Inferring the History of Interchromosomal Gene Transposition in Drosophila Using n-Dimensional Parsimony

Abstract

Gene transposition puts a new gene copy in a novel genomic environment. Moreover, genes moving between the autosomes and the X chromosome experience change in several evolutionary parameters. Previous studies of gene transposition have not utilized the phylogenetic framework that becomes possible with the availability of whole genomes from multiple species. Here we used parsimonious reconstruction on the genomic distribution of gene families to analyze interchromosomal gene transposition in Drosophila. We identified 782 genes that have moved chromosomes within the phylogeny of 10 Drosophila species, including 87 gene families with multiple independent movements on different branches of the phylogeny. Using this large catalog of transposed genes, we detected accelerated sequence evolution in duplicated genes that transposed when compared to the parental copy at the original locus. We also observed a more refined picture of the biased movement of genes from the X chromosome to the autosomes. The bias of X-to-autosome movement was significantly stronger for RNA-based movements than for DNA-based movements, and among DNAbased movements there was an excess of genes moving onto the X chromosome as well. Genes involved in female-specific functions moved onto the X chromosome while genes with male-specific functions moved off the X. There was a significant overrepresentation of proteins involving chromosomal function among transposed genes, suggesting that genetic conflict between sexes and among chromosomes may be a driving force behind gene transposition in Drosophila.

How to Infer Ancestral Genome Features by Parsimony: Dynamic Programming over an Evolutionary Tree

“…Han and Hahn [27] use k-dimensional linear parsimony to study gene duplications and losses concomitantly with transpositions between chromosomes. Homolog genes for a family are encoded in a k-dimensional integer vector by the copy numbers on k chromosomes.…”

Characterizing gene movements between chromosomes in Drosophila

“…For this approach to succeed, we would need a comprehensive identification of all gene arrangement changes in the genome. In Han and Hahn, 1 we aimed to catalog all the gene movements between chromosome arms in the ten species of Drosophila. We used the ten species that Downloaded by [University of Lethbridge] at 02:18 06 October 2015 al., 14 and showed consistent sex-bias across species in the genes we were interested in.…”

“…Other genes such as rhino, JIL-1, zucchini, AGO2, caravaggio, tefu, etc., are listed in Table S7 of Han and Hahn. 1 Many of these genes are known to evolve rapidly in their sequence as well, especially the ones that are part of the RNAi machinery that protects the genome from the invasion of transposable elements. 26 To list some examples involved in chromosome segregation, in the branch leading to the melanogaster subgroup, we found Nnf1a duplicate from element C to B creating the paralog Nnf1b, while Mis12 relocated from element B to D. These genes are both subunits of the Mis12 complex, which is a component of the centromere kinetochore.…”

“…These changes happen as mistakes during recombination or through retrotransposition. In Han and Hahn 2011, 1 we surveyed the genomes of ten Drosophila species, to identify and characterize the gene transposition events in the history of these species. In the paper, we showed that the rate of gene transposition in Drosophila is higher than previously appreciated.…”

The evolution of sex-biased gene expression in Drosophila serrata

“…On the D. melanogaster X chromosome, there is a deficit of sperm proteome-specific genes (Meisel et al 2012a) but not testis-specific genes in general (Meiklejohn and Presgraves 2012;Meisel et al 2012a). Because I used conserved synteny between D. serrata and D. melanogaster (Stocker et al 2012) to place genes on chromosomes, it is possible that genes which have transposed from the X chromosome to an autosome, a move which has occurred more than expected by chance for testis-specific genes in D. melanogaster (Betran et al 2002;Han and Hahn 2012), were incorrectly assigned to the X chromosome in D.…”