The Mitochondrial Genome of the Screamer Louse Bothriometopus (Phthiraptera: Ischnocera): Effects of Extensive Gene Rearrangements on the Evolution of the Genome

Abstract

Mitochondrial (mt) genome rearrangement has generally been studied with respect to the phenomenon itself, focusing on their phylogenetic distribution and causal mechanisms. Rearrangements have additional significance through effects on substitution, transcription, and mRNA processing. Lice are an ideal group in which to study the interactions between rearrangements and these factors due to the heightened rearrangement rate within this group. The entire mt genome of the screamer louse Bothriometopus was sequenced and compared to previously sequenced louse genomes. The mt genome is 15,564 bp, circular, and all genes are encoded on the same strand. The gene arrangement differs radically from both other louse species and the ancestral insect. Nucleotide composition is A+T biased, but there is no skew which may be due to reversal of replication direction or a transcriptional effect. Bothriometopus has both tRNA duplication and concerted evolution which has not been observed previously. Eleven of the 13 protein-coding genes have 3 0 end stem-loop structures which may allow mRNA processing without flanking tRNAs and so facilitate gene rearrangements. There are five candidate control regions capable of forming stem-loop structures. Two are structurally more similar to the control regions of other insect species than those of other lice. Analyses of Bothriometopus demonstrate that louse mt genomes, in addition to being extensively rearranged, differ significantly from most insect species in nucleotide composition biases, tRNA evolution, protein-coding gene structures and putative signaling sites such as the control region. These may be either a cause or a consequence of gene rearrangements.

The single mitochondrial chromosome typical of animals has evolved into 18 minichromosomes in the human body louse, Pediculus humanus

“…The mt genomes of three species of chewing lice and one species of the Psocoptera, i.e., a wallaby louse, Heterodoxus macropus (suborder Amblycera); a pigeon louse, Campanulotes bidentatus (suborder Ischnocera); a screamer louse, B. macrocnemis (Ischnocera); and Lepidopsocid sp. (Psocoptera), have been sequenced entirely (Shao et al 2001b(Shao et al , 2003Covacin et al 2006;Cameron et al 2007). Furthermore, seven species of chewing lice and two species of Psocoptera have been sequenced partially (Shao et al 2001a, b;Covacin et al 2006;Cameron et al 2007).…”

“…(Psocoptera), have been sequenced entirely (Shao et al 2001b(Shao et al , 2003Covacin et al 2006;Cameron et al 2007). Furthermore, seven species of chewing lice and two species of Psocoptera have been sequenced partially (Shao et al 2001a, b;Covacin et al 2006;Cameron et al 2007). There is no evidence for minicircular mt chromosomes in any of these chewing lice nor the Psocoptera.…”

“…Chewing lice infest birds and mammals and feed primarily on epidermal features, such as hairs and feathers (Price et al 2003). The mitochondrial (mt) genomes of three chewing lice have been sequenced entirely: a wallaby louse, Heterodoxus macropus (Amblycera), a pigeon louse, Campanulotes bidentatus (Ischnocera), and a screamer louse, Bothriometopus macrocnemis (Ischnocera) (Shao et al 2001b;Covacin et al 2006;Cameron et al 2007). Like most other animals, these three chewing lice have their 37 mt genes on a single circular chromosome, 14,670-, 14,804-, and 15,564-bp long, respectively.…”

Rates of genomic divergence in humans, chimpanzees and their lice

“…Mitochondrial genomes of lice are highly rearranged compared with other insects [25][26][27][28][29], and these rearrangements were hypothesized to be correlated with increased substitution rates. In fact, in the human body louse (P. humanus), the mitochondrion is divided into a number of minicircular chromosomes [15,30].…”

Nucleotide Composition of CO1 Sequences in Chelicerata (Arthropoda): Detecting New Mitogenomic Rearrangements

“…The origin of the strand-specific bias is related to asymmetric mutational constraints generating inequalities between the frequencies of the complementary bases A/T and C/G (Hassanin et al 2005;Reyes et al 1998;Tanaka and Ozawa 1994). Two asymmetric processes are potentially involved in strand bias: replication (Cameron et al 2007;Fonseca et al 2008;Hassanin et al 2005;Reyes et al 1998;Tanaka and Ozawa 1994) and transcription (Cameron et al 2007;Hassanin et al 2005). During replication and transcription processes, the strength of the mutational bias is related to the length of time each gene spends in a single-stranded state.…”