| Abstract | The evolutionary history of the largest salamander family (Plethodontidae) is characterized by extreme morphological homoplasy. Analysis of the mechanisms generating such homoplasy requires an independent molecular phylogeny. To this end, we sequenced 24 complete mitochondrial genomes (22 plethodontids and two outgroup taxa), added data for three species from GenBank, and performed partitioned and unpartitioned Bayesian, maximum likelihood, and maximum parsimony phylogenetic analyses. We explored four dataset partitioning strategies to account for evolutionary process heterogeneity among genes and codon positions, all of which yielded increased model likelihoods and decreased numbers of supported nodes in the topologies (Bayesian posterior probability >0.95) relative to the unpartitioned analysis. Our phylogenetic analyses yielded congruent trees that contrast with the traditional morphology-based taxonomy; the monophyly of three of four major groups is rejected. Reanalysis of current hypotheses in light of these evolutionary relationships suggests that (i) a larval life history stage reevolved from a direct-developing ancestor multiple times; (ii) there is no phylogenetic support for the "Out of Appalachia" hypothesis of plethodontid origins; and (iii) novel scenarios must be reconstructed for the convergent evolution of projectile tongues, reduction in toe number, and specialization for defensive tail loss. Some of these scenarios imply morphological transformation series that proceed in the opposite direction than was previously thought. In addition, they suggest surprising evolutionary lability in traits previously interpreted to be conservative. More than two-thirds of the 522 species of salamanders are members of Plethodontidae (http://amphibiaweb.org), a clade that exhibits both extreme long-term stasis and great adaptive diversity in life history, ecology, and morphology. Morphological evolution in plethodontids is characterized by extensive homoplasy (1). Previous studies examining the causes of this homoplasy identify recurrent morphological transformations and address both their outcomes, or derived character states, and their necessary ancestral preconditions (2, 3). Two plethodontid features figure prominently in shaping morphological evolution: lunglessness, a synapomorphy for the clade, and direct development, present in three of the four major groups. No well supported molecular phylogenetic hypothesis exists for plethodontids. As a consequence, all analyses of morphological homoplasy are based on phylogenies constructed from many of these same homoplastic characters (4). We present a molecular phylogenetic hypothesis for plethodontids based on 27 complete mitochondrial genomes, 24 of which were sequenced for this study. We explore four strategies for partitioning our dataset in a Bayesian phylogenetic framework and compare those results to maximum parsimony (MP) and maximum likelihood (ML) results. Our mitochondrial phylogeny differs markedly from the morphological phylogenetic hypotheses reflected in current taxonomy; accordingly, we reevaluate plethodontid life history evolution, origins, and historical biogeography. We examine three recurring evolutionary morphological transformations: modification effecting tongue protraction, reduction in toe number, and specialization for defensive tail loss (autotomy). We present scenarios of morphological transformation that will inform future research into the evolutionary history of plethodontid form. These scenarios suggest previously undescribed transformation series for homoplastic characters. Although some are consistent with traditional hypotheses regarding the direction of evolutionary change, others suggest surprising, previously unconsidered reversals in the direction of morphological evolution.
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