Comparative mitogenomics of Braconidae (Insecta: Hymenoptera) and the phylogenetic utility of mitochondrial genomes with special reference to Holometabolous insects

Abstract

BackgroundAnimal mitochondrial genomes are potential models for molecular evolution and markers for phylogenetic and population studies. Previous research has shown interesting features in hymenopteran mitochondrial genomes. Here, we conducted a comparative study of mitochondrial genomes of the family Braconidae, one of the largest families of Hymenoptera, and assessed the utility of mitochondrial genomic data for phylogenetic inference at three different hierarchical levels, i.e., Braconidae, Hymenoptera, and Holometabola.ResultsSeven mitochondrial genomes from seven subfamilies of Braconidae were sequenced. Three of the four sequenced A+T-rich regions are shown to be inverted. Furthermore, all species showed reversal of strand asymmetry, suggesting that inversion of the A+T-rich region might be a synapomorphy of the Braconidae. Gene rearrangement events occurred in all braconid species, but gene rearrangement rates were not taxonomically correlated. Most rearranged genes were tRNAs, except those of Cotesia vestalis, in which 13 protein-coding genes and 14 tRNA genes changed positions or/and directions through three kinds of gene rearrangement events. Remote inversion is posited to be the result of two independent recombination events. Evolutionary rates were lower in species of the cyclostome group than those of noncyclostomes. Phylogenetic analyses based on complete mitochondrial genomes and secondary structure of rrnS supported a sister-group relationship between Aphidiinae and cyclostomes. Many well accepted relationships within Hymenoptera, such as paraphyly of Symphyta and Evaniomorpha, a sister-group relationship between Orussoidea and Apocrita, and monophyly of Proctotrupomorpha, Ichneumonoidea and Aculeata were robustly confirmed. New hypotheses, such as a sister-group relationship between Evanioidea and Aculeata, were generated. Among holometabolous insects, Hymenoptera was shown to be the sister to all other orders. Mecoptera was recovered as the sister-group of Diptera. Neuropterida (Neuroptera + Megaloptera), and a sister-group relationship with (Diptera + Mecoptera) were supported across all analyses.ConclusionsOur comparative studies indicate that mitochondrial genomes are a useful phylogenetic tool at the ordinal level within Holometabola, at the superfamily within Hymenoptera and at the subfamily level within Braconidae. Variation at all of these hierarchical levels suggests that the utility of mitochondrial genomes is likely to be a valuable tool for systematics in other groups of arthropods.

The first mitochondrial genome for the wasp superfamily Platygastroidea: the egg parasitoidTrissolcus basalis

“…For example, the monophyly of the Proctotrupomorpha (sensu Rasnitsyn 1988) is well supported by recent studies, but the relationships among the proctotrupomorph families are still controversial (Dowton and Austin 2001;Rasnitsyn and Zhang 2010;Heraty et al 2011). Several analyses have demonstrated that the whole mt genome is a useful tool to resolve hymenopteran evolutionary relationships (Castro and Dowton 2007;Cameron et al 2008;Dowton et al 2009a;Wei et al 2010a). To date, 18 complete mt genomes and 15 nearly complete mt genomes have been successfully sequenced in the Hymenoptera, with 18 taxa added in the last 3 years.…”

Two nearly complete mitogenomes of wheat stem borers, Cephus pygmeus (L.) and Cephus sareptanus Dovnar-Zapolskij (Hymenoptera: Cephidae): An unusual elongation of rrnS gene

“…However, we have managed to obtain partial ends of the A + T-rich region in C. pygmeus after application of several approaches. Similar cases have been reported in insect mitogenomes as a frequently encountered problem Castro and Dowton, 2005;Castro et al, 2006;Mao et al, 2014;Wei et al, 2010b). The partial sequenced A + T-rich region and two tRNAs (trnI, trnQ incomplete for C. sareptanus) were therefore excluded from all subsequent analyses, but included in GenBank database.…”

“…The rrnS secondary structure is predicted for the first time in sawflies and includes 30 helices like most known hymenopteran species (Gillespie et al, 2006;Wei et al, 2009;Wu et al, 2014), but an exception was reported for braconid species (Wei et al, 2010b) (Fig. 4).…”

The complete mitochondrial genome of the leafminer Liriomyza sativae (Diptera: Agromyzidae): Great difference in the A+T-rich region compared to Liriomyza trifolii

“…The A + T-rich region had been reported to possess some essential elements involved in the initiation of replication and transcription process (Goddard and Wolstenholme, 1980;Zhang and Hewitt, 1997;Zhang et al, 1995;Wei et al, 2010aWei et al, , 2010b. Zhang and Hewitt (Zhang and Hewitt, 1997) reported five pertinent structure elements: (1) a poly-T stretch, which may be associated with the control of transcription and replication; (2) a [TA(A)] n like stretch following the poly-T stretch; (3) a highly conserved stem-and-loop structure, which may be involved in the replication; (4) a highly conserved flanking sequence of the stem and loop structure with a 5′ consensus of 'TATA' and a 3′ consensus of 'G(A) n T'; (5) a G + A-rich sequence block located downstream of the secondary structure.…”

“…It usually contains a remarkably conserved set of 37 genes including 22 encoding tRNAs, 2 encoding rRNAs (lrRNA and srRNA), and 13 encoding proteins that are involved in electron transport and oxidative phosphorylation (Wolstenholme, 1992;Boore, 1999). The mitochondrial genome is highly economized with few sections of noncoding DNA, intergenic regions, or repetitive sequences (Harrison, 1989;Lunt et al, 1998aLunt et al, , 1998b, except for the A + T-rich region (also called control region) which is the most variable region in both A + T content and length of mtDNA due to the insertions/deletions of nucleotides, variation in copy numbers of sequences repeated in tandem and extensive length variation of a variable domain (Zhang et al, 1995;Rondan Duenas et al, 2002;Wei et al, 2010aWei et al, , 2010b. Additionally, the control region harbors some essential elements that play an important role in the initiation of transcription and replication (Wolstenholme, 1992;Zhang et al, 1995;da Silva et al, 2009).…”