Animal mitochondrial (mt) genomes typically consist of a circular molecule of DNA encoding 37 genes (2 rRNA genes, 13 protein-encoding genes, and 22 tRNA genes), the arrangement of which is often highly conserved within major taxonomic groups . Consequently, when gene rearrangements occur, they may provide compelling phylogenetic markers that can corroborate or contradict hypotheses based on primary sequence data and provide resolution for deeper nodes that are often weakly supported in sequence-based phylogenies [2–6]. With recent technological and methodological advances (e.g., rolling circle amplification: [7, 8]; next generation sequencing technologies: ), and associated decreasing costs of DNA sequencing, the amplification and sequencing of whole mt genomes has become routine. As a result, there has been a marked increase in the sequencing of whole animal mt genomes over the past decade as well as the development of computational methods to extract phylogenetic information from these genomes through inferences of past gene dynamics [10–12]. To date, 1868 complete metazoan mt genomes are available in the NCBI Genomes database http://www.ncbi.nlm.nih.gov/guide/genomes/; January 8, 2010), the majority belonging to arthropods (293) and vertebrates (1292).
Compared to other major metazoan phyla, molluscan mitochondrial genomes are poorly represented at NCBI , with only 78 complete mt genomes available as of January, 2010. Despite this, molluscan mt genomes are beginning to challenge the traditional view that mitochondrial gene orders are stable over long periods of evolutionary time [13–16], a view based largely on the heavily sampled and highly conserved mt genomes of vertebrates. Instead, mollusc mt genomes demonstrate substantial heterogeneity in length and "architecture" , reflecting differences in gene complement resulting from gene loss or duplication, as well as changes in the position and strand specificity of tRNA genes, protein-encoding genes, and rRNA genes. Changes in gene arrangement within the Mollusca have been so dramatic that representatives of four classes of molluscs (Gastropoda; Bivalvia; Cephalopoda; Scaphopoda) share remarkably few mitochondrial gene boundaries, with gene orders varying extensively even across major lineages of bivalves as well as gastropods . Changes in gene arrangement have also been observed within bivalve and gastropod genera, based on changes in position of: 1) tRNAs and an rRNA gene in the oyster, Crassostrea , and 2) protein encoding and tRNA genes in the vermetid marine gastropod genus, Dendropoma . Differences in gene order are also evident between paternally versus maternally inherited mitochondrial genomes of bivalves exhibiting doubly uniparental inheritance , including the unionid freshwater bivalve, Inversidens japanensis , and the marine venerid clam, Venerupis (Ruditapes) philippinarum (NCBI, unpublished). Similar intrageneric gene translocations have now been described in 19 of 144 genera in which two or more complete mt genomes have been sequenced , including representatives of the Porifera, Platyhelminthes, Nematoda, Mollusca, Arthropoda and Chordata. Thus, growing evidence suggests that mt genomes of many metazoan phyla may be considerably more plastic than originally believed, with the conserved genome architecture of vertebrates reflecting a derived stabilization of the mt genome and not an ancestral feature .
The discovery of mt gene order changes at lower taxonomic levels, as found within the Mollusca, is exciting for several reasons. First, gene dynamics involving translocations and inversions of genes offer the promise of new and robust characters that can be used to support phylogenetic hypotheses at the level of families, genera, and species . Given the comparatively low rate of rearrangement and the astronomical number of possible gene arrangements, convergence is likely to be rare compared to four-state nucleotide sequence data . Second, it is becoming increasingly apparent that the application of mitochondrial sequences and gene order data to questions of evolutionary history and phylogenetic relatedness requires a better understanding of the evolutionary dynamics of mt genomes . Basic mechanisms of gene rearrangement associated with slipped-strand mispairing , errors in replication origins or end points , and intramolecular recombination , remain poorly understood. Likewise, tRNA remolding and tRNA recruitment events [25–28], gene rearrangement "hotspots" [29, 30], the non-random loss of duplicated genes  and gene order homoplasy [32–34], which can act to confound phylogenetic inferences based on mtDNA sequences and gene orders, need to be explored more fully. Comparison of gene arrangements at low taxonomic levels can help to elucidate the process of gene rearrangement. For instance, the signature of specific processes such as tRNA remolding or recruitment can be most easily recognized when such events have occurred recently, since remolded or recruited tRNAs can be identified through high similarity scores and phylogenetic analyses [27, 28]. Likewise, those taxonomic groupings with unusually labile genomes offer the opportunity to investigate the mechanics of gene rearrangement: telltale vestiges of gene duplication and translocation, typically erased or overwritten with time, may still be present within these genomes  and such intermediate stages can be critical to reconstructing the processes through which such gene rearrangements have occurred. Comparisons of mt genomes at low taxonomic levels, even within families and genera, can thus be extremely helpful in interpreting the evolutionary dynamics of these genomes and exploiting the phylogenetic signal retained within these DNA molecules .
Here we present further evidence of highly dynamic molluscan mt genomes by revealing extensive gene order changes within members of one caenogastropod family: the Vermetidae. Vermetids are a group of sessile, irregularly coiled, suspension-feeding gastropods found in warm temperate to tropical oceans around the world that radiated from a basal caenogastropod stock in the early Cenozoic Era. They are currently classified as members of the Hypsogastropoda [36, 37], a large and diverse group with a fossil record extending back to the Permo-Triassic boundary that includes all extant caenogastropods, except for the Architaenioglossa, Cerithioidea and Campaniloidea. While relationships within the Hypsogastropoda are not well resolved, vermetids are typically positioned within the infraorder Littorinimorpha. More specifically, molecular analyses suggest that vermetids are members of a largely asiphonate clade of gastropods including the Littorinidae, Eatoniellidae, Rissoidae, Anabathridae, Hipponicidae, Pterotracheidae, Epitoniidae, Cerithiopsidae, Eulimidae, and Naticidae . This association is also supported by morphological similarities in euspermatozoa shared by many members of this clade .
Gene order rearrangements have been recognized previously in this family  based on small (<3.5 kb) portions of the mt genome sequenced from several species within the genus Dendropoma. In this paper, we expand upon these earlier results by providing complete mt genomes for two Dendropoma species as well as for representatives of two other vermetid genera, Thylacodes and Eualetes. We also reveal additional gene rearrangements within this family through the partial genomes of the vermetid genera Thylaeodus and Vermetus. The extent of gene rearrangement within the family offers great potential for improving our phylogenetic hypothesis for the enigmatic Vermetidae as well as for understanding more fully the mechanics of gene order change within metazoan mt genomes.