Genomic changes following the reversal of a Y chromosome to an autosome inDrosophila pseudoobscura

Abstract

Robertsonian translocations resulting in fusions between sex chromosomes and autosomes shape karyotype evolution by creating new sex chromosomes from autosomes. These translocations can also reverse sex chromosomes back into autosomes, which is especially intriguing given the dramatic differences between autosomes and sex chromosomes. To study the genomic events following a Y chromosome reversal, we investigated an autosome-Y translocation in Drosophila pseudoobscura. The ancestral Y chromosome fused to a small autosome (the dot chromosome) approximately 10–15 Mya. We used single molecule real-time sequencing reads to assemble the D. pseudoobscura dot chromosome, including this Y-to-dot translocation. We find that the intervening sequence between the ancestral Y and the rest of the dot chromosome is only ~78 Kb and is not repeat-dense, suggesting that the centromere now falls outside, rather than between, the fused chromosomes. The Y-to-dot region is 100 times smaller than the D. melanogaster Y chromosome, owing to changes in repeat landscape. However, we do not find a consistent reduction in intron sizes across the Y-to-dot region. Instead, deletions in intergenic regions and possibly a small ancestral Y chromosome size may explain the compact size of the Y-to-dot translocation.

De novoassembly of a young Drosophila Y chromosome using Single-Molecule sequencing and Chromatin Conformation capture

“…The Y--derived material on the dot of D. miranda amounts to approximately 300 kb, which is substantially smaller than Y chromosomes found in Drosophila [53], suggesting that Y anc presumably lost genetic material after fusing to the dot chromosome. Similar shrinkage of the Y anc was found in its sister species D. pseudoobscura [18], which shows an inversion of the Y--derived segment with respect to D. miranda ( Figure S17). The Y anc / element F fusion breakpoint is corroborated independently by a BAC clone spanning the fusion (Figure S17), validating our genome assembly in this region.…”

An investigation of Y chromosome incorporations in 400 species of Drosophila and related genera

“…azteca , and D . affinis ) all formerly Y-linked genes ( kl-2 , kl-3 , PPr-Y , ORY , and ARY ) acquired autosomal linkage [ 21 ]; mapping and sequencing experiments showed that they moved to the small "dot chromosome" [ 22 ], amazingly remaining side-by-side [ 21 , 23 ]. However, given the findings on the montium species, one may also think that the pseudoobscura lineage is similar to what we would had observed in montium if we had sampled only the auraria clade ( Fig 3 ).…”

“…melanogaster [ 58 , 59 ], although we should keep in mind that nothing is known about the rate of rearrangements in the Drosophila Y. Such test must be done by fluorescent in situ hybridization (FISH), or by a long-read assembly [ 23 ], since Sanger or Illumina assemblies are too fragmented to provide synteny information of repetitive regions. Second, since two gene copies (Y and autosomal/X-linked) seem to have co-existed for a long time, one might expect to see both in some species.…”

“…One of the best known cases was discovered in 2005: in the D . pseudoobscura lineage the ancestral Y chromosome became part of an autosome, and was replaced by a Y chromosome with unknown origin; the formerly Y-linked genes now have autosomal inheritance [ 21 – 23 ]. As a consequence, the current D .…”

The Drosophila Dot Chromosome: Where Genes Flourish Amidst Repeats

“…When linkage disequilibrium, mutation rates, and recombination rates are compared between the F–E fusion chromosome in D. willistoni and the other chromosomes, no significant differences are found, in contrast to what is typically seen for the D. melanogaster F element ( Powell et al 2011 ). Equilibration of recombination rates between two recently joined distinct domains is underway in D. busckii , where the dot chromosome is fused to the X and Y chromosomes, creating a neo-X and a neo-Y chromosome ( Zhou and Bachtrog 2015 ); the opposite example, an old Y chromosome fusing to the dot chromosome, has also been observed ( Chang and Larracuente 2017 ). In D. busckii , the F element portion of the neo-Y chromosome is undergoing rapid changes leading to degeneration, with many more single-nucleotide polymorphisms, and insertions and deletions being detected in the neo-Y than the neo-X ( Zhou and Bachtrog 2015 ).…”