Mitochondrial Genome Diversity in Collembola: Phylogeny, Dating and Gene Order

Abstract

Collembola (springtails) are an early diverging class of apterygotes, and mark the first substantial radiation of hexapods on land. Despite extensive work, the relationships between major collembolan lineages are still debated and, apart from the Early Devonian fossil Rhyniella praecursor, which demonstrates their antiquity, the time frame of springtail evolution is unknown. In this study, we sequence two new mitochondrial genomes and reanalyze all known Collembola mt-genomes, including selected metagenomic data, to produce an improved phylogenetic hypothesis for the group, develop a tentative time frame for their differentiation, and provide a comprehensive overview of gene order diversity. Our analyses support most taxonomically recognized entities. We find support for an Entomobryomorpha + Symphypleona clade, while the position of Neelipleona could not be assessed with confidence. A Silurian time frame for their basal diversification is recovered, with an indication that divergence times may be fairly old overall. The distribution of mitochondrial gene order indicates the pancrustacean arrangement as plesiomorphic and dominant in the group, with the exception of the family Onychiuridae. We distinguished multiple instances of different arrangements in individual genomes or small clusters. We further discuss the opportunities and drawbacks associated with the inclusion of metagenomic data in a classic study on mitochondrial genome diversity.

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

“…All these gene rearrangements occur in tRNA genes but none in PCGs, as also commonly found in insects [22]. Synapomorphic gene rearrangements were observed on the familial level, which is in line with previous studies in Collembola and many groups of insects [22,44]. Three species of Onychiuridae have identical translocation of the same genes as a synapomorphy.…”

“…Additionally, the topology test also rejected Symphypleona s. l. hypothesis for the trees based on 15 nucleotide sequences using either partitioning or GHOST model. Four analyses have retrieved the topology of (Entomobryoidea + Isotomidae) + Symphypleona s. s., which is in line with the result of Leo et al [44], and is supported by their morphological similarities such as reduction of prothoracic tergum, presence of abdominal bothriotricha and chaetotaxy on legs. But this topology was not strongly supported in our analyses.…”

“…Mitogenomic analyses have also been implemented to solve some phylogenetic and taxonomic problems of Collembola [42][43]. A recent study has reported so far most comprehensive phylogenetic analysis of Collembola based on mitogenomes, with 11 families sampled [44]. In the context of their taxon sampling, they revealed the structural diversity of collembolan mitogenomes, recovered the monophyly of all four orders as well as six families, and contributed to the time frame of collembolan evolution.…”

“…topology for the position of Tullbergiidae by using datasets either including or excluding the third codon positions [44]. Resolving this problem may require further assessment involving other assumed members of the superfamily Onychiuroidea, such as Odontellidae Massoud, 1967 andPachytullbergiidae Stach, 1954.…”

Streamlining universal single‐copy orthologue and ultraconserved element design: A case study in Collembola

“…Our in silico phylogenomic analyses recovered better‐resolved reconstructions of deeper collembolan relationships than ever before (Figure 3), succeeding where many previous attempts failed (Carapelli et al, 2014; D’Haese, 2002; Leo et al, 2019; Xiong et al, 2008; Yu et al, 2015). The most recent phylogenies used mitochondrial genomes and only confidently recovered the sister group relationship of Entomobryomorpha and Symphypleona, while the monophyly of Poduromorpha and Onychiuroidea and the phylogenetic positions of Poduromorpha and Neelipleona were not resolved (Leo et al, 2019). We recovered two main highly supported topologies in our ML reconstructions with the monophyly of four orders and Onychiuroidea confirmed.…”