Abstract
BackgroundMitochondrial genome (mt-genome) data can potentially return artefactual relationships in the higher-level phylogenetic inference of insects due to the biases of accelerated substitution rates and compositional heterogeneity. Previous studies based on mt-genome data alone showed a paraphyly of Cimicomorpha (Insecta, Hemiptera) due to the positions of the families Tingidae and Reduviidae rather than the monophyly that was supported based on morphological characters, morphological and molecular combined data and large scale molecular datasets. Various strategies have been proposed to ameliorate the effects of potential mt-genome biases, including dense taxon sampling, removal of third codon positions or purine-pyrimidine coding and the use of site-heterogeneous models. In this study, we sequenced the mt-genomes of five additional Tingidae species and discussed the compositional and mutational rate heterogeneity in mt-genomes and its effect on the phylogenetic inferences of Cimicomorpha by implementing the bias-reduction strategies mentioned above.ResultsHeterogeneity in nucleotide composition and mutational biases were found in mt protein-coding genes, and the third codon exhibited high levels of saturation. Dense taxon sampling of Tingidae and Reduviidae and the other common strategies mentioned above were insufficient to recover the monophyly of the well-established group Cimicomorpha. When the sites with weak phylogenetic signals in the dataset were removed, the remaining dataset of mt-genomes can support the monophyly of Cimicomorpha; this support demonstrates that mt-genomes possess strong phylogenetic signals for the inference of higher-level phylogeny of this group. Comparison of the ratio of the removal of amino acids for each PCG showed that ATP8 has the highest ratio while CO1 has the lowest. This pattern is largely congruent with the evolutionary rate of 13 PCGs that ATP8 represents the highest evolutionary rate, whereas CO1 appears to be the lowest. Notably, the value of Ka/Ks ratios of all PCGs is less than 1, indicating that these genes are likely evolving under purifying selection.ConclusionsOur results demonstrate that mt-genomes have sites with strong phylogenetic signals for the inference of higher-level phylogeny of Cimicomorpha. Consequently, bioinformatic approaches to removing sites with weak phylogenetic signals in mt-genome without relying on an a priori tree topology would greatly improve this field.
Highlights
Mitochondrial genome data can potentially return artefactual relationships in the higher-level phylogenetic inference of insects due to the biases of accelerated substitution rates and compositional heterogeneity
General features of mt-genomes of five newly sequenced species of Tingidae In this study, we sequenced the mt-genomes of five species of Tingidae (Additional file 1), including one complete (Trachypeplus jacobsoni) and four nearly complete (Cysteochila chiniana, Dictyla platyoma, Metasalis populi, and Tingis cardui) mt-genomes
In the five newly sequenced Tingidae mt-genomes, all proteincoding genes (PCGs) initiated with ATN as the start codon, except for the ATP6 gene, which was only found in Cysteochila chiniana and started with GTG
Summary
Mitochondrial genome (mt-genome) data can potentially return artefactual relationships in the higher-level phylogenetic inference of insects due to the biases of accelerated substitution rates and compositional heterogeneity. Widely utilized in phylogenetic analyses, potential biases such as high percentages of AT content, base-compositional heterogeneity between lineages, and high evolutionary rates have all been documented in insect mt-genomes [1,2,3,4] These anomalous characteristics frequently limit their applicability in higher-level phylogenetic reconstruction of insects, leading to an incongruence with morphological and nuclear data [1,2,3,4]. The phenomena caused by these potential biases have attracted an increasing amount of attention in studies of some groups, such as Coleoptera, Thysanoptera, Psocodea, Sternorrhyncha (Hemiptera), Strepsiptera, Neuropterida and Hymenoptera [1,2,3, 7,8,9,10,11,12,13,14,15,16,17,18], showing that compositional heterogeneity is pervasive If these characteristics were shared by unrelated lineages, the apparent convergent evolution may erode a genuine phylogenetic signal [6]. Accelerated evolutionary rates and rate variation across lineages can increase susceptibility to systematic errors, such as long-branch attraction (LBA) [19,20,21]
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