Phylomitogenomic analyses on collembolan higher taxa with enhanced taxon sampling and discussion on method selection

Abstract

Collembola are a basal group of Hexapoda renowned for both unique morphological characters and significant ecological roles. However, a robust and plausible phylogenetic relationship between its deeply divergent lineages has yet to be achieved. We carried out a mitophylogenomic study based on a so far the most comprehensive mitochondrial genome dataset. Our data matrix contained mitogenomes of 31 species from almost all major families of all four orders, with 16 mitogenomes newly sequenced and annotated. We compared the linear arrangements of genes along mitochondria across species. Then we conducted 13 analyses each under a different combination of character coding, partitioning scheme and heterotachy models, and assessed their performance in phylogenetic inference. Several hypothetical tree topologies were also tested. Mitogenomic structure comparison revealed that most species share the same gene order of putative ancestral pancrustacean pattern, while seven species from Onychiuridae, Poduridae and Symphypleona bear different levels of gene rearrangements, indicating phylogenetic signals. Tomoceroidea was robustly recovered for the first time in the presence of all its families and subfamilies. Monophyly of Onychiuroidea was supported using unpartitioned models alleviating LBA. Paronellidae was revealed polyphyletic with two subfamilies inserted independently into Entomobryidae. Although Entomobryomorpha has not been well supported, more than half of the analyses obtained convincing topologies by placing Tomoceroidea within or near remaining Entomobryomorpha. The relationship between elongate-shaped and sphericalshaped collembolans still remained ambiguous, but Neelipleona tend to occupy the basal position in most trees. This study showed that mitochondrial genomes could provide important information for reconstructing the relationships among Collembola when suitable analytical approaches are implemented. Of all the data refining and model selecting schemes used in this study, the combination of nucleotide sequences, partitioning model and

Re-Evaluating the Internal Phylogenetic Relationships of Collembola by Means of Mitogenome Data

“…Leo and colleagues [2] proposed Neelipleona as the earliest diverging lineage in Collembola, although not all analyses converged to the same result, while Poduromorpha was recovered as the sister taxon to the more derived Entomobryomorpha + Symphypleona ( Figure 1F). Sun and colleagues [14], in turn, support a scenario similar to that proposed by [11] ( Figure 1C). A third relevant study [15], focusing on internal relationships among species of a single genus, did not address inter-ordinal relationships but provided a wealth of primary data.…”

“…Nuclear genomic data have been used to unravel deep-level phylogenetic relationships in hexapods, including early diverging lineages [13], but the limited number of representatives for each major group does not currently allow a thorough investigation of internal relationships at lower taxonomic levels. In this context, complete mitochondrial genomes appear to be a suitable marker, and their informativeness in terms of infraorder relationships among springtails has been assessed in certain studies [2,14,15]. In consequence of the factors of uniparental inheritance, lack of recombination, haploidy, technical feasibility of sequencing using NGS technologies and occurrence in almost all Eukaryota, complete mitochondrial genomes have now emerged as a very popular molecular marker in phylogenetic studies.…”

“…Competing hypotheses for Collembola phylogeny obtained using molecular markers and listed in chronological order. (A) Traditional view; (B) Based on ribosomal markers [9]; (C) Based on ribosomal [11] and mtDNA protein coding genes [14]; (D) Based on 16S, cox1 and 28S markers [10]; (E) Based on ribosomal markers [12]; (F) Based on mitochondrial protein coding genes [2]. Competing hypotheses for Collembola phylogeny obtained using molecular markers and listed in chronological order.…”

The complete mitochondrial genome of the springtail Allacma fusca, the internal phylogenetic relationships and gene order of Symphypleona

“…It encodes for the set of 37 genes (13 PCGs, 22 tRNAs, and 2 rRNAs) commonly observed in metazoan mitochondrial genomes. Gene arrangement differs from both the ancestral pancrustacean gene order and from alternative gene orders previously described in springtails (Boore et al 1998;Carapelli et al 2007;Leo et al 2019a;Sun et al 2020). Allacma fusca shares with the other two representatives of family Sminthuridae, Lipotrix lubbocki and Sminthurus viridis, two translocations (trnD and exchange between trnT and trnP) that may be tentatively regarded as synapomorphies for the family.…”

“…Traditionally, this taxon was grouped with Neelipleona because of the shared spherical body shape in Symphypleona sensu lato. Despite this similar morphological feature, recent molecular evidence established that Symphypleona s.s. are more closely related to springtails characterized by an elongated body (Entomobryomorpha and Poduromorpha) than to Neelipleona, supporting this latter as the basal group of springtails (Leo et al 2019a(Leo et al , 2019bSun et al 2020). However, knowledge on the systematic position of families and subfamilies within the order is still limited due, among other issues, to the restricted number of mitogenomes available.…”