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1. Patterns of crossover distribution in Drosophila mauritiana necessitate a re-thinking of the centromere effect on crossing over

   https://doi.org/10.1093/genetics/iyaf039  

   Hawley, R Scott; Price, Andrew; Li, Hua; Jagannathan, Madhav; Staber, Cynthia; Hughes, Stacie E; Williams, Stefanie; Perera, Anoja; Egidy, Rhonda R; Lawlor, Amanda; et al (March 2025, GENETICS)

   MacQueen, A (Ed.)

   Abstract We present an SNP-based crossover map for Drosophila mauritiana. Using females derived by crossing 2 different strains of D. mauritiana, we analyzed crossing over on all 5 major chromosome arms. Analysis of 105 male progeny allowed us to identify 327 crossover chromatids bearing single, double, or triple crossover events, representing 398 crossover events. We mapped the crossovers along these 5 chromosome arms using a genome sequence map that includes the euchromatin-heterochromatin boundary. Confirming previous studies, we show that the overall crossover frequency in D. mauritiana is higher than is seen in Drosophila melanogaster. Much of the increase in exchange frequency in D. mauritiana is due to a greatly diminished centromere effect. Using larval neuroblast metaphases from D. mauritiana—D. melanogaster hybrids we show that the lengths of the pericentromeric heterochromatin do not differ substantially between the species, and thus cannot explain the observed differences in crossover distribution. Using a new and robust maximum likelihood estimation tool for obtaining Weinstein tetrad distributions, we observed an increase in bivalents with 2 or more crossovers when compared with D. melanogaster. This increase in crossing over along the arms of D. mauritiana likely reflects an expansion of the crossover-available euchromatin caused by a difference in the strength of the centromere effect. The crossover pattern in D. mauritiana conflicts with the commonly accepted view of centromeres as strong polar suppressors of exchange (whose intensity is buffered by sequence nonspecific heterochromatin) and demonstrates the importance of expanding such studies into other species of Drosophila. 

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2. Turnover of retroelements and satellite DNA drives centromere reorganization over short evolutionary timescales in Drosophila

   https://doi.org/10.1371/journal.pbio.3002911  

   Courret, Cécile; Hemmer, Lucas W; Wei, Xiaolu; Patel, Prachi D; Chabot, Bryce J; Fuda, Nicholas J; Geng, Xuewen; Chang, Ching-Ho; Mellone, Barbara G; Larracuente, Amanda M (November 2024, PLOS Biology)

   Kelleher, Erin S (Ed.)

   Centromeres reside in rapidly evolving, repeat-rich genomic regions, despite their essential function in chromosome segregation. Across organisms, centromeres are rich in selfish genetic elements such as transposable elements and satellite DNAs that can bias their transmission through meiosis. However, these elements still need to cooperate at some level and contribute to, or avoid interfering with, centromere function. To gain insight into the balance between conflict and cooperation at centromeric DNA, we take advantage of the close evolutionary relationships within theDrosophila simulansclade—D.simulans,D.sechellia, andD.mauritiana—and their relative,D.melanogaster. Using chromatin profiling combined with high-resolution fluorescence in situ hybridization on stretched chromatin fibers, we characterize all centromeres across these species. We discovered dramatic centromere reorganization involving recurrent shifts between retroelements and satellite DNAs over short evolutionary timescales. We also reveal the recent origin (<240 Kya) of telocentric chromosomes inD.sechellia, where the X and fourth centromeres now sit on telomere-specific retroelements. Finally, the Y chromosome centromeres, which are the only chromosomes that do not experience female meiosis, do not show dynamic cycling between satDNA and TEs. The patterns of rapid centromere turnover in these species are consistent with genetic conflicts in the female germline and have implications for centromeric DNA function and karyotype evolution. Regardless of the evolutionary forces driving this turnover, the rapid reorganization of centromeric sequences over short evolutionary timescales highlights their potential as hotspots for evolutionary innovation. 

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3. Helicase LSH/Hells regulates kinetochore function, histone H3/Thr3 phosphorylation and centromere transcription during oocyte meiosis

   https://doi.org/10.1038/s41467-020-18009-3  

   Baumann, Claudia; Ma, Wei; Wang, Xiaotian; Kandasamy, Muthugapatti K.; Viveiros, Maria M.; De La Fuente, Rabindranath (December 2020, Nature Communications)

   null (Ed.)

   Abstract Centromeres are epigenetically determined nuclear domains strictly required for chromosome segregation and genome stability. However, the mechanisms regulating centromere and kinetochore chromatin modifications are not known. Here, we demonstrate that LSH is enriched at meiotic kinetochores and its targeted deletion induces centromere instability and abnormal chromosome segregation. Superresolution chromatin analysis resolves LSH at the inner centromere and kinetochores during oocyte meiosis. LSH knockout pachytene oocytes exhibit reduced HDAC2 and DNMT-1. Notably, mutant oocytes show a striking increase in histone H3 phosphorylation at threonine 3 (H3T3ph) and accumulation of major satellite transcripts in both prophase-I and metaphase-I chromosomes. Moreover, knockout oocytes exhibit centromere fusions, ectopic kinetochore formation and abnormal exchange of chromatin fibers between paired bivalents and asynapsed chromosomes. Our results indicate that loss of LSH affects the levels and chromosomal localization of H3T3ph and provide evidence that, by maintaining transcriptionally repressive heterochromatin, LSH may be essential to prevent deleterious meiotic recombination events at repetitive centromeric sequences. 

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4. Nested likelihood-ratio testing of the nonsynonymous:synonymous ratio suggests greater adaptation in the piRNA machinery of Drosophila melanogaster compared with Drosophila ananassae and Drosophila willistoni , two species with higher repeat content

   https://doi.org/10.1093/g3journal/jkaf017  

   Blumenstiel, Justin_P; Kingan, Sarah_B; Garrigan, Daniel; Hill, Tom; Vedanayagam, Jeffrey; Kern, ed., A. (February 2025, G3: Genes, Genomes, Genetics)

   Abstract Numerous studies have revealed a signature of strong adaptive evolution in the piwi-interacting RNA (piRNA) machinery of Drosophila melanogaster, but the cause of this pattern is not understood. Several hypotheses have been proposed. One hypothesis is that transposable element (TE) families and the piRNA machinery are co-evolving under an evolutionary arms race, perhaps due to antagonism by TEs against the piRNA machinery. A related, though not co-evolutionary, hypothesis is that recurrent TE invasion drives the piRNA machinery to adapt to novel TE strategies. A third hypothesis is that ongoing fluctuation in TE abundance leads to adaptation in the piRNA machinery that must constantly adjust between sensitivity for detecting new elements and specificity to avoid the cost of off-target gene silencing. Rapid evolution of the piRNA machinery may also be driven independently of TEs, and instead from other functions such as the role of piRNAs in suppressing sex-chromosome meiotic drive. We sought to evaluate the impact of TE abundance on adaptive evolution of the piRNA machinery in D. melanogaster and 2 species with higher repeat content—Drosophila ananassae and Drosophila willistoni. This comparison was achieved by employing a likelihood-based hypothesis testing framework based on the McDonald–Kreitman test. We show that we can reject a faster rate of adaptive evolution in the piRNA machinery of these 2 species. We propose that the high rate of adaptation in D. melanogaster is either driven by a recent influx of TEs that have occurred during range expansion or selection on other functions of the piRNA machinery. 

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5. A fast‐evolving X‐linked duplicate of importin‐α2 is overexpressed in sex‐ratio drive in Drosophila neotestacea

   https://doi.org/10.1111/mec.14928  

   Pieper, Kathleen E.; Unckless, Robert L.; Dyer, Kelly A. (December 2018, Molecular Ecology)

   Abstract Selfish genetic elements that manipulate gametogenesis to achieve a transmission advantage are known as meiotic drivers.Sex‐ratioX chromosomes (SR) are meiotic drivers that prevent the maturation of Y‐bearing sperm in male carriers to result in the production of mainly female progeny. The spread of an SR chromosome can affect host genetic diversity and genome evolution, and can even cause host extinction if it reaches sufficiently high prevalence. Meiotic drivers have evolved independently many times, though only in a few cases is the underlying genetic mechanism known. In this study we use a combination of transcriptomics and population genetics to identify widespread expression differences between the standard (ST) andsex‐ratio(SR) X chromosomes of the flyDrosophila neotestacea.We found the X chromosome is enriched for differentially expressed transcripts and that many of these X‐linked differentially expressed transcripts had elevatedK_a/K_svalues between ST and SR, indicative of potential functional differences. We identified a set of candidate transcripts, including a testis‐specific, X‐linked duplicate of the nuclear transport geneimportin‐α2that is overexpressed in SR.We find suggestions of positive selection in the lineage leading to the duplicate and that its molecular evolutionary patterns are consistent with relaxed purifying selection in ST. As these patterns are consistent with involvement in the mechanism of drive in this species, this duplicate is a strong candidate worthy of further functional investigation. Nuclear transport may be a common target for genetic conflict, as the mechanism of the autosomalSegregation Distorterdrive system inD. melanogasterinvolves the same pathway. 

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