Evolution of remarkable chromosome dynamics in two insect families with paternal genome elimination

Abstract

During meiosis in diploid organisms, Mendel’s laws suggest that homologous chromosomes should recombine and be randomly distributed to gametes. This is true for meiosis in most organisms, however, in some cases, chromosome transmission is not random, and can be biased depending on a number of factors including the parent of origin of a chromosome or selfish genes located on the chromosome. Why and how non-Mendelian inheritance evolves is not well understood in many cases, but having a good understanding of the evolution of these systems is important for establishing under what scenarios non-Mendelian inheritance might evolve and how meiosis is manipulated by certain chromosomes. This thesis focuses on two insect clades that exhibit non-Mendelian inheritance: scale insects in the family Eriococcidae and fungus gnats in the superfamily Sciaroidea. Both of these families exhibit a non-Mendelian inheritance system known as paternal genome elimination (PGE), where males only transmit chromosomes inherited from their mother to future generations. In Sciaroidea, I focus on one species with an unusual genetic system: Bradysia coprophila, which in addition to PGE has an unusual reproduction system in several other respects. I examine content and evolution of germline restricted chromosomes, which are present in the germ cells in this species but eliminated from somatic cells early in development. I characterise how many genes are on these chromosomes, and explore using genomic methods how these chromosomes evolved. I also conduct a mating preference experiment on B. coprophila to determine whether the chromosome inheritance system in this species affects male mating preferences, as this is one case among animals where we may expect males to evolve mating preferences for certain types of females. In Eriococcidae, how PGE occurs is labile, and transitions between different types of PGE are not well understood. I conduct of survey of species to establish how male meiosis differs in species across this clade, how the type of PGE affects paternal chromosomes in somatic cells, and whether there is any evidence for transitions to new genetic systems (i.e., loss of PGE) in any species within this clade. Studying these two insect systems can provide information about what happens in lineages when non-Mendelian chromosome inheritance evolves. We can determine how this affects a species behaviour, the mechanisms of chromosome inheritance, and genome evolution.