Evolution of gastropod mitochondrial genome arrangements

Abstract

BackgroundGastropod 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.ResultsComparative 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.ConclusionFour 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.

Conservation and variation in mitochondrial genomes of gastropods Oncomelania hupensis and Tricula hortensis, intermediate host snails of Schistosoma in China

“…In this study, we investigated complete protein-coding genes of 32 published gastropod species that produced 4044 length of alignable amino acids sequences. Most of the phylogenetic clades shown in the present study matched with the recent taxonomy and phylogeny of Gastropoda (Bouchet and Rocroi, 2005;Grande et al, 2008), although a bit opposite to the traditional subclasses of Gastropoda (i.e., Prosobranchia, Opisthobranchia, and Pulmonata), which was already discussed well by Grande et al (2008) and may be just beyond the topic of the present study. However, some questions still remain regarding the relationship of Caenogastropoda and Heterobranchia, two of which were thought as sister groups comprising the Apogastropoda; but in the present study, Vetigastropoda showed a closer relationship with Caenogastropoda than Heterobranchia.…”

“…The species within the Gastropoda were identified into four main lineages: Caenogastropoda, Vetigastropoda, Patellogastropoda and Heterobranchia. Within the Heterobranchia, both Pulmonata and Opisthobranchia were recovered to be polyphyletic, and P. dolabrata in the Pyramidelloidea was recovered deep within Pulmonata and Opistobranchia, which is coincident with the Gastropoda phylogentic tree constructed by Grande et al (2008). The interrelationship within Caenogastropoda matches their published taxonomy, except that C. parthenopeum is more closely related to Neogastropoda than to Littorinimorpha.…”

“…However, some questions still remain regarding the relationship of Caenogastropoda and Heterobranchia, two of which were thought as sister groups comprising the Apogastropoda; but in the present study, Vetigastropoda showed a closer relationship with Caenogastropoda than Heterobranchia. Another question is the position of Patellogastropoda L. digitalis, which has a unique mt gene order and a long branch compared to other gastropods in phylogenetic analyses (Colgan et al, 2003;Grande et al, 2008), but still showed closer relationship with Heterobranchia than with other taxa. More representatives of Vetigastropoda and Patellogastropoda need to be analyzed in order to resolve their phylogenetic positions.…”

“…The ribbed-shelled O. hupensis hupensis is well closely related with the smooth-shelled O. hupensis robertsoni, and then to T. hortensis, forming a clade of Littorinimorpha which is in turn clusted with other species in the Neogastropoda. All species in Caenogastropoda have completely the same gene arrangement in their mt genomes, and this high level of conservation is seldom found in other clades of Gastropoda (Grande et al, 2008).…”

Phylogenetic relationships and evolution of pulmonate gastropods (Mollusca): New insights from increased taxon sampling

“…The two most comprehensive data sets thus far for euthyneuran (opisthobranch and pulmonate) phylogenetics have been published by Grande et al (2008), based on mitochondrial genomes, and by Klussmann-Kolb et al (2008), based on 18S, 28S, 16S, and COI data. Dinapoli and Klussmann-Kolb (2010) also published a study focusing on early heterobranchs, i.e., the lineages that branched off just before euthyneurans.…”