Evolution of the Neo-X Chromosome in Drosophila miranda

Evolutionary patterns on the X chromosome differ from those on the autosomes. Several recent studies in Drosophila have shown that genes with sex-biased expression (i.e. genes that are expressed differentially between sexes) are distributed non-randomly between sex chromosomes and autosomes. For example, the X chromosome has a paucity of male-biased genes. Previous studies have shown that in Drosophila this pattern is often a result of an excess of gene movement off of the ancestral X chromosome as well as off of novel X chromosomes which are created as a result of a fusion between an autosome and a sex chromosome. Male-biased genes are overrepresented among the genes that move off of the X's thus leading to demasculinization of the X. While several theories have been proposed to explain this phenomenon, what exactly causes such pattern is still unclear./nOne of the difficulties in studying gene movement off of the ancestral X chromosome is the fact that this chromosome is over 50 myo and is fully differentiated from its homolog. Male-biased genes that were affected by X-linkage moved to autosomes millions of years ago and determining the causes of the movements or the temporal pattern of them is problematic./nHere we present results on gene movement in the species Drosophila miranda, which is unique in having three different X chromosomes. Muller-A is the ancestral X chromosome which is shared by all Drosophila species and is approximately 50 myo; Muller-AD is a neo-X chromosome which originated approximately 8 to 12 million years ago and is a fully developed X chromosome; and Muller-C is a very young neo-X chromosome that originated between 1 and 2 mya and is in the process of acquiring all characteristics of a mature X chromosome. Having three different X chromosomes in the same genome and especially having a very young X chromosome allowed us to look into temporal pattern of gene movement as well as see how soon after a chromosome starts segregating as an X chromosome genes start to move to autosomes./nIn Chapter 1, I give an overview of X chromosome biology, describe known patterns of X chromosome gene content in Drosophila as well as in other species and review the theories which have been proposed to explain the unusual patterns of gene movement between X chromosomes and autosomes./nIn Chapter 2, I focus on the approaches we developed to identify gene movements in Drosophila miranda. One of the major challenges in studying very recent gene movements is that very young genes often fail to assemble properly and are often absent from complete genome assemblies. We developed a pipeline to detect very young gene retroposition events using raw next generation sequencing data without relying on an assembled genome. We show that the number of young genes we found is much higher than reported previously suggesting that the rates of retroposition in Drosophila are higher than was known before and that studies that look at new gene evolution likely omit a large fraction of young genes due to them being unassembled./nIn Chapter 3, I describe the pattern of interchromosomal movement of genes in Drosophila miranda. Although it is known that the ancestral X chromosome (Muller-A) and the older neo-X chromosome (Muller-AD) are demasculinized in other species, studies of very recent gene movements as well as movements out of a very young X chromosome have not been done. While we did not observe a demasculinization pattern that has been reported in other species, we found a significant increase of young retroposed genes that originated on both Muller-C and Muller-AD. Therefore, our results suggest that out of the neo-X gene movement begins soon after a chromosome starts segregating as an X chromosome and that the demasculinization of the older neo-X (Muller-AD) is still in progress.

Advisor: Bachtrog, Doris