Transposable element accumulation drives size differences among polymorphic Y chromosomes in Drosophila

Y chromosomes of many species are gene poor and show low levels of
nucleotide variation, yet often display high amounts of structural
diversity. Dobzhansky cataloged several morphologically distinct Y
chromosomes in Drosophila pseudoobscura that differ in
size and shape, but the molecular causes of their dramatic size
differences are unclear. Here we use cytogenetics and long-read sequencing
to study the sequence content of polymorphic Y chromosomes in D.
pseudoobscura. We show that Y chromosomes differ by almost 2-fold in size,
ranging from 30 to 60 Mb. Most of this size difference is caused by a
handful of active transposable elements (TEs) that have recently expanded
on the largest Y chromosome, with different elements being responsible for
Y expansion on differently sized D. pseudoobscura Y’s.
We show that Y chromosomes differ in their heterochromatin enrichment,
expression of Y-enriched TEs, and also influence expression of dozens of
autosomal and X-linked genes. Intriguingly, the same helitron element that
showed the most drastic amplification on the largest Y in D.
pseudoobscura independently amplified on a polymorphic large Y
chromosome in D. affinis, suggesting that some TEs are inherently
more prone to become deregulated on Y chromosomes.