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Species Tree Reconstruction of a Poorly Resolved Clade of Salamanders (Ambystomatidae) Using Multiple Nuclear Loci ⇑ Joshua S

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Species Tree Reconstruction of a Poorly Resolved Clade of Salamanders (Ambystomatidae) Using Multiple Nuclear Loci ⇑ Joshua S Molecular Phylogenetics and Evolution 68 (2013) 671–682 Contents lists available at SciVerse ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Species tree reconstruction of a poorly resolved clade of salamanders (Ambystomatidae) using multiple nuclear loci ⇑ Joshua S. Williams a, , John H. Niedzwiecki b, David W. Weisrock a a Department of Biology, University of Kentucky, Lexington, KY 40506, USA b Department of Biology, Belmont University, Nashville, TN 37212, USA article info abstract Article history: The analysis of diverse data sets can yield different phylogenetic estimates that challenge systematists to Received 13 June 2012 explain the source of discordance. The mole salamanders (family Ambystomatidae) are a classic example Revised 14 April 2013 of this phylogenetic conflict. Previous attempts to resolve the ambystomatid species tree using allozymic, Accepted 16 April 2013 morphological, and mitochondrial sequence data have yielded different estimates, making it unclear Available online 28 April 2013 which data source best approximates ambystomatid phylogeny and which ones yield phylogenetically inaccurate reconstructions. To shed light on this conflict, we present the first multi-locus DNA Keywords: sequence-based phylogenetic study of the Ambystomatidae. We utilized a range of analyses, including Coalescent analysis coalescent-based methods of species-tree estimation that account for incomplete lineage sorting within Concordance analysis Bayesian analysis a locus and concordance-based methods that estimate the number of sampled loci that support a partic- Gene tree ular clade. We repeated these analyses with the removal of individual loci to determine if any locus has a Species tree disproportionate effect on our phylogenetic results. Collectively, these results robustly resolved many Ambystoma deep and relatively shallow clades within Ambystoma, including the placement of A. gracile and A. talpoid- eum as the sister clade to a clade containing all remaining ambystomatids, and the placement of A. mac- ulatum as the sister lineage to all remaining ambystomatids excluding A. gracile and A. talpoideum. Both Bayesian coalescent and concordance methods produced similar results, highlighting strongly supported branches in the species tree. Furthermore, coalescent-based analyses that excluded loci produced over- lapping species-tree posterior distributions, suggesting that no particular locus – including mtDNA – dis- proportionately contributed to our species-tree estimates. Overall, our phylogenetic estimates have greater similarity with previous allozyme and mitochondrial sequence-based phylogenetic estimates. However, intermediate depths of divergence in the ambystomatid species tree remain unresolved, poten- tially highlighting a region of rapid species radiation or a hard polytomy, which limits our ability to com- ment on previous morphologically-based taxonomic groups. Published by Elsevier Inc. 1. Introduction vidual data sets can sometimes identify the source of discordance (e.g., Wiens and Hollingsworth, 2000), in other studies individual Systematists are often challenged to explain phylogenetic con- data sets can yield convincingly strong support, precluding resolu- flict arising from the analysis of diverse data sets (e.g., morpholog- tion of the conflict. In these situations, collection of additional data ical and molecular data) (Shaffer et al., 1991; Wiens and from an independently evolving source will be necessary to eluci- Hollingsworth, 2000). Individual data sets can be phylogenetically date phylogenetic history and shed light on the source of the initial misleading if parallel evolution has produced homoplastic charac- phylogenetic conflict. ters, a problem inherent in both morphological and molecular Phylogenetic reconstruction of multiple independent loci can characters (Hillis, 1987). Furthermore, properties of the underlying also yield discordance among gene trees, a product of a number phylogeny itself can facilitate inaccurate estimation when terminal of processes, including incomplete lineage sorting (deep coales- branches are long relative to internal branches [e.g., long branch cence) and lateral gene transfer (Maddison, 1997). Concatenated attraction (Felsenstein, 1978)]. While further exploration of indi- phylogenetic analysis of loci represents a traditional approach to resolving a prevailing species tree from a collection of loci, with ⇑ the potential to yield strongly supported trees when large numbers Corresponding author. Address: DNA Analysis Facility on Science Hill at Yale of loci are considered, even when there is gene tree discordance University, 170 Whitney Ave., ESC Room 150, New Haven, CT 06511, USA. Fax: +1 203 432 7394. (Rokas and Carroll, 2005). However, despite this potential, concat- E-mail address: [email protected] (J.S. Williams). enation has been shown to have a high probability for statistical 1055-7903/$ - see front matter Published by Elsevier Inc. http://dx.doi.org/10.1016/j.ympev.2013.04.013 672 J.S. Williams et al. / Molecular Phylogenetics and Evolution 68 (2013) 671–682 inconsistency when there is substantial gene tree discordance, data sources, including the morphological placement of A. gracile resulting in strongly supported yet inaccurate phylogenies (Kubat- as the sister lineage to all other Ambystoma species. However, the ko and Degnan, 2007; Weisrock et al., 2012). Methods that esti- Linguaelapsus clade has been highlighted as a particularly striking mate a species tree from independently estimated gene trees, example of discordance between morphological and molecular including those that account for the stochastic nature of genetic data sets (Shaffer et al., 1991). Combined analysis of the data only drift in the lineage-sorting process, may be more likely to recon- weakly supports the Linguaelapsus clade (Jones et al., 1993; Shaf- struct the true species phylogeny, despite strongly supported dis- fer et al., 1991), but individual data sets each strongly support dif- cordance among gene trees (Edwards et al., 2007; Leache and ferent placements for its component taxa. Whether or not this Rannala, 2011). discordance results from homoplasy in one, or both, data sets, or The phylogeny of salamander species of the family Ambystom- extreme non-independence among characters is not clear. atidae represents a classic example of phylogenetic conflict arising Phylogenetic reconstruction of the Ambystomatidae using mul- from the analysis of very different data sources (Shaffer et al., tiple independent sources of DNA sequence data represents one 1991). The Ambystomatidae are broadly distributed across North step towards elucidating the factors causing this strong discor- America, and feature a diverse array of life-history phenotypes. dance. There have been previous attempts to reconstruct ambys- This includes a radiation of US and Mexican species (the tiger sal- tomatid phylogeny using mtDNA sequence data. Bogart (2003) amanders) that vary in their propensity to metamorphose, and a presented a phylogenetic tree based on cytochrome b (cytb) and group of unisexual populations in eastern North America that are 16S sequence data that included all species of Ambystoma, except putatively of hybrid origin. Phylogenetic analyses of allozymic for A. annulatum. This tree placed A. texanum and A. barbouri to- and morphological data sets collected from sexual Ambystoma spe- gether in a clade, with A. mabeei maintaining a close relationship cies (and representative tiger salamander species) yield a number with these two species; however, the Linguaelapsus clade was of discordant topological patterns. The strongest of these involves not recovered. In a subsequent mtDNA study of the origin of uni- a morphologically supported clade, named Linguaelapsus, com- sexual ambystomatids using cytb sequence data, Robertson et al. prising Ambystoma annulatum, A. barbouri, A. cingulatum, A. mabeei, (2006) resolved a clade that contained Linguaelapsus species (A. and A. texanum (Fig. 1A) (Kraus, 1988). In contrast, parsimony and annulatum was not sampled) along with representative tiger sala- maximum-likelihood analysis of allozymic data strongly support mander taxa. However, this clade – and the majority of interspe- very different placements of these taxa within the Ambystoma tree cific relationships – received very low parsimony and Bayesian (Fig. 1B). A number of other relationships differ between the two branch support. This study may also have been misled by the inclu- sion of a nuclear paralog of cytb (Bi and Bogart, 2010). In this study, we have presented the first multi-locus nuclear A Ambystoma gracile DNA sequence data set ever collected to resolve phylogenetic rela- 91 A. tigrinum tionships among sexual species of Ambystoma. We included repre- A. californiense sentatives of nearly all sexual species, including multiple 74 A. laterale representatives of the diverse tiger salamander clade. Sequence A. jeffersonianum data were generated from 14 nuclear loci, a majority of which were 22 A. macrodactylum located on separate linkage groups, and a mitochondrial locus. To A. maculatum avoid the complexities and challenges associated with sampling al- leles from heterozygous individuals for use in concatenated phylo- 59 A. opacum 42 A. talpoideum genetic analysis (Weisrock et al., 2012), we focused on analyses A. mabeei that allow for the independent reconstruction of locus-specific 96 gene trees. We explored gene-tree discordance among loci
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