Saint-Leandre, B. | bioRxiv Science

bioRxiv2023

Evolution of chemosensory tissues and cells across ecologically diverse Drosophilids

Chemosensory systems display exceptional variation between species, but little is known about how the evolution of gene expression and cell types contribute to this diversity. We have generated transcriptomes for five chemosensory tissues across six ecologically diverse Drosophila species and integrated their analyses with single-cell datasets to address these questions. The evolution of chemosensory transcriptomes has been predominantly shaped by stabilizing selection, but several thousand genes have nevertheless evolved expression changes in each tissue. Phylogenetic analyses of differentially expressed genes revealed strong evidence that their expression changes have been driven by a combination of cis-regulatory and cell composition evolution. We have also found that chemosensory-related gene families have undergone pervasive expression level changes and numerous species-specific expression gains/losses. Follow-up experiments revealed several chemoreceptors that evolved novel patterns of tissue and cellular expression that likely contribute to sensory differences. Finally, analyses of the genes that are differentially expressed between sexes uncovered extensive species-specific differences. Among these rapid changes, we discovered a D. melanogaster-specific excess of male-biased gene expression in its forelegs and identified sensory and muscle cells as the primary source of this dimorphism. Together, our analyses provide new insights for understanding evolutionary changes in ecologically key tissues at both global and individual gene levels.

evolutionary biology↗

bioRxiv2018

Diversification and collapse of a telomere elongation mechanism

In virtually all eukaryotes, telomerase counteracts chromosome erosion by adding repetitive sequence to terminal ends. Drosophila melanogaster instead relies on specialized retrotransposons that insert preferentially at telomeres. This exchange of goods between host and mobile element--wherein the mobile element provides an essential genome service and the host provides a hospitable niche for mobile element propagation--has been called a genomic symbiosis. However, these telomere-specialized, jockey family elements may actually evolve to selfishly over-replicate in the genomes that they ostensibly serve. Under this intra-genomic conflict model, we expect rapid diversification of telomere-specialized retrotransposon lineages and possibly, the breakdown of this tenuous relationship. Here we report data consistent with both predictions. Searching the raw reads of the 15-million-year-old melanogaster species group, we generated de novo jockey retrotransposon consensus sequences and used phylogenetic tree-building to delineate four distinct telomere-associated lineages. Recurrent gains, losses, and replacements account for this striking retrotransposon lineage diversity. Moreover, an ancestrally telomere-specialized element has escaped, residing now throughout the genome of D. rhopaloa. In D. biarmipes, telomere-specialized elements have disappeared completely. De novo assembly of long-reads and cytogenetics confirmed this species-specific collapse of retrotransposon-dependent telomere elongation. Instead, telomere-restricted satellite DNA and DNA transposon fragments occupy its terminal ends. We infer that D. biarmipes relies instead on a recombination-based mechanism conserved from yeast to flies to humans. Combined with previous reports of adaptive evolution at host proteins that regulate telomere length, telomere-associated retrotransposon diversification and disappearance offer compelling evidence that intra-genomic conflict shapes Drosophila telomere evolution.

evolutionary biology↗