Abstract

Prior to this study, complete mitochondrial genomes from Order Thysanoptera were restricted to a single family, the Thripidae, resulting in a biased view of their evolution. Here we present the sequences for the mitochondrial genomes of four additional thrips species, adding three extra families and an additional subfamily, thus greatly improving taxonomic coverage. Thrips mitochondrial genomes are marked by high rates of gene rearrangement, duplications of the control region and tRNA mutations. Derived features of mitochondrial tRNAs in thrips include gene duplications, anticodon mutations, loss of secondary structures and high gene translocation rates. Duplicated control regions are found in the Aeolothripidae and the ‘core’ Thripinae clade but do not appear to promote gene rearrangement as previously proposed. Phylogenetic analysis of thrips mitochondrial sequence data supports the monophyly of two suborders, a sister-group relationship between Stenurothripidae and Thripidae, and suggests a novel set of relationships between thripid genera. Ancestral state reconstructions indicate that genome rearrangements are common, with just eight gene blocks conserved between any thrips species and the ancestral insect mitochondrial genome. Conversely, 71 derived rearrangements are shared between at least two species, and 24 of these are unambiguous synapomorphies for clades identified by phylogenetic analysis. While the reconstructed sequence of genome rearrangements among the protein-coding and ribosomal RNA genes could be inferred across the phylogeny, direct inference of phylogeny from rearrangement data in MLGO resulted in a highly discordant set of relationships inconsistent with both sequence-based phylogenies and previous morphological analysis. Given the demonstrated rates of genomic evolution within thrips, extensive sampling is needed to fully understand these phenomena across the order.

Highlights

  • Complete mitochondrial genomes have been shown to be useful for phylogenetic and evolutionary studies at various taxonomic scales, as they provide more phylogenetic information than individual genes alone[1,2,3,4]

  • Most of the genes in F. vespiformis, H. indicus, and R. cruentatus were encoded on the majority strand except three protein-coding genes (PCGs) and three transfer RNA (tRNA)

  • The majority of genes in G. uzeli were encoded by the majority strand, a slightly larger number were encoded on the minority strand, four PCGs, fifteen tRNAs and both ribosomal RNAs

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Summary

Introduction

Complete mitochondrial genomes have been shown to be useful for phylogenetic and evolutionary studies at various taxonomic scales, as they provide more phylogenetic information than individual genes alone[1,2,3,4]. In addition to sequence variation, metazoan mitochondrial genomes exhibit variation in a number of features, such as length, tRNA secondary structure, gene order, and the number and internal structure of control regions[6,7,8]. These features can provide evidence for evolutionary relationships among taxa at high and/or low taxonomic levels beyond that provided by analysis of mitochondrial sequence data alone[9,10,11]. In the only major study of thrips phylogenetics, Buckman et al (2013) used multiple molecular markers to test the relationships within thrips, of families and subfamilies[25] Their data supported the monophyly of Tubulifera and Terebrantia and of the families Phlaeothripidae, Aeolothripidae, Melanthripidae and Thripidae. To determine relationships within Thysanoptera, analyses with sequence-based and genome rearrangement phylogenetic inference methods were used

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