (Pinzon): east side M. grayii LACM 106363 (G132) Galapagos: Floreana: Black Beach M. habelii LACM 106384 (G205) Galapagos: Marchena: south side M. habelii LACM 106389 (G210) Galapagos: Marchena: south side M. koepckeorum LACM 122590 (P6-193) Peru: Lambayeque: Cerro de la Vieja: ca. 7 km S (by rd) Motupe M. occipitalis LACM 154351 (G4-78) Ecuador: Ancon at Basurera M. pacificus LACM 106398 (G192) Galapagos: Pinta: southwest side M. pacificus LACM 106399 (G193) Galapagos: Pinta: southwest side M. peruvianus LACM 122684 (P6-381) Peru: Lima: El Paraiso Peninsula: ca 6.2 km W (by rd) jct Pan Am Hwy M. peruvianus LACM 154394 (G4-91) Ecuador: Santa Elena Peninsula, Punto Carnero M. stolzmanni LACM 122648 (P6-290) Peru: Cajamarca: ca 13 km SSE (by rd) Hacienda Molino Viejo (Ochentiuno) M. stolzmanni LACM 122667 (P6-258) Peru: Cajamarca: Bellavista M. theresiae LACM 122695 (P6-389) Peru: Lima: El Paraiso Peninsula: ca 6.2 km W (by rd) jct Pan Am Hwy M. tigris LACM 122720 (P6-84) Peru: Lima: ca 3 km SE Asia Vieja T. etheridgei [at LACM] (TC-921) Bolivia: 0.5 km SW Parotania RR station T. hispidus [at LACM] (4-94) Venezuela: Isla Margarita T. hispidus [at LACM] (4-76) Venezuela: Playa Guiria D. Kizirian et al. / Molecular Phylogenetics and Evolution 32 (2004) 761–769 763 DNA polymerase (Perkin–Elmer) kits. PCR cocktails Decay indices (Bremer, 1988) were calculated using comprised water (17–35 ll), 10 X buffer (5.0 ll), MgCl2 TreeRot (version 2.0) with the number of heuristic (4.0–7.0 ll), dNTPs (5.0 ll), heavy and light strand searches increased to 1000 to increase accuracy of indi- primers (10 mM; 1.0 or 2.5 ll), Taq polymerase (0.3 ll), ces (Sorenson, 1999). Bootstrap statistics were calcu- and template DNA (0.7–1.0 ll). Reactions were sub- lated using PAUP* (fast-heuristic search, nreps ¼ 1002) jected to a variety of thermal-cycling profiles including and assumed model parameters calculated with Model an initial heating (1–5 min, 95 °C) then 32–43 cycles of test (i.e., GTR + I + C). denaturation (35 s, 94 °C), annealing (35–45 s, 48–58 °C), MrBayes (version 3.0; Huelsenbeck and Ronquist, extension (60 s; or 150 s plus 4 s added to each sub- 2001) was used to estimate posterior probabilities of sequent cycle; 70 °C, or 72 °C), and a final extension clades under a likelihood model. Substitution rates were (7 min, 72 °C). allowed to be different, subject to the constraints of time- To reduce the risk of contamination, all reagents, reversibility (GTR; n ¼ 6). Among-site rate variation was primer stocks, DNA extractions, and PCR cocktails drawn from a gamma distribution with some proportion were prepared in a facility that was physically isolated being invariant (rates ¼ invgamma). Model parameters from areas where post-PCR procedures were performed. for structural and protein-coding partitions were treated Kim Wipes were used to shield aerosol created when as unlinked [unlink revmat ¼ (all) shape ¼ (all) pinvar ¼ tubes were opened.
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