Mitochondrial genome deletions and minicirclesare common in lice (Insecta: Phthiraptera)

Background:The gene composition, gene order and structure of the mitochondrial genome are remarkably stableacross bilaterian animals. Lice (Insecta: Phthiraptera) are a major exception to this genomic stability in that thecanonical single chromosome with 37 genes found in almost all other bilaterians has been lost in multiple lineagesin favour of multiple, minicircular chromosomes with less than 37 genes on each chromosome.

Results:Minicircular mt genomes are found in six of the ten louse species examined to date and three types ofminicircles were identified: heteroplasmic minicircles which coexist with full sized mt genomes (type 1); multigenechromosomes with short, simple control regions, we infer that the genome consists of several such chromosomes(type 2); and multiple, single to three gene chromosomes with large, complex control regions (type 3). Mappingminicircle types onto a phylogenetic tree of lice fails to show a pattern of their occurrence consistent with anevolutionary series of minicircle types. Analysis of the nuclear-encoded, mitochondrially-targetted genes inferredfrom the body louse,Pediculus, suggests that the loss of mitochondrial single-stranded binding protein (mtSSB)may be responsible for the presence of minicircles in at least species with the most derived type 3 minicircles(Pediculus, Damalinia).

Conclusions:Minicircular mt genomes are common in lice and appear to have arisen multiple times within thegroup. Life history adaptive explanations which attribute minicircular mt genomes in lice to the adoption of blood-feeding in the Anoplura are not supported by this expanded data set as minicircles are found in multiple non-blood feeding louse groups but are not found in the blood-feeding genusHeterodoxus. In contrast, a mechanistexplanation based on the loss of mtSSB suggests that minicircles may be selectively favoured due to the incapacityof the mt replisome to synthesize long replicative products without mtSSB and thus the loss of this gene lead tothe formation of minicircles in lice.