The Complete Mitochondrial Genome of the Chicken Body Louse, Menacanthus cornutus, and Evolutionary Patterns of Extensive Gene Rearrangements in the Mitochondrial Genomes of Amblycera (Psocodea: Phthiraptera)

Abstract

Animal mitochondrial (mt) genomes are typically double-strand circular DNA molecules, but diverse structural variations have been widely found in multiple groups. In parasitic lice (Phthiraptera), the structure of mt genomes varies remarkably across all five suborders. In this study, we reported the complete mt genome of a chicken body louse, Menacanthus cornutus, which has a typical single circular mt chromosome and drastic mt gene rearrangements. This mt genome is 15,693 bp in length, consisting of 13 protein-coding genes, 23 tRNA genes, 2 rRNA genes, and a control region. A comparison with a typical insect mt genome suggested that two highly similar trnM are present in the mt genome of M. cornutus. Moreover, almost every single gene was rearranged, and over half of mt genes were inverted. Phylogenetic analyses inferred from the mt genome sequences supported the monophyly and position of Amblycera. Mapped over the phylogenetic relationships of Amblycera, we identified two inversion events for the conserved gene blocks in Boopidae and Menoponidae. The inverted ND4L-ND4 was likely a synapomorphic rearrangement in Menoponidae. Our study demonstrated the importance of sequencing mt genomes for additional taxa to uncover the mechanism underlying the structural evolution of the mt genome in parasitic lice.

Mitochondrial Genome Fragmentation Occurred Multiple Times Independently in Bird Lice of the Families Menoponidae and Laemobothriidae

“…The evidence available to date indicates that mt genome fragmentation occurred independently at least 14 times among parasitic lice (infraorder Phthiraptera): once in eutherian mammal lice in three parvorders (Anoplura, Rhynchophthirina, and Trichodectera) [ 16 , 20 ], four to five times in amblyceran lice ([ 20 ], and the present study), and nine times in ischnoceran lice [ 20 ]. The independent evolution of fragmented mt genomes is also supported by the observations of the typical single-chromosome mt genomes in 16 amblyceran species from four different families (Boopiidae, Laemobothriidae, Menoponidae, and Ricinidae) ([ 16 , 17 , 22 , 23 ], and the current study), in 10 ischnoceran species from 10 genera [ 16 , 18 , 21 , 41 ], but not in any species in Anoplura, Rhynchophthirina, or Trichodectera [ 4 , 5 , 6 , 7 , 8 , 9 , 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 ].…”

“…These fragmentation events are independent of the fragmentation observed in eutherian mammal lice of the parvorders Anoplura, Rhynchophthirina, and Trichodectera, which apparently occurred only once in the most recent common ancestor of these three parvorders [ 3 , 16 , 19 , 20 ]. The typical single-chromosome mt genome has not been seen in any species from Anoplura, Rhynchophthirina, or Trichodectera, but has been seen in 10 species from 10 different genera of Ischnocera and seven species of Amblycera from three families (Boopiidae; Menoponidae, and Ricinidae) [ 16 , 21 , 22 , 23 ].…”