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Molecular Phylogenetic Analyses Support the Monophyly of Hexapoda and Suggest the Paraphyly of Entognatha

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Molecular Phylogenetic Analyses Support the Monophyly of Hexapoda and Suggest the Paraphyly of Entognatha

Go Sasaki et al. BMC Evol Biol.

Abstract

Background: Molecular phylogenetic analyses have revealed that Hexapoda and Crustacea form a common clade (the Pancrustacea), which is now widely accepted among zoologists; however, the origin of Hexapoda remains unresolved. The main problems are the unclear relationships among the basal hexapod lineages, Protura (proturans), Collembola (springtails), Diplura (diplurans), and Ectognatha (bristletails, silverfishes, and all winged insects). Mitogenomic analyses have challenged hexapod monophyly and suggested the reciprocal paraphyly of Hexapoda and Crustacea, whereas studies based on nuclear molecular data support the monophyletic origin of hexapods. Additionally, there are significant discrepancies with respect to these issues between the results of morphological and molecular studies. To investigate these problems, we performed phylogenetic analyses of Pancrustacea based on the protein sequences of three orthologous nuclear genes encoding the catalytic subunit of DNA polymerase delta and the largest and second largest subunits of RNA polymerase II from 64 species of arthropods, including representatives of all hexapod orders.

Results: Phylogenetic analyses were conducted based on the inferred amino acid (aa) sequences (~3400 aa in total) of the three genes using the maximum likelihood (ML) method and Bayesian inference. Analyses were also performed with additional datasets generated by excluding long-branch taxa or by using different outgroups. These analyses all yielded essentially the same results. All hexapods were clustered into a common clade, with Branchiopoda as its sister lineage, whereas Crustacea was paraphyletic. Within Hexapoda, the lineages Ectognatha, Palaeoptera, Neoptera, Polyneoptera, and Holometabola were each confirmed to be monophyletic with robust support, but monophyly was not supported for Entognatha (Protura + Collembola + Diplura), Ellipura (Protura + Collembola), or Nonoculata (Protura + Diplura). Instead, our results showed that Protura is the sister lineage to all other hexapods and that Diplura or Diplura + Collembola is closely related to Ectognatha.

Conclusion: This is the first study to include all hexapod orders in a phylogenetic analysis using multiple nuclear protein-coding genes to investigate the phylogeny of Hexapoda, with an emphasis on Entognatha. The results strongly support the monophyletic origin of hexapods but reject the monophyly of Entognatha, Ellipura, and Nonoculata. Our results provided the first molecular evidence in support of Protura as the sister group to other hexapods. These findings are expected to provide additional insights into the origin of hexapods and the processes involved in the adaptation of insects to life on land.

Figures

Figure 1
Figure 1
The major hypotheses of the basal hexapod relationships proposed in recent studies. (A) Traditional view based on morphology [20,49]. (B) Based on mitogenomic data [22,23]. (C) Based on fossil data [32], comparative embryological evidence [33,34], morphological data [28,35], and some molecular sequences (EF-1α, EF-2, and RAN polymerase II) [36]. (D) Based on nuclear molecular data [7,8,29,30,37].
Figure 2
Figure 2
The ML tree of pancrustaceans inferred from the amino acid sequences of DPD1, RPB1, and RPB2. The branch lengths were calculated from the concatenated alignment of the three protein sequences. Bootstrap values and posterior probabilities are shown at nodes. Dot-marked nodes: bootstrap value > 90%, posterior probability = 1.00. Circle-marked nodes: bootstrap value 70%-90%, posterior probability = 1.00 (except node 59). Internal branches drawn as dotted lines: not supported by Bayesian analysis.
Figure 3
Figure 3
Phylogenetic tree of Hexapoda using crustaceans as outgroups. (A) With collembolans. (B) Without collembolans. Phylogenetic analyses were performed with RAxML and MrBayes. The bootstrap value and posterior probability are shown at each node. The topologies of Ectognatha are omitted in this tree. For the details of these analyses and the original trees, see Additional files 8, 9, 10 and 11.

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