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Caudata: Dicamptodontidae) Molecular Phylogenetics and Evolution 36 (2005) 90–100 www.elsevier.com/locate/ympev Testing hypotheses of speciation timing in Dicamptodon copei and Dicamptodon aterrimus (Caudata: Dicamptodontidae) Craig A. Steelea,¤, Bryan C. Carstensb, Andrew Storfera, Jack Sullivanb,c a School of Biological Sciences, Washington State University, Pullman, WA 99164-4236, USA b Department of Biological Sciences, University of Idaho, Moscow, ID 83844-3051, USA c Initiative in Bioinformatics and Evolutionary Studies (IBEST), USA Received 28 August 2004; revised 6 December 2004 Available online 25 January 2005 Abstract Giant salamanders of the genus Dicamptodon are members of the mesic forest ecosystem that occurs in the PaciWc Northwest of North America. We estimate the phylogeny of the genus to test several hypotheses concerning speciation and the origin of current species distributions. SpeciWcally, we test competing a priori hypotheses of dispersal and vicariance to explain the disjunct inland dis- tribution of the Idaho giant salamander (D. aterrimus) and to test the hypothesis of Pleistocene speciation of Cope’s giant salaman- der (D. copei) using Bayesian hypothesis testing. We determined that available outgroups were too divergent to root the phylogeny eVectively, and we calculated Bayesian posterior probabilities for each of the 15 possible root placements for this four-taxon group. This analysis placed the root on the branch leading to D. aterrimus, indicating that current distribution and speciation of D. aterri- mus Wt the ancient vicariance hypothesis and are attributable to the orogeny of the Cascade Mountains rather than recent inland dis- persal. Furthermore, test results indicate that D. copei is distantly related to other coastal lineages and likely originated much earlier than the Pleistocene. These results suggest that speciation within the genus is attributable to ancient geologic events, while more recent Pleistocene glaciation has shaped genetic variation and distributions within the extant species. 2004 Elsevier Inc. All rights reserved. Keywords: Bayesian hypothesis testing; Biogeography; Dicamptodon; PaciWc Northwest 1. Introduction and southeastern portions of the United States (Austin et al., 2002; Avise and Walker, 1998; Donovan et al., A current trend in evolutionary biology has been the 2000; Zamudio and Savage, 2003) and recently in the examination of speciation, current range distributions, western U.S., especially in the PaciWc Northwest (Dem- and patterns of genetic subdivision in the context of boski and Cook, 2001; Green et al., 1996; Soltis et al., Pleistocene climate change and the associated cycles of 1997). glacial advance and retreat (Austin et al., 2002; Church The PaciWc Northwest (PNW) of North America has et al., 2003; Crespi et al., 2003; Starkey et al., 2003; been inXuenced by numerous geological processes that Steinfartz et al., 2000; Sullivan et al., 2000; Zamudio and have resulted in a complex and varied topography. The Savage, 2003). Several studies invoke pre-Pleistocene combination of geologically ancient mountain ranges events or conditions to explain patterns of genetic struc- overlain with recent Pleistocene glaciation provides a ture, speciation, and disjunct populations in the eastern complex, yet well-deWned historical context with which to interpret genetic data (Cracraft, 1988; Riddle, 1996). ¤ Corresponding author. As a result, tractable predictive hypotheses are possible E-mail address: [email protected] (C.A. Steele). with respect to speciation and phylogeography of the 1055-7903/$ - see front matter 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ympev.2004.12.001 C.A. Steele et al. / Molecular Phylogenetics and Evolution 36 (2005) 90–100 91 region (Brunsfeld et al., 2001). Within the PNW, conif- erous rainforest ecosystems occur along the western coast of North America, from southern Alaska to northern California, with a disjunct inland forest in the northern Rocky Mountains (NRM) of British Colum- bia, Idaho, and extreme western Montana. Mesic for- ests have long been established in the PNW, dating to the mid Eocene in the NRM and were established in their present coastal range by the early Pliocene (5– 2mya; Graham, 1993). The uplift of the Cascades established a rain shadow that caused xeriWcation of the Columbia basin prior to the Pleistocene (2 mya; Daubenmire, 1952; Graham, 1993), which eVectively divided mesic forests into a coastal element and an inland element. Subsequent Pleistocene glaciation resulted in severe southern compression of the PNW mesic forests during glacial maxima (Delcourt and Del- court, 1993; Soltis et al., 1997; Waitt and Thorson, 1983), and would have forced mesic forest organisms into refugia. The giant salamanders of the genus Dicamptodon are endemic to mesic forests of the PNW. Members of this genus provide an ideal study system for examining bio- geographic hypotheses since the species are widespread throughout the western United States with several species Fig. 1. Approximate distribution of the four species in the salamander genus Dicamptodon. Numbers indicate approximate sampling sites endemic to particular geographic locales. The genus was and correspond to numbers in Appendix. Populations sometimes originally considered monotypic (Tihen, 1958) but subse- included several nearby localities; refer to Appendix for speciWc local- quent morphological (Nussbaum, 1970, 1976) and molec- ity information. ular studies (Daugherty et al., 1983; Good, 1989) have resulted in recognition of four species (Fig. 1). D. copei is found primarily in the Olympic Peninsula and Coast 2001). The ancient vicariance hypothesis invokes pre- Range of Washington, D. ensatus is restricted to regions Pleistocene isolation of ancestral D. aterrimus from the surrounding the San Francisco Bay, and D. tenebrosus is rest of the genus, associated with xeriWcation of the widespread and ranges from the Cascade Mountains in Columbia basin following the Cascade orogeny. It pre- British Columbia in the north through Washington and dicts deep genetic divergence and reciprocal monophyly Oregon into California. D. tenebrosus forms a contact between D. aterrimus and coastal Dicamptodon species zone with D. ensatus north of San Francisco and is sym- (Fig. 2A), and requires that D. aterrimus persisted in a ref- patric with D. copei in parts of western Washington and uge located in one or more of the river canyons south of extreme northern Oregon. The fourth species, D. aterri- glacial maxima throughout the Pleistocene. Phylogeo- mus, occurs in a disjunct portion of the mesic forest eco- graphic studies of two other PNW amphibian lineages system in northern Idaho and is geographically isolated endemic to the mesic forests, Ascaphus truei/A. montanus from the rest of the genus. Results of allozyme studies (Neilson et al., 2001) and Plethodon vandykei/P. idahoensis have consistently shown that the highest genetic distances (Carstens et al., 2004), provide support for the ancient within the genus occur between D. aterrimus and coastal vicariance hypothesis. Alternatively, D. aterrimus could be species (Daugherty et al., 1983; Good, 1989), but relation- a post-Pleistocene arrival to the NRM, with either a ships within coastal lineages have not yet been resolved southern dispersal route through the central Oregon high- (Good, 1989). Here, we use mitochondrial DNA sequence lands or a northern route through southern British data to resolve relationships within Dicamptodon with two Columbia and northern Washington as glaciers retreated. complementary analyses. First, we test for monophyly of These inland dispersal hypotheses predict a topology each of the four described species and second, we test a where D. aterrimus is nested within the clade from which priori hypotheses regarding speciation for D. aterrimus its ancestors originated: either the clade of northern D. and D. copei derived from biogeographic studies in the tenebrosus haplotypes for the inland dispersal-north PNW mesic forest ecosystem. hypothesis (Fig. 2B), or southern D. tenebrosus haplotypes The competing hypotheses relevant to speciation of D. for the inland dispersal-south hypothesis (Fig. 2C). aterrimus in the inland mesic posit either pre-Pleistocene A second taxon for which a priori hypotheses have vicariance or post-Pleistocene dispersal (Brunsfeld et al., been erected is D. copei (Nussbaum, 1976), the only 92 C.A. Steele et al. / Molecular Phylogenetics and Evolution 36 (2005) 90–100 explicitly test a priori hypotheses related to the specia- tion of D. aterrimus and D. copei. In doing so, we evalu- ate the relative inXuence of pre-Pleistocene and Pleistocene geological events on speciation within the genus. 2. Materials and methods 2.1. DNA extraction, ampliWcation, and sequencing We obtained tissue samples from throughout the geo- graphic range of each species and included: 12 D. copei from Wve populations, 46 D. tenebrosus from 16 popula- tions, 10 D. ensatus from Wve populations, and used sequence from six D. aterrimus from Carstens et al. (2005) that represented the greatest divergence within this species (Fig. 1; Appendix). Sample sizes ranged from 1 to 5 with an average of 2.8 samples per population. The Ambystomatidae is traditionally considered to be the sister taxon to the Dicamptodontidae (Larson, 1991), and we used sequence from Ambystoma mexicanum as a putative outgroup. DNA was extracted from 10 to 20 mg tail clips, which had been stored in 90% EtOH, either with the DNeasy Tissue kit (Qiagen;
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