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Accelerated evolution of mitochondrial but not nuclear genomes of Hymenoptera: new evidence from crabronid wasps.

Kaltenpoth M, Showers Corneli P, Dunn DM, Weiss RB, Strohm E, Seger J - PLoS ONE (2012)

Bottom Line: This effect should result in elevated substitution rates of both nuclear and mitochondrial genes, but to date no extensive comparative study has tested this hypothesis in insects.The mt-genome of P. triangulum is 16,029 bp in size with a mean A+T content of 83.6%, and it encodes the 37 genes typically found in arthropod mt genomes (13 protein-coding, 22 tRNA, and two rRNA genes).Thus, our results suggest that the ancestral parasitic lifestyle of Apocrita is unlikely to be the major cause for the elevated substitution rates observed in hymenopteran mitochondrial genomes.

View Article: PubMed Central - PubMed

Affiliation: Research Group Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany. mkaltenpoth@ice.mpg.de

ABSTRACT
Mitochondrial genes in animals are especially useful as molecular markers for the reconstruction of phylogenies among closely related taxa, due to the generally high substitution rates. Several insect orders, notably Hymenoptera and Phthiraptera, show exceptionally high rates of mitochondrial molecular evolution, which has been attributed to the parasitic lifestyle of current or ancestral members of these taxa. Parasitism has been hypothesized to entail frequent population bottlenecks that increase rates of molecular evolution by reducing the efficiency of purifying selection. This effect should result in elevated substitution rates of both nuclear and mitochondrial genes, but to date no extensive comparative study has tested this hypothesis in insects. Here we report the mitochondrial genome of a crabronid wasp, the European beewolf (Philanthus triangulum, Hymenoptera, Crabronidae), and we use it to compare evolutionary rates among the four largest holometabolous insect orders (Coleoptera, Diptera, Hymenoptera, Lepidoptera) based on phylogenies reconstructed with whole mitochondrial genomes as well as four single-copy nuclear genes (18S rRNA, arginine kinase, wingless, phosphoenolpyruvate carboxykinase). The mt-genome of P. triangulum is 16,029 bp in size with a mean A+T content of 83.6%, and it encodes the 37 genes typically found in arthropod mt genomes (13 protein-coding, 22 tRNA, and two rRNA genes). Five translocations of tRNA genes were discovered relative to the putative ancestral genome arrangement in insects, and the unusual start codon TTG was predicted for cox2. Phylogenetic analyses revealed significantly longer branches leading to the apocritan Hymenoptera as well as the Orussoidea, to a lesser extent the Cephoidea, and, possibly, the Tenthredinoidea than any of the other holometabolous insect orders for all mitochondrial but none of the four nuclear genes tested. Thus, our results suggest that the ancestral parasitic lifestyle of Apocrita is unlikely to be the major cause for the elevated substitution rates observed in hymenopteran mitochondrial genomes.

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Maximum likelihood tree inferred from the mitochondrial 12S and 16SrRNA gene sequences of 50 representative taxa from the four major holometabolous insect orders.Branches are color-coded based on order-level taxonomic affiliations (see Fig. 2).
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pone-0032826-g003: Maximum likelihood tree inferred from the mitochondrial 12S and 16SrRNA gene sequences of 50 representative taxa from the four major holometabolous insect orders.Branches are color-coded based on order-level taxonomic affiliations (see Fig. 2).

Mentions: Bayesian and maximum likelihood analyses were used to reconstruct the phylogeny of holometabolous insects based on mitochondrial protein-coding and rRNA genes. Analyses including the 1st and 2nd positions of all protein-coding genes recovered most of the expected relationships on the order, suborder, superfamily and family level, with three notable exceptions: The gall midge genera Rhopalomyia and Mayetiola (Diptera, Cecidomyiidae) were consistently misplaced in the Hymenoptera; the only Raphidiopteran was placed at the base of the Hymenoptera instead of within the Neuropterida (Neuroptera+Mecoptera); and the non-aculeate genus Evania erroneously grouped as a sister group of Radoszkowskius within the Aculeata (Fig. 2) [74], [75]. As in previous phylogenetic studies, the Hymenoptera were recovered as the most basal of the holometabolous insect orders [75], [76], Diptera and Mecoptera were sister groups and together represented the sister group of the Neuropterida [77], which disagrees with a recent study based on single-copy nuclear genes that revealed the Coleoptera and Strepsiptera to be the closest relatives to the Neuropterida [75]. Including the 3rd positions in the phylogenetic analysis led to the loss of monophyly in the Coleoptera, and an analysis with only the 3rd positions did not recover the Coleoptera or the Lepidoptera as monophyletic clades, and several of the expected relationships below order level were not recovered as monophyletic clades (Fig. S1). A maximum likelihood phylogeny of the two mitochondrial rRNA genes with a subset of 50 taxa recovered the Lepidoptera, Diptera, and Hymenoptera as monophyletic, but not the Coleoptera or many of the relationships on lower taxonomic levels (Fig. 3). Our results agree with an earlier study indicating that Bayesian analyses of 1st and 2nd protein-coding positions are most useful to recover uncontroversial relationships within the Hymenoptera when using mitochondrial genomes [8].


Accelerated evolution of mitochondrial but not nuclear genomes of Hymenoptera: new evidence from crabronid wasps.

Kaltenpoth M, Showers Corneli P, Dunn DM, Weiss RB, Strohm E, Seger J - PLoS ONE (2012)

Maximum likelihood tree inferred from the mitochondrial 12S and 16SrRNA gene sequences of 50 representative taxa from the four major holometabolous insect orders.Branches are color-coded based on order-level taxonomic affiliations (see Fig. 2).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3295772&req=5

pone-0032826-g003: Maximum likelihood tree inferred from the mitochondrial 12S and 16SrRNA gene sequences of 50 representative taxa from the four major holometabolous insect orders.Branches are color-coded based on order-level taxonomic affiliations (see Fig. 2).
Mentions: Bayesian and maximum likelihood analyses were used to reconstruct the phylogeny of holometabolous insects based on mitochondrial protein-coding and rRNA genes. Analyses including the 1st and 2nd positions of all protein-coding genes recovered most of the expected relationships on the order, suborder, superfamily and family level, with three notable exceptions: The gall midge genera Rhopalomyia and Mayetiola (Diptera, Cecidomyiidae) were consistently misplaced in the Hymenoptera; the only Raphidiopteran was placed at the base of the Hymenoptera instead of within the Neuropterida (Neuroptera+Mecoptera); and the non-aculeate genus Evania erroneously grouped as a sister group of Radoszkowskius within the Aculeata (Fig. 2) [74], [75]. As in previous phylogenetic studies, the Hymenoptera were recovered as the most basal of the holometabolous insect orders [75], [76], Diptera and Mecoptera were sister groups and together represented the sister group of the Neuropterida [77], which disagrees with a recent study based on single-copy nuclear genes that revealed the Coleoptera and Strepsiptera to be the closest relatives to the Neuropterida [75]. Including the 3rd positions in the phylogenetic analysis led to the loss of monophyly in the Coleoptera, and an analysis with only the 3rd positions did not recover the Coleoptera or the Lepidoptera as monophyletic clades, and several of the expected relationships below order level were not recovered as monophyletic clades (Fig. S1). A maximum likelihood phylogeny of the two mitochondrial rRNA genes with a subset of 50 taxa recovered the Lepidoptera, Diptera, and Hymenoptera as monophyletic, but not the Coleoptera or many of the relationships on lower taxonomic levels (Fig. 3). Our results agree with an earlier study indicating that Bayesian analyses of 1st and 2nd protein-coding positions are most useful to recover uncontroversial relationships within the Hymenoptera when using mitochondrial genomes [8].

Bottom Line: This effect should result in elevated substitution rates of both nuclear and mitochondrial genes, but to date no extensive comparative study has tested this hypothesis in insects.The mt-genome of P. triangulum is 16,029 bp in size with a mean A+T content of 83.6%, and it encodes the 37 genes typically found in arthropod mt genomes (13 protein-coding, 22 tRNA, and two rRNA genes).Thus, our results suggest that the ancestral parasitic lifestyle of Apocrita is unlikely to be the major cause for the elevated substitution rates observed in hymenopteran mitochondrial genomes.

View Article: PubMed Central - PubMed

Affiliation: Research Group Insect Symbiosis, Max Planck Institute for Chemical Ecology, Jena, Germany. mkaltenpoth@ice.mpg.de

ABSTRACT
Mitochondrial genes in animals are especially useful as molecular markers for the reconstruction of phylogenies among closely related taxa, due to the generally high substitution rates. Several insect orders, notably Hymenoptera and Phthiraptera, show exceptionally high rates of mitochondrial molecular evolution, which has been attributed to the parasitic lifestyle of current or ancestral members of these taxa. Parasitism has been hypothesized to entail frequent population bottlenecks that increase rates of molecular evolution by reducing the efficiency of purifying selection. This effect should result in elevated substitution rates of both nuclear and mitochondrial genes, but to date no extensive comparative study has tested this hypothesis in insects. Here we report the mitochondrial genome of a crabronid wasp, the European beewolf (Philanthus triangulum, Hymenoptera, Crabronidae), and we use it to compare evolutionary rates among the four largest holometabolous insect orders (Coleoptera, Diptera, Hymenoptera, Lepidoptera) based on phylogenies reconstructed with whole mitochondrial genomes as well as four single-copy nuclear genes (18S rRNA, arginine kinase, wingless, phosphoenolpyruvate carboxykinase). The mt-genome of P. triangulum is 16,029 bp in size with a mean A+T content of 83.6%, and it encodes the 37 genes typically found in arthropod mt genomes (13 protein-coding, 22 tRNA, and two rRNA genes). Five translocations of tRNA genes were discovered relative to the putative ancestral genome arrangement in insects, and the unusual start codon TTG was predicted for cox2. Phylogenetic analyses revealed significantly longer branches leading to the apocritan Hymenoptera as well as the Orussoidea, to a lesser extent the Cephoidea, and, possibly, the Tenthredinoidea than any of the other holometabolous insect orders for all mitochondrial but none of the four nuclear genes tested. Thus, our results suggest that the ancestral parasitic lifestyle of Apocrita is unlikely to be the major cause for the elevated substitution rates observed in hymenopteran mitochondrial genomes.

Show MeSH