Mitochondrial genomes within bark lice (Insecta: Psocodea: Psocomorpha) reveal novel gene rearrangements containing phylogenetic signal

Abstract

Psocodea (booklice and parasitic lice) is an order of insects containing species with extensive mitochondrial genome rearrangements, particularly within the suborder Troctomorpha, in which some species possess an extremely fragmented mitochondrial genome with several small minichromosomes. In the remaining suborders of Psocodea, there are groups with the ancestral pancrustacean arrangement, quite extensive rearrangements (e.g. Trogiomorpha), or in which the small number of species analysed to date have rearrangements of only a few protein‐coding genes and/or tRNAs (e.g. Psocomorpha). Despite the apparent high rate of rearrangements in the order as a whole, a small number of complete mitochondrial genomes are available, especially for suborder Psocomorpha, the largest free‐living suborder. To understand the evolution of the gene arrangement of the mitochondrial genome within Psocomorpha and its phylogenetic implications, we assembled and analysed the mitochondrial genomes of 33 species of bark lice belonging to nine families in two infraorders. Within the infraorder Homilopsocidea, four families were analysed, mainly from Lachesillidae (which included 22 species of this family). Within the infraorder Caeciliusetae, seven species representing five families were analysed. Mitochondrial gene rearrangements were identified in seven of the nine families. Some of these rearrangements were unique to a single species, while some contained phylogenetic signal, being shared by related species. These rearrangements typically corresponded to transpositions and inversions of tRNAs, possibly caused by tandem duplication–random loss (TDRL) and/or recombination events. Phylogenetic analyses of mitochondrial gene sequences provided phylogenetic resolution for several branches of the tree, including monophyly of Lachesillinae. The genus Hemicaecilius Enderlein was found to be embedded within the genus Lachesilla Westwood, rending the latter paraphyletic. Monophyly was also never recovered for Lachesillidae and Elipsocidae as currently defined. However, instability was observed for some higher level relationships within Psocomorpha, including the relationships among the major clades of Lachesillidae.

Mitochondrial gene rearrangements suggest a new genus in the subfamily Cantharinae (Coleoptera)

“…Similar to other insects (Hasegawa et al, 2011; Li et al, 2020; Li et al, 2021; Saenz Manchola et al, 2021), the mitogenomes of the “semifumatus” group, Cephalomalthinus , and Rhagonycha exhibited a typical high A + T bias and a higher proportion of bases A and G than T and C. This compositional heterogeneity and strand asymmetry are typically attributed to energy efficiency trade‐offs (Chen et al, 2016; Rocha & Danchin, 2002) and likely result from mutations and selection pressures (Kono et al, 2018), respectively. In addition, the initiation and termination codons in the PCGs of all studied taxa were consistent with the generally observed pattern in the class Insecta (Li et al, 2020; Li et al, 2021), and the incomplete stop codon TA commonly occurs in insects and may be caused by post‐transcriptional polyadenylation (Ojala et al, 1981).…”

Mitochondrial phylogenomics and mitogenome organization in the parasitoid wasp family Braconidae (Hymenoptera: Ichneumonoidea)

“…Mt gene rearrangements have been shown to be phylogenetically informative at different evolutionary scales in various insect orders, recovering particular patterns for specific lineages [ 7 , 25 , 29 , 52 – 55 ]. In Hymenoptera, sawflies and woodwasps (previously known as Symphyta) usually have a conserved mt gene order, whereas various gene rearrangements have been reported for Apocrita [ 9 , 56 ].…”

First Report on Mitochondrial Gene Rearrangement in Non-Biting Midges, Revealing a Synapomorphy in Stenochironomus Kieffer (Diptera: Chironomidae)

“…Since the concept of using mitochondrial gene rearrangements as phylogenetic markers has been proposed in the mid-1980s [3], the synapomorphic gene rearrangements have been identified in many taxa, supporting the monophyletic or systematic relationships of related lineages [9,12,13]. In insect mitogenomes, patterns of gene arrangement are usually conserved within lineages [6], but gene rearrangements have also been observed involving tRNA and PCG within many orders, such as Blattodea [14], Ephemeroptera [15,16], Hemiptera [17,18], Hymenoptera [12,19], Lepidoptera [20], Mantodea [21,22], Orthoptera [23,24], Phthiraptera [25], Psocoptera [9], and Thysanoptera [26]. For the mitogenomes of Diptera, gene rearrangements have been detected within several families, e.g., Calliphoridae [27], Cecidomyiidae [28], and Mycetophilidae [29].…”

“…The typical mitogenome of insect is a 14-20 kb circular molecule, containing 37 genes (13 proteincoding genes, two ribosomal RNA genes, and 22 transfer RNA genes) and a control region on a single chromosome [4] characterized by the small genome size, maternal inheritance, low sequence recombination, and fast evolution rates [1,5,6]. Benefited by the high-throughput sequencing technology, nucleotide sequences of mitogenomes are now widely used in phylogenetic and evolutionary studies [7][8][9]. Besides, gene rearrangement is an additional type of data to support relationships of taxa, with rearrangement synapomorphies identified across multiple orders and at many different taxonomic levels [1,10,11].…”

“…Besides, gene rearrangement is an additional type of data to support relationships of taxa, with rearrangement synapomorphies identified across multiple orders and at many different taxonomic levels [1,10,11]. Since the concept of using mitochondrial gene rearrangements as phylogenetic markers has been proposed in the mid-1980s [3], the synapomorphic gene rearrangements have been identified in many taxa, supporting the monophyletic or systematic relationships of related lineages [9,12,13]. In insect mitogenomes, patterns of gene arrangement are usually conserved within lineages [6], but gene rearrangements have also been observed involving tRNA and PCG within many orders, such as Blattodea [14], Ephemeroptera [15,16], Hemiptera [17,18], Hymenoptera [12,19], Lepidoptera [20], Mantodea [21,22], Orthoptera [23,24], Phthiraptera [25], Psocoptera [9], and Thysanoptera [26].…”