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Evolution of gastropod mitochondrial genome arrangements.

Grande C, Templado J, Zardoya R - BMC Evol. Biol. (2008)

Bottom Line: This result rejects the validity of the derived clade Apogastropoda (Caenogastropoda + Heterobranchia).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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal, 2, 28006, Madrid, Spain. grande@berkeley.edu

ABSTRACT

Background: 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.

Results: 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.

Conclusion: 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.

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Hypothesized mitochondrial gene rearrangements during Gastropoda evolution based on observed gene orders and the recovered BI phylogenetic hypothesis. Inversion (indicated by the arrow) and transpositions of protein coding, tRNAs and rRNA genes are depicted among the different taxa (except between H. rubra-L. digitalis and H. rubra- Heterobranchia due to the high number of changes). Genes encoded by the minor strand are underlined. Genes located in apomorphic arrangements are colored.
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Figure 4: Hypothesized mitochondrial gene rearrangements during Gastropoda evolution based on observed gene orders and the recovered BI phylogenetic hypothesis. Inversion (indicated by the arrow) and transpositions of protein coding, tRNAs and rRNA genes are depicted among the different taxa (except between H. rubra-L. digitalis and H. rubra- Heterobranchia due to the high number of changes). Genes encoded by the minor strand are underlined. Genes located in apomorphic arrangements are colored.

Mentions: Each of the five newly determined gastropod mt genomes exhibits a different gene order (Fig. 4). Moreover, among all reported gastropod mt genomes only two sets of species (I. obsoleta + L. cerithiformis, and A. californiaca + P. strigosa) have the same gene order (Fig. 4). Despite the observed arrangement diversity, several general patterns may be inferred. The gene order of the L. digitalis mt genome is the most divergent among all gastropod mtDNAs sequenced thus far. The vetigastropoda H. rubra mt genome has the same gene order of the cephalopod O. vulgaris mt genome except for the relative position of three tRNA (trnC, trnD and trnN) genes (Fig. 4). The identical gene order exhibit by the two caenogastropod mt genomes only differs from that of O. vulgaris in one translocation and one inversion (Fig. 4). Despite several autapomorphies, all heterobranch mt genomes analyzed in this study share a general conserved gene order, which substantially differs from that of other gastropods (Fig. 4). S. pectinata and P. dolabrata show several autapomorphies that involve changes not only in the relative position of tRNAs but also of some protein coding genes (cox2, nad4L, and atp6) (Fig. 4). M. myosotis and C. nemoralis have autapomorphic relative positions for nad4L and cox3 genes, respectively (Fig. 4). Changes in the remaining analyzed heterobranch mt genomes affect the arrangement of trnW, trnY, trnC, trnP, and trnT genes (Fig. 4).


Evolution of gastropod mitochondrial genome arrangements.

Grande C, Templado J, Zardoya R - BMC Evol. Biol. (2008)

Hypothesized mitochondrial gene rearrangements during Gastropoda evolution based on observed gene orders and the recovered BI phylogenetic hypothesis. Inversion (indicated by the arrow) and transpositions of protein coding, tRNAs and rRNA genes are depicted among the different taxa (except between H. rubra-L. digitalis and H. rubra- Heterobranchia due to the high number of changes). Genes encoded by the minor strand are underlined. Genes located in apomorphic arrangements are colored.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2291457&req=5

Figure 4: Hypothesized mitochondrial gene rearrangements during Gastropoda evolution based on observed gene orders and the recovered BI phylogenetic hypothesis. Inversion (indicated by the arrow) and transpositions of protein coding, tRNAs and rRNA genes are depicted among the different taxa (except between H. rubra-L. digitalis and H. rubra- Heterobranchia due to the high number of changes). Genes encoded by the minor strand are underlined. Genes located in apomorphic arrangements are colored.
Mentions: Each of the five newly determined gastropod mt genomes exhibits a different gene order (Fig. 4). Moreover, among all reported gastropod mt genomes only two sets of species (I. obsoleta + L. cerithiformis, and A. californiaca + P. strigosa) have the same gene order (Fig. 4). Despite the observed arrangement diversity, several general patterns may be inferred. The gene order of the L. digitalis mt genome is the most divergent among all gastropod mtDNAs sequenced thus far. The vetigastropoda H. rubra mt genome has the same gene order of the cephalopod O. vulgaris mt genome except for the relative position of three tRNA (trnC, trnD and trnN) genes (Fig. 4). The identical gene order exhibit by the two caenogastropod mt genomes only differs from that of O. vulgaris in one translocation and one inversion (Fig. 4). Despite several autapomorphies, all heterobranch mt genomes analyzed in this study share a general conserved gene order, which substantially differs from that of other gastropods (Fig. 4). S. pectinata and P. dolabrata show several autapomorphies that involve changes not only in the relative position of tRNAs but also of some protein coding genes (cox2, nad4L, and atp6) (Fig. 4). M. myosotis and C. nemoralis have autapomorphic relative positions for nad4L and cox3 genes, respectively (Fig. 4). Changes in the remaining analyzed heterobranch mt genomes affect the arrangement of trnW, trnY, trnC, trnP, and trnT genes (Fig. 4).

Bottom Line: This result rejects the validity of the derived clade Apogastropoda (Caenogastropoda + Heterobranchia).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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José Gutiérrez Abascal, 2, 28006, Madrid, Spain. grande@berkeley.edu

ABSTRACT

Background: 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.

Results: 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.

Conclusion: 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.

Show MeSH
Related in: MedlinePlus