While short-read sequencing technology has resulted in a sharp increase in the number of species with genome assemblies, these assemblies are typically highly fragmented. Repeats pose the largest challenge for reference genome assembly, and pericentromeric regions and the repeat-rich Y chromosome are typically ignored from sequencing projects. Here, we assemble the genome of Drosophila miranda using long reads for contig formation, chromatin interaction maps for scaffolding and short reads, and optical mapping and bacterial artificial chromosome (BAC) clone sequencing for consensus validation. Our assembly recovers entire chromosomes and contains large fractions of repetitive DNA, including about 41.5 Mb of pericentromeric and telomeric regions, and >100 Mb of the recently formed highly repetitive neo-Y chromosome. While Y chromosome evolution is typically characterized by global sequence loss and shrinkage, the neo-Y increased in size by almost 3-fold because of the accumulation of repetitive sequences. Our high-quality assembly allows us to reconstruct the chromosomal events that have led to the unusual sex chromosome karyotype in D. miranda, including the independent de novo formation of a pair of sex chromosomes at two distinct time points, or the reversion of a former Y chromosome to an autosome.

Centromeres are the basic unit for chromosome inheritance, but their evolutionary dynamics is poorly understood. We generate high-quality reference genomes for multiple Drosophila obscura group species to reconstruct karyotype evolution. All chromosomes in this lineage were ancestrally telocentric and the creation of metacentric chromosomes in some species was driven by de novo seeding of new centromeres at ancestrally gene-rich regions, independently of chromosomal rearrangements. The emergence of centromeres resulted in a drastic size increase due to repeat accumulation, and dozens of genes previously located in euchromatin are now embedded in pericentromeric heterochromatin. Metacentric chromosomes secondarily became telocentric in the pseudoobscura subgroup through centromere repositioning and a pericentric inversion. The former (peri)centric sequences left behind shrunk dramatically in size after their inactivation, yet contain remnants of their evolutionary past, including increased repeat-content and heterochromatic environment. Centromere movements are accompanied by rapid turnover of the major satellite DNA detected in (peri)centromeric regions.

The Drosophila nasuta species complex contains over a dozen recently diverged species that are distributed widely across South-East Asia, and which shows varying degrees of pre- and postzygotic isolation. Here, we assemble a high-quality genome for D. albomicans using single-molecule sequencing and chromatin conformation capture, and draft genomes for 11 additional species and 67 individuals across the clade, to infer the species phylogeny and patterns of genetic diversity in this group. Our assembly recovers entire chromosomes, and we date the origin of this radiation ∼2 Ma. Despite low levels of overall differentiation, most species or subspecies show clear clustering into their designated taxonomic groups using population genetics and phylogenetic methods. Local evolutionary history is heterogeneous across the genome, and differs between the autosomes and the X chromosome for species in the sulfurigaster subgroup, likely due to autosomal introgression. Our study establishes the nasuta species complex as a promising model system to further characterize the evolution of pre- and postzygotic isolation in this clade.

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Centromeres are the basic unit for chromosome inheritance, but their evolutionary dynamics is poorly understood. We generate high--quality reference genomes for multiple Drosophila obscura group species to reconstruct karyotype evolution. All chromosomes in this lineage were ancestrally telocentric and the creation of metacentric chromosomes in some species was driven by de novo seeding of new centromeres at ancestrally gene--rich regions, independently of chromosomal rearrangements. The emergence of centromeres resulted in a drastic size increase due to repeat accumulation, and dozens of genes previously located in euchromatin are now embedded in pericentromeric heterochromatin. Metacentric chromosomes secondarily became telocentric in the pseudoobscura subgroup through centromere repositioning and a pericentric inversion. The former (peri)centric sequences left behind shrunk dramatically in size after their inactivation, yet contain remnants of their evolutionary past, including increased repeat--content and heterochromatic environment. Centromere movements are accompanied by rapid turnover of the major satellite DNA detected in (peri)centromeric regions.

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Significance It is increasingly recognized that sex chromosomes are not only the battlegrounds between sexes but also the Great Walls fencing off introgression between diverging lineages. Here we dissect the multifaceted roles of sex chromosomes using experimental evolution, whole-genome resequencing, and theoretical modeling, taking advantage of hybrid populations between a Drosophila sister species pair in the early stage of speciation that have different sex chromosome systems. Our work sheds light onto the complex roles of neo-sex chromosome evolution in creating a sex-dependent asymmetrical introgression barrier at a species boundary, and we show how diverse population genetic forces act in concert to explain observed patterns of introgression across the genome.