Collembolan Transcriptomes Highlight Molecular Evolution of Hexapods and Provide Clues on the Adaptation to Terrestrial Life

PLoS One. 2015 Jun 15;10(6):e0130600. doi: 10.1371/journal.pone.0130600. eCollection 2015.

Abstract

Background: Collembola (springtails) represent a soil-living lineage of hexapods in between insects and crustaceans. Consequently, their genomes may hold key information on the early processes leading to evolution of Hexapoda from a crustacean ancestor.

Method: We assembled and annotated transcriptomes of the Collembola Folsomia candida and Orchesella cincta, and performed comparative analysis with protein-coding gene sequences of three crustaceans and three insects to identify adaptive signatures associated with the evolution of hexapods within the pancrustacean clade.

Results: Assembly of the springtail transcriptomes resulted in 37,730 transcripts with predicted open reading frames for F. candida and 32,154 for O. cincta, of which 34.2% were functionally annotated for F. candida and 38.4% for O. cincta. Subsequently, we predicted orthologous clusters among eight species and applied the branch-site test to detect episodic positive selection in the Hexapoda and Collembola lineages. A subset of 250 genes showed significant positive selection along the Hexapoda branch and 57 in the Collembola lineage. Gene Ontology categories enriched in these genes include metabolism, stress response (i.e. DNA repair, immune response), ion transport, ATP metabolism, regulation and development-related processes (i.e. eye development, neurological development).

Conclusions: We suggest that the identified gene families represent processes that have played a key role in the divergence of hexapods within the pancrustacean clade that eventually evolved into the most species-rich group of all animals, the hexapods. Furthermore, some adaptive signatures in collembolans may provide valuable clues to understand evolution of hexapods on land.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Physiological / genetics
  • Animals
  • Arthropods / classification*
  • Arthropods / genetics*
  • Base Sequence
  • Biological Evolution
  • Evolution, Molecular
  • High-Throughput Nucleotide Sequencing
  • Phylogeny
  • Sequence Analysis, DNA
  • Transcriptome / genetics

Associated data

  • BioProject/PRJNA211850
  • BioProject/PRJNA211851
  • SRA/SRR935329
  • SRA/SRR935330

Grants and funding

This research was supported by a grant from the Dutch Biotechnology based Ecologically Balanced Sustainable Industrial Consortium (BE-BASIC), grant number F08.001.03, http://www.be-basic.org. In addition, D. Roelofs is supported by the European Union FP7 large scale intergration Project ‘Sustainable Nanotechnologies (SUN)’, Grant number 604305. Keygene NV provided support in the form of salaries for E. Datema, but did not have any additional role in the study design, data collection and analysis, decision to publish or preparation of the manuscript.