Comparative sex chromosome evolution in Drosophila robusta species group
Authors: Kamalakar chatla; Doris Bachtrog
Affiliation: University of California Berkeley
Keywords: a. genome evolution; e. heterochromatin
Neo-sex chromosomes frequently arise within the Drosophila genus through fusions between the ancestral X and Y chromosomes with autosomes. Typically, newly formed neo-Y chromosomes degenerate and become heterochromatinized, and the gene loss creates selective pressure for the homologue (neo-X) to acquire dosage compensation mechanisms to maintain proper gene dosage in males. Systematic, comparative studies are needed to study the dynamics of sex chromosome evolution, including heterochromatinization of neo-Y and dosage compensation on neo-X. In order to dissect the molecular mechanisms and evolutionary pressures driving the differentiation of these neo-sex chromosomes, we generated high-quality reference genomes, including Y chromosomes, using Nanopore single molecule sequencing combined with Hi-C scaffolding for several species with neo-sex chromosomes of varying age. We sequenced D. nigromelanica, D. melanica, D. robusta and D. lacertosa whose neo-sex chromosomes formed between 4.6 MY to 15 MY ago. The assembled Y chromosomes sizes varied from 10 Mb to 65 Mb which is inversely proportional to the age of neo-Y chromosomes. Homology to the neo-X and gene density decreased with Y age. D. nigromelanica harbors the youngest neo-Y chromosome maintaining 59% of genes, while the oldest neo-Y chromosome in D. lacertosa has less than 5% of genes remaining. All four species showed gene decay with accumulation of repetitive DNA on the neo-Y chromosome, and tandem amplification of some protein-coding genes. The neo-Y chromosome of D. nigromelanica is almost double the size of the ancestral autosome due to massive acquisition of repetitive DNA and tandem amplification of protein-coding genes. The three species carrying the older neo-sex chromosomes have fully dosage compensated neo-Xs that acquired male-specific lethal (MSL) complex binding sites. In contrast, D. nigromelanica’s neo-X is not fully dosage compensated yet. Overall, our high-quality genome assemblies help to dissect the evolutionary trajectory of neo-sex chromosomes differentiation.