Translocation of Y-Linked Genes to the Dot Chromosome in Drosophila pseudoobscura

Abstract

One of the most striking cases of sex chromosome reorganization in Drosophila occurred in the lineage ancestral to Drosophila pseudoobscura, where there was a translocation of Y-linked genes to an autosome. These genes went from being present only in males, never recombining, and having an effective population size of 0.5N to a state of autosomal linkage, where they are passed through both sexes, may recombine, and their effective population size has quadrupled. These genes appear to be functional, and they underwent a drastic reduction in intron size after the translocation. A Y-autosome translocation may pose problems in meiosis if the rDNA locus responsible for X-Y pairing had also moved to an autosome. In this study, we demonstrate that the Y-autosome translocation moved Y-linked genes onto the dot chromosome, a small, mainly heterochromatic autosome with some sex chromosome-like properties. The rDNA repeats occur exclusively on the X chromosome in D. pseudoobscura, but we found that the new Y chromosome of this species harbors four clusters bearing only the intergenic spacer region (IGS) of the rDNA repeats. This arrangement appears analogous to the situation in Drosophila simulans, where X-rDNA to Y-IGS pairing could be responsible for X-Y chromosome pairing. We postulate that the nascent D. pseudoobscura Y chromosome acquired and amplified copies of the IGS, suggesting a potential mechanism for X-Y pairing in D. pseudoobscura.

The Birds and the Bees and the Flowers and the Trees: Lessons from Genetic Mapping of Sex Determination in Plants and Animals

“…Many species have X0 systems, including some nematodes and insects, and these most likely evolved from XY GSD (Shearman 2002), after genetic degeneration of the Y chromosome and movement of genes essential for male functions to other chromosomes. Such gene movement has been documented in Drosophila pseudoobscura (Carvalho and Clark 2005;Koerich et al 2008;Larracuente et al 2010). X0 species, such as C. elegans (Gladden et al 2007), must also have a dosage-sensitive sex determination system, where the different amounts of one or more X chromosome transcripts between the sexes provide a ''counting mechanism'' relative to autosomal elements.…”

The house fly Y Chromosome is young and minimally differentiated from its ancient X Chromosome partner

“…In both cases, one of the formerly autosomal homologs evolves into an X (or Z) Chromosome, and the other homolog evolves into a Y (or W) Chromosome. In some cases, one or both of the ancestral sex chromosomes can revert back to an autosome when a different autosome becomes a new sex chromosome (Carvalho and Clark 2005;Larracuente et al 2010;. In all of the scenarios described above, the X and Y (or Z and W) Chromosomes evolve in concert, with an evolutionary transition in one sex chromosome producing a corresponding change in its partner.…”

“…In species with the ancestral karyotype, females are XX and males are XY, with a male-determining locus (M factor) on the Y Chromosome . Many sex chromosome transitions have occurred across Brachycera, including fusions of ancestral autosomes with the X Chromosome, autosomes transitioning into sex chromosomes, and complete reversions of the ancestral X to an autosome (Carvalho and Clark 2005;Baker and Wilkinson 2010;Larracuente et al 2010;Bachtrog 2013, 2015).…”

Simple Method for Fluorescence DNA <em>In Situ</em> Hybridization to Squashed Chromosomes

“…Although not shown here, this method is also effective for mapping non-repetitive sequences in euchromatin 10 . Using long, biotinylated probes provides more flexibility in detecting low copy number sequences as the signal can easily be amplified by repeated treatments of biotinylated anti-avidin and rhodamine-avidin 9 . To visualize single-copy sequences, multiple probes spanning the sequence may be necessary.…”

“…This method was originally designed for the rapid mapping of highly repetitive DNA sequences in heterochromatic regions of Drosophila larval neuroblasts by using commercially synthesized oligos that are conjugated with fluorescence dyes. However, this method also works for mapping repetitive sequences by using larger probes synthesized through other means 9,10 and across multiple different tissue and chromosome types.…”