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Phylogenetic analysis of the true water bugs (Insecta: Hemiptera: Heteroptera: Nepomorpha): evidence from mitochondrial genomes.

ABSTRACT: BACKGROUND:The true water bugs are grouped in infraorder Nepomorpha (Insecta: Hemiptera: Heteroptera) and are of great economic importance. The phylogenetic relationships within Nepomorpha and the taxonomic hierarchies of Pleoidea and Aphelocheiroidea are uncertain. Most of the previous studies were based on morphological characters without algorithmic assessment. In the latest study, the molecular markers employed in phylogenetic analyses were partial sequences of 16S rDNA and 18S rDNA with a total length about 1 kb. Up to now, no mitochondrial genome of the true water bugs has been sequenced, which is one of the largest data sets that could be compared across animal taxa. In this study we analyzed the unresolved problems in Nepomorpha using evidence from mitochondrial genomes. RESULTS:Nine mitochondrial genomes of Nepomorpha and five of other hemipterans were sequenced. These mitochondrial genomes contain the commonly found 37 genes without gene rearrangements. Based on the nucleotide sequences of mt-genomes, Pleoidea is not a member of the Nepomorpha and Aphelocheiroidea should be grouped back into Naucoroidea. Phylogenetic relationships among the superfamilies of Nepomorpha were resolved robustly. CONCLUSION:The mt-genome is an effective data source for resolving intraordinal phylogenetic problems at the superfamily level within Heteroptera. The mitochondrial genomes of the true water bugs are typical insect mt-genomes. Based on the nucleotide sequences of the mt-genomes, we propose the Pleoidea to be a separate heteropteran infraorder. The infraorder Nepomorpha consists of five superfamilies with the relationships (Corixoidea + ((Naucoroidea + Notonectoidea) + (Ochteroidea + Nepoidea))).

SUBMITTER: Hua J

PROVIDER: S-EPMC2711072 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Phylogenetic analysis of the true water bugs (Insecta: Hemiptera: Heteroptera: Nepomorpha): evidence from mitochondrial genomes.

Hua Jimeng J Li Ming M Dong Pengzhi P Cui Ying Y Xie Qiang Q Bu Wenjun W

BMC evolutionary biology 20090615

<h4>Background</h4>The true water bugs are grouped in infraorder Nepomorpha (Insecta: Hemiptera: Heteroptera) and are of great economic importance. The phylogenetic relationships within Nepomorpha and the taxonomic hierarchies of Pleoidea and Aphelocheiroidea are uncertain. Most of the previous studies were based on morphological characters without algorithmic assessment. In the latest study, the molecular markers employed in phylogenetic analyses were partial sequences of 16S rDNA and 18S rDNA ...[more]

PMID: 19523246

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Project description:BackgroundMost previous studies of morphological and molecular data have consistently supported the monophyly of the true water bugs (Hemiptera: Nepomorpha). An exception is a recent study by Hua et al. (BMC Evol Biol 9: 134, 2009) based on nine nepomorphan mitochondrial genomes. In the analysis of Hua et al. (BMC Evol Biol 9: 134, 2009), the water bugs in the group Pleoidea formed the sister group to a clade that consisted of Nepomorpha (the remaining true water bugs) + Leptopodomorpha (shore bugs) + Cimicomorpha (assassin bugs and relatives) + Pentatomomorpha (stink bugs and relatives), thereby suggesting that fully aquatic hemipterans evolved independently at least twice. Based on these results, Hua et al. (BMC Evol Biol 9: 134, 2009) elevated the Pleoidea to a new infraorder, the Plemorpha.ResultsOur reanalysis suggests that the lack of support for the monophyly of the true water bugs (including Pleoidea) by Hua et al. (BMC Evol Biol 9: 134, 2009) likely resulted from inadequate taxon sampling. In particular, long-branch attraction (LBA) between the distant outgroup taxa and Pleoidea, as well as LBA among taxa in the ingroup, made Nepomorpha appear to be polyphyletic. We used three complementary strategies to test and alleviate the effects of LBA: (1) the removal of distant outgroups from the analysis; (2) the addition of closely related outgroups; and (3) the addition of a mitochondrial genome from a second family of Pleoidea. We also performed likelihood-ratio tests to examine the support for monophyly of Nepomorpha with different combinations of taxa included in the analysis. Furthermore, we found that specimens of Helotrephes sp. were misidentified as Paraplea frontalis (Fieber, 1844) by Hua et al. (BMC Evol Biol 9: 134, 2009).ConclusionsAll analyses that included the addition of more taxa significantly and consistently supported the placement of Pleoidea within the Nepomorpha (i.e., supported the monophyly of the traditional true water bugs). Our analyses further support a close relationship between Notonectoidea and Pleoidea within Nepomorpha, and the superfamilies Nepoidea, Ochteroidea, Naucoroidea, and Pleoidea are resolved as monophyletic in all trees with strong support. Our results also confirmed that monophyly of Nepomorpha clearly is not refuted by the mitochondrial genome data.

Project description:BackgroundNucleotide sequences and the gene arrangements of mitochondrial genomes are effective tools for resolving phylogenetic problems. Hemipteroid insects are known to possess highly reorganized mitochondrial genomes, but in the suborder Heteroptera (Insecta: Hemiptera), there was only one complete mitochondrial genome sequenced without gene rearrangement and the phylogeny of infraorder Pentatomomorpha in Heteroptera was still uncertain.ResultsFifteen mitochondrial genomes of the suborder Heteroptera were sequenced. Gene rearrangements were found as follows: 1) tRNA-I and tRNA-Q switched positions in Aradidae, 2) tRNA-T and tRNA-P switched positions in Largidae and Pyrrhocoridae. Two recombination events were found in Alydidae and Malcidae. The other mt-genomes were organized in the same way as observed in Drosophila yakuba. The phylogenetic analyses of infraorder Pentatomomorpha based on the nucleotide sequence raised the hypothesis of (Aradoidea + (Pentatomoidea + (Pyrrhocoroidea + (Lygaeoidea + Coreoidea)))). The rearrangement of tRNA-T and tRNA-P also linked Largidae and Pyrrhocoridae together. Furthermore, the conserved sequence block in the unusual intergenic spacers between tRNA-H and ND4 favored the monophyly of Lygaeoidea. Tetranucleotide ATCA was inferred to be the initiation codon of ND2 in Cydnidae. No correlation was found between the rates of nucleotide substitution and gene rearrangement. CG content was significantly correlated with the nucleotide substitution rate of each gene. For ND1, there was a positive correlation (P < 0.01) between amino acids variations and hydrophobicity, but a negative correlation (P < 0.01) for ND6. No conserved sequence was found among the control regions and these regions were not always the most AT-rich region of the mt-genome.ConclusionHeteropteran insects are extremely complex groups worthy of further study because of the unusual tetranucleotide initiation codon and their great mt-genomic diversity, including gene rearrangements and recombinations. The mt-genome is a powerful molecular marker for resolving phylogeny at the level of the superfamily and family. Gene rearrangements were not correlated with nucleotide substitution rates. CG content variation caused the different evolutionary patterns among genes. For ND1, in many polar or nonpolar regions the specific identity of the amino acid residues might be more important than maintaining the polarity of these regions, while the opposite is true for ND6. Most sequences of the control regions did not appear to be important for regulatory functions. Finally, we suggest that the term "AT-rich regions" should not be used.

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Phylogenetic analysis of the true water bugs (Insecta: Hemiptera: Heteroptera: Nepomorpha): evidence from mitochondrial genomes.

Publications

Phylogenetic analysis of the true water bugs (Insecta: Hemiptera: Heteroptera: Nepomorpha): evidence from mitochondrial genomes.

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