Fragmented mitochondrial genomes are present in both major clades of the blood-sucking lice (suborder Anoplura): evidence from two Hoplopleura rodent lice (family Hoplopleuridae)

Abstract

BackgroundThe suborder Anoplura contains 540 species of blood-sucking lice that parasitize over 840 species of eutherian mammals. Fragmented mitochondrial (mt) genomes have been found in the lice of humans, pigs, horses and rats from four families: Pediculidae, Pthiridae, Haematopinidae and Polyplacidae. These lice, eight species in total, are from the same major clade of the Anoplura. The mt genomes of these lice consist of 9–20 minichromosomes; each minichromosome is 1.5–4 kb in size and has 1–8 genes. To understand mt genome fragmentation in the other major clade of the Anoplura, we sequenced the mt genomes of two species of rodent lice in the genus Hoplopleura (family Hoplopleuridae).ResultsWe identified 28 mt genes on 10 minichromosomes in the mouse louse, Ho. akanezumi; each minichromosome is 1.7–2.7 kb long and has 1–6 genes. We identified 34 mt genes on 11 minichromosomes in the rat louse, Ho. kitti; each minichromosome is 1.8–2.8 kb long and has 1–5 genes. Ho. akanezumi also has a chimeric minichromosome with parts of two rRNA genes and a full-length tRNA gene for tyrosine. These two rodent lice share the same pattern for the distribution of all of the protein-coding and rRNA genes but differ in tRNA gene content and gene arrangement in four minichromosomes. Like the four genera of blood-sucking lice that have been investigated in previous studies, the Hoplopleura species have four minichromosomes that are only found in this genus.ConclusionsOur results indicate that fragmented mt genomes were present in the most recent common ancestor of the two major clades of the blood-sucking lice, which lived ~75 million years ago. Intra-genus variation in the pattern of mt genome fragmentation is common in the blood-sucking lice (suborder Anoplura) and genus-specific minichromosomes are potential synapomorphies. Future studies should expand into more species, genera and families of blood-sucking lice to explore further the phylogenetic utility of the novel features associated with fragmented mt genomes.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-751) contains supplementary material, which is available to authorized users.

The Mitochondrial Genome of the Guanaco Louse, Microthoracius praelongiceps: Insights into the Ancestral Mitochondrial Karyotype of Sucking Lice (Anoplura, Insecta)

“…The different locations of trnI between the great ape lice and the Hoplopleura rodent lice can be explained by two independent split events of nad2-trnI-cox1-trnL 2 minichromosome if it is ancestral to sucking lice (Jiang et al. 2013; Dong et al 2014a; Song et al. 2014).…”

“…2014); 5) the lice of the greater bandicoot rat and the Asian house rat, Polyplax asiatica and Polyplax spinulosa (Dong et al. 2014b); and 6) the lice of the Cheverier’s field mouse and the Bower’s white-toothed rat, Hoplopleura akanezumi and Hoplopleura kitti (Dong et al. 2014a).…”

Mitochondrial genomes ofColumbicolafeather lice are highly fragmented, indicating repeated evolution of minicircle-type genomes in parasitic lice

“…Columbicola mitochondrial genome appears to be much more fragmented than that of any other feather louse species reported by Cameron et al (2011), which had between 6 and 22 full genes on the recovered chromosomes. The mitochondrial genomes of Columbicola are also more fragmented than the mitochondrial genomes of most mammal associated lice (Jiang et al 2013, Dong et al 2014a, b, Herd et al 2015. Columbicola has a similar level of fragmentation to the human louse (Pediculus humanus), which has at least 20 minicircles and an average of two genes per circle (Shao et al 2009(Shao et al , 2012.…”

“…Highly fragmented mitochondrial genomes in lice were first identified in human lice (Pediculus humanus) (Shao et al 2009), and minicircle-type mitochondrial genomes have since been confirmed in several other genera of sucking lice (Anoplura; Jiang et al 2013, Dong et al 2014a,b, Herd et al 2015, Shao et al 2017, elephant and warthog lice (Rhyncophthirina; Shao et al 2015), and chewing lice in the family Trichodectidae (Cameron et al 2011, Song et al 2019). Phylogenetic analyses have indicated that these three lineages of mammalian lice form a monophyletic group, which suggests highly fragmented mitochondrial genomes evolved once in the common ancestor of this group, as suggested by Song et al (2019).…”

“…Variation within a genus ranges from just 1 of 18 minicircles being different between two species of Pediculus (Herd et al 2015) to 9 of 11 minicircles being different between species of Polyplax (Dong et al 2014b). Other than Polyplax, over two-thirds of minicircles are shared by all members of a genus of sucking louse (17/19 to 4/12) suggesting that minicircle arrangements are stable at the genus-level within mammal-associated lice (Dong et al 2014a). As might be expected given this level of variation, few derived gene-boundaries are shared between Columbicola species and other lice, of which only trnI-cox1 and trnY-cox2 are likely of phylogenetic significance being shared by the common ancestor of a clade comprising all Ischnocera, Anoplura, and Rhychophthirina (c.f.…”