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

Abstract

BackgroundCollembola (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.MethodWe 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.ResultsAssembly 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).ConclusionsWe 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.

Chemical signaling and insect attraction is a conserved trait in yeasts

“…By the Pennsylvanian, ca. 320 mya, pterygot insects were present, including further derived holometabolous insects (Engel & Grimaldi, 2004;Faddeeva et al, 2015;Knecht, Engel, & Benner, 2011;Misof et al, 2014;Nel et al, 2013).…”

Developmental expression and evolution of hexamerin and haemocyanin fromFolsomia candida(Collembola)

“…We explored haemocyanin and hexamerin sequences in basal hexapods (Collembola, Diplura and Protura) by PCR cloning, rapid amplification of cDNA ends (RACE) and mining from transcriptomes/genomes (our unpublished data; Misof et al , ; Faddeeva et al , ). In total, we report 17 new sequences here (with nine complete sequences shown in bold in Table ): three collembolan hexamerins, 10 dipluran hexamerins and four collembolan haemocyanins (Table ).…”

“…In total, we report 17 new sequences here (with nine complete sequences shown in bold in Table ): three collembolan hexamerins, 10 dipluran hexamerins and four collembolan haemocyanins (Table ). Amongst these sequences, two collembolan hexamerins [Fca(DK)Hx1 from F. candida (Denmark strain, DK; hexamerin, Hx) and Fca(SH)Hx1 from F. candida (Shanghai strain, SH)] and eight dipluran hexamerins (LweHx2, LweHx3, LweHx4 and LweHx5 from Lepidocampa weberi ; OjaHx4 from Occasjapyx japonicus ; OsiHx1, OsiHx2 and OsiHx3 from Octostigma sinensis ) are totally new, whereas the others from Collembola and Diplura were previously predicted as haemocyanins, haemocyanin‐like or hexamerin‐like in published transcriptomes (Misof et al , ; Faddeeva et al , ). In this study, we validated and re‐annotated these sequences as haemocyanin 1 (Hc1), haemocyanin 2 (Hc2) and hexamerin (Hx), respectively, according to the results of phylogenetic analysis (Table ).…”

“…We did not find any other hexamerins from these two strains of F . candida despite comprehensively screening their transcriptomes and genomes (Misof et al , ; Faddeeva et al , ; our unpublished data) and conducting PCR amplification of samples at different developmental stages.…”

“…We explored haemocyanin and hexamerin sequences in basal hexapods (Collembola, Diplura and Protura) by PCR cloning, rapid amplification of cDNA ends (RACE) and mining from transcriptomes/genomes (our unpublished data; Misof et al, 2014;Faddeeva et al, 2015). In total, we report 17 new sequences here (with nine complete sequences shown in bold in Table 1): three collembolan hexamerins, 10 dipluran hexamerins and four collembolan haemocyanins (Table 1) (Misof et al, 2014;Faddeeva et al, 2015). In this study, we validated and re-annotated these sequences as haemocyanin 1 (Hc1), haemocyanin 2 (Hc2) and hexamerin (Hx), respectively, according to the results of phylogenetic analysis (Table 1).…”