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.
Highlights
Mitochondrial genes have been used extensively for phylogenetic studies in insects
An additional problem with mitochondrial sequences is that differences in mitochondrial evolutionary rates among insect lineages can cause long-branch attraction problems [3] that result in unrelated taxa with high substitution rates erroneously grouping together in phylogenetic trees [4]
While the protein-coding and rRNA genes were conserved in positions and orientations relative to the inferred ancestral arrangement in insect mitochondrial genomes [58], five translocations of tRNAs were detected (tRNA-Met/-Gln; tRNATrp; tRNA-Glu/-Ser(AGN); tRNA-Pro/-Thr; tRNA-Ile)
Summary
Mitochondrial genes have been used extensively for phylogenetic studies in insects. Their generally high substitution rates render them especially useful to resolve the relationships among closely related taxa [1]. Using complete mitochondrial genome sequences as well as four different nuclear gene datasets, we reconstructed the phylogenetic relationships among the four largest holometabolous insect orders (Coleoptera, Hymenoptera, Diptera, and Lepidoptera), and we compared the substitution rates of mitochondrial and nuclear genes among the orders.
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