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Y chromosomes across diverse species convergently evolve a gene-poor, heterochromatic organization enriched for duplicated genes, LTR retrotransposons, and satellite DNA. Sexual antagonism and a loss of recombination play major roles in the degeneration of young Y chromosomes. However, the processes shaping the evolution of mature, already degenerated Y chromosomes are less well-understood. Because Y chromosomes evolve rapidly, comparisons between closely related species are particularly useful. We generated de novo long-read assemblies complemented with cytological validation to reveal Y chromosome organization in three closely related species of the Drosophila simulans complex, which diverged only 250,000 years ago and share >98% sequence identity. We find these Y chromosomes are divergent in their organization and repetitive DNA composition and discover new Y-linked gene families whose evolution is driven by both positive selection and gene conversion. These Y chromosomes are also enriched for large deletions, suggesting that the repair of double-strand breaks on Y chromosomes may be biased toward microhomology-mediated end joining over canonical non-homologous end-joining. We propose that this repair mechanism contributes to the convergent evolution of Y chromosome organization across organisms. 

The rapid evolution of repetitive DNA sequences, including satellite DNA, tandem duplications, and transposable elements, underlies phenotypic evolution and contributes to hybrid incompatibilities between species. However, repetitive genomic regions are fragmented and misassembled in most contemporary genome assemblies. We generated highly contiguous de novo reference genomes for the Drosophila simulans species complex ( D. simulans , D. mauritiana , and D. sechellia ), which speciated ∼250,000 yr ago. Our assemblies are comparable in contiguity and accuracy to the current D. melanogaster genome, allowing us to directly compare repetitive sequences between these four species. We find that at least 15% of the D. simulans complex species genomes fail to align uniquely to D. melanogaster owing to structural divergence—twice the number of single-nucleotide substitutions. We also find rapid turnover of satellite DNA and extensive structural divergence in heterochromatic regions, whereas the euchromatic gene content is mostly conserved. Despite the overall preservation of gene synteny, euchromatin in each species has been shaped by clade- and species-specific inversions, transposable elements, expansions and contractions of satellite and tRNA tandem arrays, and gene duplications. We also find rapid divergence among Y-linked genes, including copy number variation and recent gene duplications from autosomes. Our assemblies provide a valuable resource for studying genome evolution and its consequences for phenotypic evolution in these genetic model species. 

Glowing fireflies dancing in the dark are one of the most enchanting sights of a warm summer night. Their light signals are ‘love messages’ that help the insects find a mate – yet, they also warn a potential predator that these beetles have powerful chemical defenses. The light comes from a specialized organ of the firefly where a small molecule, luciferin, is broken down by the enzyme luciferase. Fireflies are an ancient group, with the common ancestor of the two main lineages originating over 100 million years ago. But fireflies are not the only insects that produce light: certain click beetles are also bioluminescent. Fireflies and click beetles are closely related, and they both use identical luciferin and similar luciferases to create light. This would suggest that bioluminescence was already present in the common ancestor of the two families. However, the specialized organs in which the chemical reactions take place are entirely different, which would indicate that the ability to produce light arose independently in each group. Here, Fallon, Lower et al. try to resolve this discrepancy and to find out how many times bioluminescence evolved in beetles. This required using cutting-edge DNA sequencing to carefully piece together the genomes of two species of fireflies (Photinus pyralis and Aquatica lateralis) and one species of click beetle (Ignelater luminosus). The genetic analysis revealed that, in all species, the genes for luciferases were very similar to the genetic sequences around them, which code for proteins that break down fat. This indicates that the ancestral luciferase arose from one of these metabolic genes getting duplicated, and then one of the copies evolving a new role. However, the genes for luciferase were very different between the fireflies and the click beetles. Further analyses suggested that bioluminescence evolved at least twice: once in an ancestor of fireflies, and once in the ancestor of the bioluminescent click beetles. More results came from the reconstituted genomes. For example, Fallon, Lower et al. identified the genes ‘turned on’ in the bioluminescent organ of the fireflies. This made it possible to list genes that may be involved in creating luciferin, and enable flies to grow brightly for long periods. In addition, the genetic information yielded sequences from bacteria that likely live inside firefly cells, and which may participate in the light-making process or the production of potent chemical defenses. Better genetic knowledge of beetle bioluminescence could bring new advances for both insects and humans. It may help researchers find and design better light-emitting molecules useful to track and quantify proteins of interest in a cell. Ultimately, it would allow a detailed understanding of firefly populations around the world, which could contribute to firefly ecotourism and help to protect these glowing insects from increasing environmental threats.