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Open Access Highly Accessed Research article

Molecular phylogenetic analyses support the monophyly of Hexapoda and suggest the paraphyly of Entognatha

Go Sasaki14, Keisuke Ishiwata125, Ryuichiro Machida3, Takashi Miyata1 and Zhi-Hui Su12*

Author Affiliations

1 JT Biohistory Research Hall, 1-1 Murasaki-cho, Takatsuki, Osaka 569–1125, Japan

2 Department of Biological Sciences, Graduate School of Science, Osaka University, Osaka 560-0043, Japan

3 Sugadaira Montane Research Center, University of Tsukuba, Sugadaira Kogen, Ueda, Nagano 386-2204, Japan

4 Present address: School of Medicine, Kumamoto University, Kumamoto 860-8556, Japan

5 Present address: Division of Functional Genomics, Advanced Science Research Center, Kanazawa University, Kanazawa 920-0934, Japan

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BMC Evolutionary Biology 2013, 13:236  doi:10.1186/1471-2148-13-236

Published: 31 October 2013

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.

Keywords:
Pancrustacea; Hexapoda; Entognatha; Molecular phylogeny; RNA polymerase gene; DNA polymerase gene