Abstract

BackgroundMolecular 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.ResultsPhylogenetic 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.ConclusionThis 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.

Highlights

  • Molecular phylogenetic analyses have revealed that Hexapoda and Crustacea form a common clade, which is widely accepted among zoologists; the origin of Hexapoda remains unresolved

  • The origin of Hexapoda is still an open question, and the phylogenetic relationships among the basal hexapod lineages remain unclear despite the considerable research efforts that have conducted in attempts to resolve them

  • Sequence and alignment dataset In this study, the nuclear genes encoding DNA polymerase delta catalytic subunit (DPD1), RNA polymerase II largest subunit (RPB1), and RNA polymerase II second largest subunit (RPB2) were amplified and sequenced in 14 arthropods, which consisted of six species of Entognatha, six species of Crustacea, one myriapod, and one chelicerate (Additional file 1)

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Summary

Introduction

Molecular phylogenetic analyses have revealed that Hexapoda and Crustacea form a common clade (the Pancrustacea), which is widely accepted among zoologists; the origin of Hexapoda remains unresolved. 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. Hexapods are traditionally considered to be a monophyletic group [21], Nardi and colleagues [22,23] presented phylogenetic trees based on mitochondrial DNA sequences that indicated that collembolans and diplurans branched off much earlier than the separation between ectognathans and some crustaceans such as branchiopods and malacostracans, implying that hexapods are not monophyletic (Figure 1B) In support of this hypothesis, Cook et al [24] analyzed mitogenomic data and suggested that hexapods and crustaceans may be mutually paraphyletic. These contradictory results have currently called much attention to the problem of the origin, phylogeny, and evolution of hexapods, and to interpretations of the adaptation of insects to life on land

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