Dataset Information

Evolutionary dynamics of the mitochondrial genome in the evaniomorpha (hymenoptera)—a group with an intermediate rate of gene rearrangement.

ABSTRACT: We determined the complete mitochondrial (mt) genomes of three evaniomorph species, Ceraphron sp. (Ceraphronoidea), Gasteruption sp. (Evanioidea), and Orthogonalys pulchella (Trigonalyoidea) as well as the nearly complete mt genome from another evaniomorph species, Megalyra sp. (Megalyroidea). Each of them possesses dramatic gene rearrangements, including protein-coding or rRNA genes. Gene inversions were identified in all of these mt genomes; for example, the two rRNA genes have inverted and moved into the nad2-cox1 junction in the Megalyra sp. mt genome. In addition, we found two copies of a 10-bp complementary repeat at the beginning of rrnS and at the end of trnL(2) in the Gasteruption sp. mt genome, consistent with recombination as the possible mechanism for gene inversion and long-range movement. Although each of the genomes contains a number of repeats of varying size, there was no consistent association of the size or number of repeats with the extent or type of gene rearrangement. The breakpoint distance analysis showed the Evaniomorpha has an intermediate rate of gene rearrangement. Sequence-based phylogenetic analyses of 13 protein-coding and 2 rRNA genes in 22 hymenopteran taxa recovered a paraphyletic Evaniomorpha with the Aculeata nested within it. Within the Evaniomorpha, our analyses confirmed the Trigonalyoidea + Megalyroidea as the sister group to the Aculeata and recovered a novel clade, Ceraphronoidea + Evanioidea. In contrast to previous hymenopteran phylogenetic studies, the internal relationships of the Evaniomorpha were highly supported and robust to the variation of alignment approach and phylogenetic inference approach.

SUBMITTER: Mao M

PROVIDER: S-EPMC4122943 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Evolutionary dynamics of the mitochondrial genome in the evaniomorpha (hymenoptera)—a group with an intermediate rate of gene rearrangement.

Mao Meng M Gibson Tracey T Dowton Mark M

Genome biology and evolution 20140701 7

We determined the complete mitochondrial (mt) genomes of three evaniomorph species, Ceraphron sp. (Ceraphronoidea), Gasteruption sp. (Evanioidea), and Orthogonalys pulchella (Trigonalyoidea) as well as the nearly complete mt genome from another evaniomorph species, Megalyra sp. (Megalyroidea). Each of them possesses dramatic gene rearrangements, including protein-coding or rRNA genes. Gene inversions were identified in all of these mt genomes; for example, the two rRNA genes have inverted and mo ...[more]

PMID: 25115010

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Project description:Studies of mitochondrial genomes have a wide range of applications in phylogeny, population genetics, and evolutionary biology. In this study, we sequenced and analyzed the mitochondrial genome of Ooencyrtusplautus Huang & Noyes, 1994 (Hymenoptera, Encyrtidae). The nearly complete mitogenome of O.plautus was 15,730 bp in size, including 13 PCGs (protein-coding genes), 22 tRNAs, 2 rRNAs, and a nearly complete control region. The nucleotide composition was significantly biased toward adenine and thymine, with an A + T content of 84.6%. We used the reference sequence of Chouioiacunea and calculated the Ka/Ks ratio for each set of PCGs. The highest value of the Ka/Ks ratio within 13 PCGs was found in nad2 with 1.1, suggesting that they were subjected to positive selection. This phenomenon was first discovered in Encyrtidae. Compared with other encyrtid mitogenomes, a translocation of trnW was found in O.plautus, which was the first of its kind to be reported in Encyrtidae. Comparing with ancestral arrangement pattern, wasps reflect extensive gene rearrangements. Although these insects have a high frequency of gene rearrangement, species from the same family and genus tend to have similar gene sequences. As the number of sequenced mitochondrial genomes in Chalcidoidea increases, we summarize some of the rules of gene rearrangement in Chalcidoidea, that is four gene clusters with frequent gene rearrangements. Ten mitogenomes were included to reconstruct the phylogenetic trees of Encyrtidae based on both 13 PCGs (nucleotides of protein coding genes) and AA matrix (amino acids of protein coding genes) using the maximum likelihood and Bayesian inference methods. The phylogenetic tree reconstructed by Bayesian inference based on AA data set showed that Aenasiusarizonensis and Metaphycuseriococci formed a clade representing Tetracneminae. The remaining six species formed a monophyletic clade representing Encyrtinae. In Encyrtinae, Encyrtus forms a monophyletic clade as a sister group to the clade formed by O.plautus and Diaphorencyrtusaligarhensis. Encyrtussasakii and Encyrtusrhodooccisiae were most closely related species in this monophyletic clade. In addition, gene rearrangements can provide a valuable information for molecular phylogenetic reconstruction. These results enhance our understanding of phylogenetic relationships among Encyrtidae.

Project description:BackgroundMitochondrial genomic (mitogenomic) reorganizations are rarely found in closely-related animals, yet drastic reorganizations have been found in the Ranoides frogs. The phylogenetic relationships of the three major ranoid taxa (Natatanura, Microhylidae, and Afrobatrachia) have been problematic, and mitogenomic information for afrobatrachians has not been available. Several molecular models for mitochondrial (mt) gene rearrangements have been proposed, but observational evidence has been insufficient to evaluate them. Furthermore, evolutionary trends in rearranged mt genes have not been well understood. To gain molecular and phylogenetic insights into these issues, we analyzed the mt genomes of four afrobatrachian species (Breviceps adspersus, Hemisus marmoratus, Hyperolius marmoratus, and Trichobatrachus robustus) and performed molecular phylogenetic analyses. Furthermore we searched for two evolutionary patterns expected in the rearranged mt genes of ranoids.ResultsExtensively reorganized mt genomes having many duplicated and rearranged genes were found in three of the four afrobatrachians analyzed. In fact, Breviceps has the largest known mt genome among vertebrates. Although the kinds of duplicated and rearranged genes differed among these species, a remarkable gene rearrangement pattern of non-tandemly copied genes situated within tandemly-copied regions was commonly found. Furthermore, the existence of concerted evolution was observed between non-neighboring copies of triplicated 12S and 16S ribosomal RNA regions.ConclusionsPhylogenetic analyses based on mitogenomic data support a close relationship between Afrobatrachia and Microhylidae, with their estimated divergence 100 million years ago consistent with present-day endemism of afrobatrachians on the African continent. The afrobatrachian mt data supported the first tandem and second non-tandem duplication model for mt gene rearrangements and the recombination-based model for concerted evolution of duplicated mt regions. We also showed that specific nucleotide substitution and compositional patterns expected in duplicated and rearranged mt genes did not occur, suggesting no disadvantage in employing these genes for phylogenetic inference.

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Project description:BackgroundThe primary energy-producing pathway in eukaryotic cells, the oxidative phosphorylation (OXPHOS) system, comprises proteins encoded by both mitochondrial and nuclear genes. To maintain the function of the OXPHOS system, the pattern of substitutions in mitochondrial and nuclear genes may not be completely independent. It has been suggested that slightly deleterious substitutions in mitochondrial genes are compensated by substitutions in the interacting nuclear genes due to positive selection. Among the four largest insect orders, Coleoptera (beetles), Hymenoptera (sawflies, wasps, ants, and bees), Diptera (midges, mosquitoes, and flies) and Lepidoptera (moths and butterflies), the mitochondrial genes of Hymenoptera exhibit an exceptionally high amino acid substitution rate while the evolution of nuclear OXPHOS genes is largely unknown. Therefore, Hymenoptera is an excellent model group for testing the hypothesis of positive selection driving the substitution rate of nuclear OXPHOS genes. In this study, we report the evolutionary rate of OXPHOS genes in Hymenoptera and test for evidence of positive selection in nuclear OXPHOS genes of Hymenoptera.ResultsOur analyses revealed that the amino acid substitution rate of mitochondrial and nuclear OXPHOS genes in Hymenoptera is higher than that in other studied insect orders. In contrast, the amino acid substitution rate of non-OXPHOS genes in Hymenoptera is lower than the rate in other insect orders. Overall, we found the dN/dS ratio of the nuclear OXPHOS genes to be higher in Hymenoptera than in other insect orders. However, nuclear OXPHOS genes with high dN/dS ratio did not always exhibit a high amino acid substitution rate. Using branch-site and site model tests, we identified various codon sites that evolved under positive selection in nuclear OXPHOS genes.ConclusionsOur results showed that nuclear OXPHOS genes in Hymenoptera are evolving faster than the genes in other three insect orders. The branch test suggested that while some nuclear OXPHOS genes in Hymenoptera show a signature of positive selection, the pattern is not consistent across all nuclear OXPHOS genes. As only few codon sites were under positive selection, we suggested that positive selection might not be the only factor contributing to the rapid evolution of nuclear OXPHOS genes in Hymenoptera.

Dataset Information

Evolutionary dynamics of the mitochondrial genome in the evaniomorpha (hymenoptera)—a group with an intermediate rate of gene rearrangement.

Publications

Evolutionary dynamics of the mitochondrial genome in the evaniomorpha (hymenoptera)—a group with an intermediate rate of gene rearrangement.

Similar Datasets

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