Morphological homoplasy, life history evolution, and historical biogeography of plethodontid salamanders inferred from complete mitochondrial genomes

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.partitioned Bayesian analysis ͉ larvae ͉ tongues ͉ tail autotomy ͉ digits M ore 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 phylo...

Cytogenetic analysis of the Asian Plethodontid salamander, Karsenia koreana: Evidence for karyotypic conservation, chromosome repatterning, and genome size evolution

“…Hydromantes, long considered to be a relative of Batrachoseps and Sg Bolitoglossa (bolitoglossines of Wake 1966), stood out as the only lineage with 14 pairs of chromosomes; all other bolitoglossines have 13 pairs (Sessions & Kezer 1991). We now know that Sg Hydromantes is a plethondontine and not a bolitoglossine (Mueller et al 2004;Vieites et al 2007). In this respect Karsenia and Sg Hydromantes are typical members of the Plethodontinae, of which Plethodon is also typical.…”

“…The proximal cause for this phenomenon is likely related to the presence of large, slowly dividing cells and reduced metabolic rates in species with very large genomes, which retard the rapid developmental changes demanded during amphibian metamorphosis. From this perspective, the relatively small genomes of Desmognathus may have enabled the homoplasic evolution of larvae in this genus (Chippindale et al 2004, Mueller et al 2004. The spelerpines and Hemidactylium, all of which have a larval stage, also have relatively small genomes ( Figure 6).…”

“…The recent discovery of an Asian plethodontid from South Korea, Karsenia koreana (Min et al 2005), has helped to clarify the phylogenetic relationships and historical biogeography of Holarctic plethodontids. Molecular phylogenetic studies of these species have led to a reassessment of their taxonomy and phylogenetic relationships (Mueller et al 2004, Wiens et al 2005Vieites et al 2007). In conflict with traditional taxonomy (Wake 1966), molecular evidence from complete mitochondrial genomes and multiple nuclear loci identifies two distinct subfamilies: Plethodontinae and Hemidactyliinae ( Figure 1) (Vieites et al 2007).…”

Limb regeneration in a direct‐developing terrestrial salamander, Bolitoglossa ramosi (Caudata: Plethodontidae)

“…Plethodontidae species show some biological differences from the other families such as enucleated red blood cells, a projectile tongue, the absence of lungs (Wake, 2009), tail autotomy (Mueller, Macey, Jaekel, Wake, & Boore, 2004), nasolabial grooves and postaxial development of the digits (Wake & Hanken, 1996). They also undergo direct development, where the embryos develop to an adult without any larval stages (Chippindale, Bonett, Baldwin, & Wiens, 2004).…”

Embryonic Staging Table for a Direct‐Developing Salamander, Plethodon cinereus (Plethodontidae)

“…Development of the genus Plethodon is particularly interesting given recent phylogenetic studies, which consistently nest the super-genus Desmognathus within a larger direct-developing clade that includes Plethodon (Chippindale et al, 2004;Mueller et al, 2004;Kozak et al, 2005Kozak et al, , 2009Macey, 2005;Vieites et al, 2007). These studies strongly suggest a reacquisition of larvae within the genus Desmognathus (see also Wake et al, 2011;Fig.…”