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Abstract Transposable elements (TEs), despite generally being considered deleterious, represent a substantial portion of most eukaryotic genomes. Specific genomic regions, such as telomeres and pericentromeres, are often densely populated with TEs. In these regions, which tend to be gene-poor, reduced recombination shelters the genome from the deleterious effects of TEs. Here, we describe unusually large and continuous pericentromeric transposable element-rich regions in all chromosomes of the genome assembly of Pegoscapus hoffmeyeri sp. A (511.79 Mbp), a Neotropical fig wasp that is the obligate pollinator of Ficus obtusifolia. The identified pericentromeric transposable element-rich regions span nearly half (46%) of the genome, and harbor over 40% of all annotated genes, including 30% of conserved Benchmarking Universal Single-Copy Orthologs genes. We present evidence that low recombination in these transposable element-rich regions generates strong bimodal molecular evolution patterns genome-wide. Patterns of nucleotide diversity and protein-coding gene evolution in transposable element-rich regions are consistent with a reduced efficiency of selection and suggestive of strong Hill–Robertson effects. A significant reduction in third codon position GC content (GC3) in transposable element-rich regions emerged as the most distinctive gene feature differentiating genes in transposable element-rich regions from those in the rest of the genome, a pattern that likely results from the absence of GC-biased gene conversion. This remarkable bimodal compartmental genome organization in the genome of P. hoffmeyeri provides a unique example of how genome organization with compartmental transposable element distribution can lead to context-dependent gene evolution shaped by common evolutionary forces. 

Abstract Structural genomic variants are key drivers of phenotypic evolution. They can span hundreds to millions of base pairs and can thus affect large numbers of genetic elements. Although structural variation is quite common within and between species, its characterization depends upon the quality of genome assemblies and the proportion of repetitive elements. Using new high-quality genome assemblies, we report a complex and previously hidden landscape of structural divergence between the genomes of Drosophila persimilis and D. pseudoobscura, two classic species in speciation research, and study the relationships among structural variants, transposable elements, and gene expression divergence. The new assemblies confirm the already known fixed inversion differences between these species. Consistent with previous studies showing higher levels of nucleotide divergence between fixed inversions relative to collinear regions of the genome, we also find a significant overrepresentation of INDELs inside the inversions. We find that transposable elements accumulate in regions with low levels of recombination, and spatial correlation analyses reveal a strong association between transposable elements and structural variants. We also report a strong association between differentially expressed (DE) genes and structural variants and an overrepresentation of DE genes inside the fixed chromosomal inversions that separate this species pair. Interestingly, species-specific structural variants are overrepresented in DE genes involved in neural development, spermatogenesis, and oocyte-to-embryo transition. Overall, our results highlight the association of transposable elements with structural variants and their importance in driving evolutionary divergence. 

By shaping meiotic recombination, chromosomal inversions can influence genetic exchange between hybridizing species. Despite the recognized importance of inversions in evolutionary processes such as divergence and speciation, teasing apart the effects of inversions over time remains challenging. For example, are their effects on sequence divergence primarily generated through creating blocks of linkage-disequilibrium pre-speciation or through preventing gene flux after speciation? We provide a comprehensive look into the influence of inversions on gene flow throughout the evolutionary history of a classic system: Drosophila pseudoobscura and D. persimilis. We use extensive whole-genome sequence data to report patterns of introgression and divergence with respect to chromosomal arrangements. Overall, we find evidence that inversions have contributed to divergence patterns between Drosophila pseudoobscura and D. persimilis over three distinct timescales: 1) segregation of ancestral polymorphism early in the speciation process, 2) gene flow after the split of D. pseudoobscura and D. persimilis, but prior to the split of D. pseudoobscura subspecies, and 3) recent gene flow between sympatric D. pseudoobscura and D. persimilis, after the split of D. pseudoobscura subspecies. We discuss these results in terms of our understanding of evolution in this classic system and provide cautions for interpreting divergence measures in other systems.