Novel gene rearrangement in the mitochondrial genome of Anastatus fulloi (Hymenoptera Chalcidoidea) and phylogenetic implications for Chalcidoidea

Abstract

The genus Anastatus comprises a large group of parasitoids, including several biological control agents in agricultural and forest systems. The taxonomy and phylogeny of these species remain controversial. In this study, the mitogenome of A. fulloi Sheng and Wang was sequenced and characterized. The nearly full-length mitogenome of A. fulloi was 15,692 bp, compromising 13 protein-coding genes (PCGs), 2 rRNA genes, 22 tRNA genes and a control region (CR). The total A + T contents were 83.83%, 82.18%, 87.58%, 87.27%, and 82.13% in the whole mitogenome, 13 PCGs, 22 tRNA genes, 2 rRNA genes, and CR, respectively. The mitogenome presented negative AT skews and positive GC skews, except for the CR. Most PCGs were encoded on the heavy strand, started with ATN codons, and ended with TAA codons. Among the 3736 amino acid-encoding codons, TTA (Leu1), CGA (Arg), TCA (Ser2), and TCT (Ser2) were predominant. Most tRNAs had cloverleaf secondary structures, except trnS1, with the absence of a dihydrouridine (DHU) arm. Compared with mitogenomes of the ancestral insect and another parasitoid within Eupelmidae, large-scale rearrangements were found in the mitogenome of A. fulloi, especially inversions and inverse transpositions of tRNA genes. The gene arrangements of parasitoid mitogenomes within Chalcidoidea were variable. A novel gene arrangement was presented in the mitogenome of A. fulloi. Phylogenetic analyses based on the 13 protein-coding genes of 20 parasitoids indicated that the phylogenetic relationship of 6 superfamilies could be presented as Mymaridae + (Eupelmidae + (Encyrtidae + (Trichogrammatidae + (Pteromalidae + Eulophidae)))). This study presents the first mitogenome of the Anastatus genus and offers insights into the identification, taxonomy, and phylogeny of these parasitoids.

Novel Mitochondrial Gene Rearrangement and Intergenic Regions Exist in the Mitochondrial Genomes from Four Newly Established Families of Praying Mantises (Insecta: Mantodea)

“…Among our newly sequenced mantis mitogenomes, the gene rearrangement regions covered those seen in previous studies such as the K-D cluster and the A-R-N cluster [ 8 , 11 , 30 ], as weak as a new rearrangement region ( Cytb-S2-ND1 ). Up to now, explanation of gene rearrangements has commonly used the tandem duplication–random loss (TDRL) model in insects, especially in Mantodea [ 6 , 32 , 35 , 37 , 81 ]. Therefore, this model was equally applicable to this study ( Figure 1 ).…”

“…Gene rearrangement and degeneration in the COX2-K-D-ATP8 region was unique to Eremiaphiloidea, especially in Toxoderidae [ 8 , 11 ]. This approach has also been applied in previous studies to further investigate the phylogenetic relationships within an order [ 6 , 8 , 9 , 11 , 32 , 39 , 44 , 81 ]. As for disputes that existed, these were raised mainly as a result of the relatively scant dataset with too few mitogenomes in the same family.…”

“…The gene arrangement of almost all insect mitogenomes is compact according to the ancestral phenotype, but exceptions have been detected in some orders, including Hymenoptera, Hemiptera, Ephemeroptera, and Mantodea, among others [ 28 , 32 , 33 , 34 , 35 , 36 , 37 , 38 ]. Gene rearrangements are a relatively common phenomenon in insects, but gene duplications are rare [ 26 ].…”

“…Meanwhile, extra CR- I - Q - M clusters with several non-coding regions (NCRs) were often found in Mantidae [ 6 , 8 ]. Hence, as a potential evolutionary marker, gene arrangements have been extensively applied in discussing evolutionary patterns and constructing or reconstructing systematic relationships among insect species [ 26 , 28 , 32 , 36 , 42 , 43 ].…”

“…As a result, they were frequently associated with gene duplication mechanisms [ 44 , 50 ]. The tandem duplication random loss (TDRL) model [ 50 ] has been intensively and extensively utilized in explaining the origin and mechanism of gene rearrangements in mitogenomes of mayflies [ 28 , 34 ], bees [ 32 , 38 ], praying mantises [ 6 , 8 , 11 , 30 ], and even in crabs [ 51 ].…”