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Genus Xantusia (Squamata: Xantusiidae)

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Genus Xantusia (Squamata: Xantusiidae) Brigham Young University BYU ScholarsArchive Faculty Publications 2004-09-01 Testing Species Boundaries in an Ancient Species Complex with Deep Phylogeographic History: Genus Xantusia (Squamata: Xantusiidae) Keith A. Crandall Elizabeth A. Sinclair Robert L. Bezy Kathryn Bolles Jose L. Camarillo See next page for additional authors Follow this and additional works at: https://scholarsarchive.byu.edu/facpub Part of the Biology Commons BYU ScholarsArchive Citation Crandall, Keith A.; Sinclair, Elizabeth A.; Bezy, Robert L.; Bolles, Kathryn; Camarillo, Jose L.; and Sites, Jack W., "Testing Species Boundaries in an Ancient Species Complex with Deep Phylogeographic History: Genus Xantusia (Squamata: Xantusiidae)" (2004). Faculty Publications. 417. https://scholarsarchive.byu.edu/facpub/417 This Peer-Reviewed Article is brought to you for free and open access by BYU ScholarsArchive. It has been accepted for inclusion in Faculty Publications by an authorized administrator of BYU ScholarsArchive. For more information, please contact [email protected], [email protected]. Authors Keith A. Crandall, Elizabeth A. Sinclair, Robert L. Bezy, Kathryn Bolles, Jose L. Camarillo, and Jack W. Sites This peer-reviewed article is available at BYU ScholarsArchive: https://scholarsarchive.byu.edu/facpub/417 vol. 164, no. 3 the american naturalist september 2004 ൴ Testing Species Boundaries in an Ancient Species Complex with Deep Phylogeographic History: Genus Xantusia (Squamata: Xantusiidae) Elizabeth A. Sinclair,1,2,* Robert L. Bezy,3 Kathryn Bolles,3 Jose L. Camarillo R.,4 Keith A. Crandall,1,5 and Jack W. Sites, Jr.1,5 1. Department of Integrative Biology, Brigham Young University, vicariant events usually hypothesized for the fauna of the Baja Cal- Provo, Utah 84602; ifornia peninsula, and the existence of deeply divergent clades 2. Division of Science and Engineering, Murdoch University, (18.8%–26.9%) elsewhere in the complex indicates the occurrence Murdoch, Western Australia 6150, Australia; of ancient sundering events whose genetic signatures were not erased 3. Natural History Museum of Los Angeles County, Los Angeles, by the late Wisconsin vegetation changes. We present a revised tax- California 90007; onomic arrangement for this genus consistent with the distinct 4. Laboratrio y Coleccio´n de Herpetolgı´a, CyMA, Escuela Nacional mtDNA lineages and discuss the phylogeographic history of this de Estudios Profesionales Iztacala, A.P. 314, Tlalnepantla, Estado genus as a model system for studies of speciation in North American de Me´xico, Mexico; deserts. 5. Monte L. Bean Life Science Museum, Brigham Young University, Provo, Utah 84602 Keywords: species boundaries, phylogeography, mtDNA, maximum likelihood, Bayesian analysis, nested clade analysis, Xantusia. Submitted October 3, 2002; Accepted August 27, 2003; Electronically published July 30, 2004 Online enhancements: table, figure, appendixes. Morphologically conservative species complexes with deep phylogeographic structure are likely to pose particular problems when attempting to delimit species boundaries. Limited morphological variation may mask considerable evolutionary diversity in some groups (e.g., Highton 2000; abstract: Identification of species in natural populations has re- Wake and Jockusch 2000), yet reliance on the mtDNA cently received increased attention with a number of investigators proposing rigorous methods for species delimitation. Morphologi- locus alone may overresolve this diversity (Irwin 2002) or cally conservative species (or species complexes) with deep phylo- provide misleading results (e.g., Shaw 2002). Several new genetic histories (and limited gene flow) are likely to pose particular methods attempt to combine morphological and molec- problems when attempting to delimit species, yet this is crucial to ular data (Puorto et al. 2001; Wiens and Penkrot 2002) comparative studies of the geography of speciation. We apply two or to integrate these with ecological, physiological, or life- methods of species delimitation to an ancient group of lizards (genus history data (Templeton 1998, 2001) to delimit species. Xantusia) that occur throughout southwestern North America. Mi- Species are obviously fundamental to virtually all studies tochondrial cytochrome b and nicotinamide adenine dinucleotide dehydrogenase subunit 4 gene sequences were generated from sam- in evolutionary biology and biodiversity assessment, and ples taken throughout the geographic range of Xantusia. Maximum rigorous delimitation of their boundaries clearly impacts likelihood, Bayesian, and nested cladogram analyses were used to inferences made in all areas (Brown et al. 1996; Blackburn estimate relationships among haplotypes and to infer evolutionary and Gaston 1998; Peterson and Navarro-Sigu¨enza 1999). processes. We found multiple well-supported independent lineages Rigorous delimitation of species coupled with detailed dis- within Xantusia, for which there is considerable discordance with tributional data is also required for phylogenetic study of the currently recognized taxonomy. High levels of sequence diver- the geography of speciation (Losos and Glor 2003). gence (21.3%) suggest that the pattern in Xantusia may predate the Species biology lies at the interface between population genetics and systematics; relationships above the species * Corresponding author. Address for correspondence: Department of Inte- grative Biology, Brigham Young University, Provo, Utah 84602; e-mail level are of a hierarchical nature (and hence traditional [email protected]. phylogenetic methods can be used for tree reconstruction), Am. Nat. 2004. Vol. 164, pp. 396–414. ᭧ 2004 by The University of Chicago. while relationships below the species level are tokogenetic, 0003-0147/2004/16403-20370$15.00. All rights reserved. and nonhierarchical network-based approaches are more Phylogeography of Xantusia 397 appropriate (Davis 1996; Posada and Crandall 2001). Here, we take a molecular-based phylogenetic approach Given the nature of these relationships, we propose that to hypothesize species boundaries and biogeographic pat- a reasonable approach to identifying species boundaries terns in X. vigilis using partial DNA sequences from the might incorporate traditional phylogenetic methods to re- mitochondrial cytochrome b (cyt b) and nicotinamide ad- cover deep lineages and nonhierarchical methods to un- enine dinucleotide dehydrogenase subunit 4 (ND4) gene derstand shallower (unresolved) relationships within line- regions. Extensive sampling was conducted across the en- ages and to infer the processes responsible for their genetic tire range of the genus to delimit species boundaries based diversity. Here, we adopt the concept of species as inde- on the Wiens and Penkrot (2002) molecular approach and pendent evolutionary lineages (Mayden 1997; de Queiroz contrast the biogeographic pattern reflected in the Xan- 1998) and apply two recently developed methods to de- tusia phylogeny with those for other North American de- limit species boundaries. Wiens and Penkrot (2002) pro- sert vertebrates. We draw attention to general issues of pose an explicit (qualitative) protocol for delimiting spe- testing species boundaries in morphologically conserva- cies boundaries based on haplotype phylogenies integrated tive, low-vagility species and to geographic sampling and with the nonhierarchical network-based approach of Tem- limitations of the NCA. Because these limitations can now pleton et al. (1995; nested clade analysis [NCA]). The NCA be accommodated in future research designs, we suggest was recently extended explicitly to test species boundaries that Xantusia offers many attributes as a model system for within the context of the cohesion species concept (Tem- further study of the geography of speciation in south- pleton 1989, 2001). Both methods should provide the same western North America. result relating to the identification of independent lineages, but inferences from the NCA may also provide infor- mation about the processes leading to and following spe- Material and Methods ciation. We are aware of the limitations of the NCA (Know- Data Collection les and Maddison 2002; Petit and Grivet 2002; Masta et al. 2003) and return to some of these points in the We obtained mtDNA sequence data from a total of 122 discussion. individuals of Xantusia from 87 localities. All localities are The night lizards (genus Xantusia) provide an excellent summarized in table A1 and figure A1 in the online edition study system for cryptic-species diagnosis due to the large of the American Naturalist or are available from the au- number of allopatric populations that are deeply divergent thors on request. Our sampling locations closely reflect genetically (Bezy and Sites 1987; Lovich 2001; Papenfuss the known distribution of Xantusia vigilis (map in Bezy et al. 2001) but difficult to diagnose on the basis of mor- 1982), but not all known localities were sampled, and new phology, when individual and geographic variation is fully localities continue to be reported (e.g., Feldman et al. appraised (Bezy 1967a, 1967b; Bezy and Flores-Villela 2003). All named taxa were sampled, including Xantusia 1999). Xantusia occurs throughout the southwestern de- henshawi gracilis (),n p 1 Xantusia bolsonae (),n p 1 Xan- sert region of North America (fig. 1; fig. A1 in the online tusia sanchezi (),n p 2 Xantusia riversiana (n p 1 ), and edition of the American Naturalist), an area with unusually the seven described subspecies of X. vigilis (),in-n p 117 complex
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