Origins and Evolutionary Patterns of the 1.688 Satellite DNA Family in Drosophila Phylogeny

Satellite DNAs (satDNAs) are a ubiquitous feature of eukaryotic genomes and are usually the major components of constitutive heterochromatin. The 1.688 satDNA, also known as the 359 bp satellite, is one of the most abundant repetitive sequences in Drosophila melanogaster and has been linked to several different biological functions. We investigated the presence and evolution of the 1.688 satDNA in 16 Drosophila genomes. We find that the 1.688 satDNA family is much more ancient than previously appreciated, being shared among part of the melanogaster group that diverged from a common ancestor ∼27 Mya. We found that the 1.688 satDNA family has two major subfamilies spread throughout Drosophila phylogeny (∼360 bp and ∼190 bp). Phylogenetic analysis of ∼10,000 repeats extracted from 14 of the species revealed that the 1.688 satDNA family is present within heterochromatin and euchromatin. A high number of euchromatic repeats are gene proximal, suggesting the potential for local gene regulation. Notably, heterochromatic copies display concerted evolution and a species-specific pattern, whereas euchromatic repeats display a more typical evolutionary pattern, suggesting that chromatin domains may influence the evolution of these sequences. Overall, our data indicate the 1.688 satDNA as the most perduring satDNA family described in Drosophila phylogeny to date. Our study provides a strong foundation for future work on the functional roles of 1.688 satDNA across many Drosophila species.

Positive Selection and Functional Divergence at Meiosis Genes That Mediate Crossing Over Across the Drosophila Phylogeny

Meiotic crossing over ensures proper segregation of homologous chromosomes and generates genotypic diversity. Despite these functions, little is known about the genetic factors and population genetic forces involved in the evolution of recombination rate differences among species. The dicistronic meiosis gene, mei-217/mei-218, mediates most of the species differences in crossover rate and patterning during female meiosis between the closely related fruitfly species, Drosophila melanogaster and D. mauritiana. The MEI-218 protein is one of several meiosis-specific mini-chromosome maintenance (mei-MCM) proteins that form a multi-protein complex essential to crossover formation, whereas the BLM helicase acts as an anti-crossover protein. Here we study the molecular evolution of five genes— mei-218, the other three known members of the mei-MCM complex, and Blm— over the phylogenies of three Drosophila species groups— melanogaster, obscura, and virilis. We then use transgenic assays in D. melanogaster to test if molecular evolution at mei-218 has functional consequences for crossing over using alleles from the distantly related species D. pseudoobscura and D. virilis. Our molecular evolutionary analyses reveal recurrent positive selection at two mei-MCM genes. Our transgenic assays show that sequence divergence among mei-218 alleles from D. melanogaster, D. pseudoobscura, and D. virilis has functional consequences for crossing over. In a D. melanogaster genetic background, the D. pseudoobscura mei-218 allele nearly rescues wildtype crossover rates but alters crossover patterning, whereas the D. virilis mei-218 allele conversely rescues wildtype crossover patterning but not crossover rates. These experiments demonstrate functional divergence at mei-218 and suggest that crossover rate and patterning are separable functions.

Transposable element dynamics are consistent across the Drosophila phylogeny, despite drastically differing content

BackgroundThe evolutionary dynamics of transposable elements (TEs) vary across the tree of life and even between closely related species with similar ecologies. In Drosophila, most of the focus on TE dynamics has been completed in Drosophila melanogaster and the overall pattern indicates that TEs show an excess of low frequency insertions, consistent with their frequent turn over and high fitness cost in the genome. Outside of D. melanogaster, insertions in the species Drosophila algonquin, suggests that this situation may not be universal, even within Drosophila. Here we test whether the pattern observed in D. melanogaster is similar across five Drosophila species that share a common ancestor more than fifty million years ago.ResultsFor the most part, TE family and order insertion frequency patterns are broadly conserved between species, supporting the idea that TEs have invaded species recently, are mostly costly and dynamics are conserved in orthologous regions of the host genomeConclusionsMost TEs retain similar activities and fitness costs across the Drosophila phylogeny, suggesting little evidence of drift in the dynamics of TEs across the phylogeny, and that most TEs have invaded species recently.

Reannotation of eight Drosophila genomes

The sequenced genomes in the Drosophila phylogeny is a central resource for comparative work supporting the understanding of the Drosophila melanogaster non-mammalian model system. These have also facilitated studying the selected and random differences that distinguish the thousands of extant species of Drosophila. However, full utility has been hampered by uneven genome annotation. We have generated a large expression profile dataset for nine species of Drosophila and trained a transcriptome assembly approach on Drosophila melanogaster to develop a pipeline that best matched the extensively curated annotation. We then applied this to the other species to add tens of thousands of new gene models per species. We also developed new orthologs to facilitate cross-species comparisons. We validated the new annotation of the distantly related Drosophila grimshawi with an extensive collection of newly sequenced cDNAs. This reannoation will facilitate understanding both the core commonalities and the species differences in this important group of model organisms.

Variable Rates of Simple Satellite Gains across the Drosophila Phylogeny

Simple satellites are tandemly repeating short DNA motifs that can span megabases in eukaryotic genomes. Because they can cause genomic instability through nonallelic homologous exchange, they are primarily found in the repressive heterochromatin near centromeres and telomeres where recombination is minimal, and on the Y chromosome, where they accumulate as the chromosome degenerates. Interestingly, the types and abundances of simple satellites often vary dramatically between closely related species, suggesting that they turn over rapidly. However, limited sampling has prevented detailed understanding of their evolutionary dynamics. Here, we characterize simple satellites from whole-genome sequences generated from males and females of nine Drosophila species, spanning 40 Ma of evolution. We show that PCR-free library preparation and postsequencing GC-correction better capture satellite quantities than conventional methods. We find that over half of the 207 simple satellites identified are species-specific, consistent with previous descriptions of their rapid evolution. Based on a maximum parsimony framework, we determined that most interspecific differences are due to lineage-specific gains. Simple satellites gained within a species are typically a single mutation away from abundant existing satellites, suggesting that they likely emerge from existing satellites, especially in the genomes of satellite-rich species. Interestingly, unlike most of the other lineages which experience various degrees of gains, the lineage leading up to the satellite-poor D. pseudoobscura and D. persimilis appears to be recalcitrant to gains, providing a counterpoint to the notion that simple satellites are universally rapidly evolving.