Article

Evolution of gastropod mitochondrial genome arrangements

Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal, 2, 28006, Madrid, Spain.
BMC Evolutionary Biology (Impact Factor: 3.41). 02/2008; 8:61. DOI: 10.1186/1471-2148-8-61
Source: PubMed

ABSTRACT Gastropod mitochondrial genomes exhibit an unusually great variety of gene orders compared to other metazoan mitochondrial genome such as e.g those of vertebrates. Hence, gastropod mitochondrial genomes constitute a good model system to study patterns, rates, and mechanisms of mitochondrial genome rearrangement. However, this kind of evolutionary comparative analysis requires a robust phylogenetic framework of the group under study, which has been elusive so far for gastropods in spite of the efforts carried out during the last two decades. Here, we report the complete nucleotide sequence of five mitochondrial genomes of gastropods (Pyramidella dolabrata, Ascobulla fragilis, Siphonaria pectinata, Onchidella celtica, and Myosotella myosotis), and we analyze them together with another ten complete mitochondrial genomes of gastropods currently available in molecular databases in order to reconstruct the phylogenetic relationships among the main lineages of gastropods.
Comparative analyses with other mollusk mitochondrial genomes allowed us to describe molecular features and general trends in the evolution of mitochondrial genome organization in gastropods. Phylogenetic reconstruction with commonly used methods of phylogenetic inference (ME, MP, ML, BI) arrived at a single topology, which was used to reconstruct the evolution of mitochondrial gene rearrangements in the group.
Four main lineages were identified within gastropods: Caenogastropoda, Vetigastropoda, Patellogastropoda, and Heterobranchia. Caenogastropoda and Vetigastropoda are sister taxa, as well as, Patellogastropoda and Heterobranchia. This result rejects the validity of the derived clade Apogastropoda (Caenogastropoda + Heterobranchia). The position of Patellogastropoda remains unclear likely due to long-branch attraction biases. Within Heterobranchia, the most heterogeneous group of gastropods, neither Euthyneura (because of the inclusion of P. dolabrata) nor Pulmonata (polyphyletic) nor Opisthobranchia (because of the inclusion S. pectinata) were recovered as monophyletic groups. The gene order of the Vetigastropoda might represent the ancestral mitochondrial gene order for Gastropoda and we propose that at least three major rearrangements have taken place in the evolution of gastropods: one in the ancestor of Caenogastropoda, another in the ancestor of Patellogastropoda, and one more in the ancestor of Heterobranchia.

Download full-text

Full-text

Available from: José Templado, Jun 21, 2015
2 Followers
 · 
290 Views
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Few molecular studies have addressed the phylogenetic relationships within Acanthochitonina. Here, we use high-throughput sequencing to determine three mitochondrial genomes of Acanthochitonina. We further explore phylogenetic relationships with expanded taxon sampling based on mitochondrial and nuclear sequence data. Phylogenetic analyses recover two major lineages roughly corresponding to Cryptoplacoidea and Mopalioidea, but the necessity of reassigning multiple genera challenges their conventional definition and that of the families Mopaliidae, Schizoplacidae and Lepidochitonidae. Two mitogenomes share a gene rearrangement that might represent a synapomorphy for Lepidochitonidae. Our phylogenetic results support the reinterpretation of certain morphological characters as homologous, previously assumed to be convergent. They further reveal that major Acanthochitonina lineages were restricted to particular ocean basins, where they diverged into endemisms with disparate morphology. Our results are corroborated by morphological and biogeographical evidence and contribute toward resolving the phylogenetic relationships of Acanthochitonina, and highlight the need for further phylogenetic and systematic studies.
    Journal of Natural History 12/2014; 48:2825-2853. DOI:10.1080/00222933.2014.963721 · 0.93 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Abstract The first complete mitochondrial genome (mitogenome) of Cerithioidea (Gastropoda: Caenogastropoda) was determined using a freshwater snail Semisulcospira libertina (Cerithioidea: Semisulcospiridae) as a representative species of the superfamily. The mitogenome was 15,432 bp in length, including 13 typical invertebrate protein-coding genes, 22 transfer RNA genes and 2 ribosomal RNA genes. The overall base composition was 31.4% for A, 17.8% for C, 34.8% for T and 16.0% for G with a A + T bias. The mitogenome of S. libertina displayed novel gene order arrangement compared with published Caenogastropoda mitogenomes to date. This mitogenome contributed in resolving phylogenetic position and interrelationships of Cerithioidea.
    Mitochondrial DNA 01/2014; DOI:10.3109/19401736.2013.861449 · 1.70 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Pulmonates, with over 30,000 described species, represent the largest radiation of non-marine animals outside of Arthropoda. The pulmonate lung was a key evolutionary innovation enabling diversification of terrestrial and freshwater snails and slugs. However, recent studies drew conflicting conclusions about pulmonate monophyly, and support for a sister group is lacking, hindering our understanding of this major animal radiation. Analyses of mitochondrial protein-coding genes recovered a paraphyletic Pulmonata grading into a monophyletic Opisthobranchia, a traditional group of sea slugs long considered sister to pulmonates. Conversely, analyses of datsets dominated by nuclear rDNA indicated Opisthobranchia is paraphyletic with respect to Pulmonata. No study resolved the placement of two key taxa: Sacoglossa, an opisthobranch group including photosynthetic sea slugs, and Siphonarioidea, intertidal limpet-like snails traditionally in Pulmonata. To examine evolutionary relationships at the base of the pulmonate radiation, we performed a phylogenomic analysis of 102 nuclear protein-coding gene regions for 19 gastropods. Opisthobranchia was recovered as paraphyletic with respect to Panpulmonata, a clade in which Sacoglossa was sister to Pulmonata, with Siphonarioidea as the basal pulmonate lineage. Siphonarioideans share a similar gill structure with shelled sacoglossans but lack the contractile pneumostome of pulmonates, suggesting descent from an evolutionary intermediate that facilitated the pulmonate radiation into non-marine habitats.
    Molecular Phylogenetics and Evolution 07/2013; 69(3). DOI:10.1016/j.ympev.2013.07.001 · 4.02 Impact Factor