Abstract
BackgroundHeterobranchia is a diverse clade of marine, freshwater, and terrestrial gastropod molluscs. It includes such disparate taxa as nudibranchs, sea hares, bubble snails, pulmonate land snails and slugs, and a number of (mostly small-bodied) poorly known snails and slugs collectively referred to as the “lower heterobranchs”. Evolutionary relationships within Heterobranchia have been challenging to resolve and the group has been subject to frequent and significant taxonomic revision. Mitochondrial (mt) genomes can be a useful molecular marker for phylogenetics but, to date, sequences have been available for only a relatively small subset of Heterobranchia.ResultsTo assess the utility of mitochondrial genomes for resolving evolutionary relationships within this clade, eleven new mt genomes were sequenced including representatives of several groups of “lower heterobranchs”. Maximum likelihood analyses of concatenated matrices of the thirteen protein coding genes found weak support for most higher-level relationships even after several taxa with extremely high rates of evolution were excluded. Bayesian inference with the CAT + GTR model resulted in a reconstruction that is much more consistent with the current understanding of heterobranch phylogeny. Notably, this analysis recovered Valvatoidea and Orbitestelloidea in a polytomy with a clade including all other heterobranchs, highlighting these taxa as important to understanding early heterobranch evolution. Also, dramatic gene rearrangements were detected within and between multiple clades. However, a single gene order is conserved across the majority of heterobranch clades.ConclusionsAnalysis of mitochondrial genomes in a Bayesian framework with the site heterogeneous CAT + GTR model resulted in a topology largely consistent with the current understanding of heterobranch phylogeny. However, mitochondrial genomes appear to be too variable to serve as good phylogenetic markers for robustly resolving a number of deeper splits within this clade.
Highlights
Heterobranchia is a diverse clade of marine, freshwater, and terrestrial gastropod molluscs
The name Heterobranchia was coined by Burmeister (1837), but it is most commonly attributed to Gray (1840) who used it to unite Opisthobranchia and Pulmonata
Maximum likelihood analyses A partitioned maximum likelihood (ML) analysis of this data matrix using the best-fitting model for each gene (Additional file 2: Figure S1; see additional data on FigShare for more information) resulted in a tree with Valvata cristata (Valvatoidea) recovered as the sister taxon to a clade containing all other heterobranchs with successive branching of Microdiscula charopa (Orbitestelloidea), a clade composed of Clione limacina (Gymnosomata), Psilaxis radiatus (Architectonicoidea), Omalogyra atomus (Omalogyroidea), and Rissoella morrocayensis (Rissoelloidae), and Rhopalocaulis grandidieri (Veronicelloidea), which was the sister taxon of all remaining Heterobranchia
Summary
Heterobranchia is a diverse clade of marine, freshwater, and terrestrial gastropod molluscs It includes such disparate taxa as nudibranchs, sea hares, bubble snails, pulmonate land snails and slugs, and a number of (mostly small-bodied) poorly known snails and slugs collectively referred to as the “lower heterobranchs”. The name Heterobranchia was coined by Burmeister (1837), but it is most commonly attributed to Gray (1840) who used it to unite Opisthobranchia (e.g., sea slugs) and Pulmonata (e.g., land snails) This group was later renamed Euthyneura to reflect the secondarily detorted arrangement of the cerebrovisceral commisures [23], but Heterobranchia was redefined to include Euthyneura and a grouping of taxa that are generally referred to as the “lower Heterobranchia” or Allogastropoda [24, 25] including, at times, Pyramidelloidea, Architectonicoidea, Valvatoidea, Orbitestelloidea, Omalogyridae, Rissoellidae, Glacidorbidae, Tjaernoeiidae, Cimidae, Rhodopemorpha, and Murchisonellidae [21, 22, 24,25,26,27,28,29,30]. Opisthobranchia has since been demonstrated to be a non-monophyletic group as sea slug clades such as Sacoglossa and Acochlidia share a more recent common ancestor with the pulmonates than other sea slugs as do some “lower” heterobranchs like Pyramidelloidea and Glacidorbidae [8, 13, 22, 31, 32], reviewed by [19]
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