Mitochondrial genome evolution and molecular phylogeny of parasitic lice (infraorder: Phthiraptera)

Parasitic lice (infraorder Phthiraptera) have five parvorders: Amblycera, Anoplura Ischnocera, Rhynchophthirina and Trichodectera. Sucking lice are in the parvorder Anoplura and chewing lice are in the other four parvorders. Fragmented mitochondrial (mt) genome has been found in lice of all five parvorders. Anoplura, Rhynchophthirina, and Trichodectera species studied so far, all have extensively fragmented mt genomes. For Amblycera and Ischnocera, some species (e.g.,  pigeon lice) have fragmented mt genomes whereas others have single-chromosome mt genomes. As a shared derived  character, mt genome fragmentation supported the close phylogenetic relationship among the three parvorders: Anoplura,  Rhynchophthirina and Trichodectera. However, a few studies showed that mt genome fragmentation could occur  independently in different lineages of parasitic lice. In this thesis, I investigated the mt genome evolution in a broader range of parasitic lice including both chewing lice and sucking lice from birds and mammals. The potential use of mt genome fragmentation in resolving phylogenetic relationships among parasitic lice was explored and discussed.

This thesis has six chapters. Chapter 1 is a literature review, in which I introduced parasitic lice and their mt genomes. In Chapter 2, I analysed the variation in mt karyotype between the macaque louse and the colobus louse (both in the genus Pedicinus) and inferred the mt karyotype of the most recent common ancestor of higher primate lice. I discovered that two of the inferred ancestral mt minichromosomes of higher primate lice merged as one in the macaque louse whereas one of the ancestral minichromosomes split into two in the colobus louse after these two species diverged from their most recent common ancestor. The findings of this chapter have been published in Fu & Dong et al. (2020).

In Chapter 3, I reconstructed the phylogeny of sucking lice and inferred the ancestral mt karyotype of Polyplax sucking lice. I discovered that: 1) tRNA genes are entirely responsible for mt karyotype variation in three Polyplax species studied to date; and 2) tRNA gene translocation is frequent between different types of minichromosomes and towards the boundaries with control regions. A similar tRNA gene translocation pattern can also be seen in other sucking lice with fragmented mt genomes. The findings of this chapter have been published in Dong et al. (2021).

n Chapter 4, I assembled the mt genomes of five seal louse species (family Echinophthiriidae) and the gorilla louse (Pthirus gorillae). I then inferred the mt karyotype of the most recent common ancestor of seal lice. My results indicated that: 1) at least three ancestral mt minichromosomes of sucking lice have split in the lineage leading to seal lice; 2) two ancestral minichromosomes of seal lice have merged in the lineage to the northern fur seal louse; and 3) one minichromosome ancestral to primate lice has split in the lineage to the gorilla louse. My analysis of mt karyotypes and gene sequences also indicated the possibility of a host switch of crabeater seal louse to Weddell seals. The findings of this chapter have been published in Dong et al. (2022).

In Chapter 5, I sequenced and assembled the mt genomes of 17 species of Amblycera lice – 14 in the family Menoponidae and three in the family Laemobothriidae. I found that four Menoponidae species in three genera (Actornithophilus, Austromenopon and Myrsidea) have fragmented mt genomes, whereas all the other 13 Amblycera species have the typical single-chromosome mt genomes. My analysis showed that mt genome fragmentation occurred four times independently in
each of the four genera: Actornithophilus, Austromenopon, Myrsidea and Laemobothrion. The manuscript that reports the findings of this chapter has been externally reviewed by the journal Cladistics and a revised manuscript is currently under review with the journal.

In Chapter 6, I summarized my research findings and discussed further study that can be done in the future. This thesis is a significant contribution to our understanding of the evolution of mt genomes of parasitic lice. For the first time, I discovered that: 1) mt karyotype evolved in opposite directions between two closely related congeneric species: macaque louse (Pedicinus obtusus) and colobus louse (Pedicinus badii); 2) for sucking lice, tRNA gene translocation is frequent between different types of minichromosomes and towards the boundaries with control regions; 3) minichromosomal split was much more frequent than minichromosomal merger in seal lice, and a host switch likely occurred from crabeater seals to Weddell seals; 4) mt genome fragmentation occurred four times independently in each of the four genera of Amblycera:  Actornithophilus, Austromenopon, Myrsidea and Laemobothrion; and 5) each independent mt genome fragmentation event produced unique shared derived minichromosomal characters that could be informative in resolving the phylogeny of parasitic lice at different taxonomic levels.