Spontaneous gain of susceptibility suggests a novel mechanism of resistance to hybrid dysgenesis in Drosophila virilis

Funikov, Sergei; Куликова, Д. А.; Krasnov, George S.; Rezvykh, Alexander P.; Chuvakova, Lubov N.; Shostak, N. G.; Zelentsova, E. S.; Blumenstiel, Justin P.; Evgen’ev, Michael B.

doi:10.1371/journal.pgen.1007400

Cited by 6 publications

(28 citation statements)

References 37 publications

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“…We confirmed that candidate dysgenic TE copy numbers were consistently different between Strain 160 (TE+) and Strain 9 (TE-) as expected (Erwin et al 2015;Funikov et al 2018). Specifically Penelope, Polyphemus, Paris, Helena, Skippy, and Slicemaster were enriched in Strain 160 compared to Strain 9 ( Fig 1A).…”

Section: Estimates Of Copy Number and Divergence In Dysgenic Causing Tessupporting

confidence: 80%

“…Taken together, our genetic data support the inference that TEs contribute to elevated reproductive isolation observed in the interspecific cross that involves dysgenic TEs, and are inconsistent with alternative hybrid incompatibility models to explain this elevated isolation. In addition, with genomic data we also assessed which candidate TE might be responsible for observed dysgenesis patterns among inducing D. virilis strains compared to non-inducing D. virilis and D. lummei, and confirmed Polyphemus as a strong candidate (Funikov et al 2018;Hemmer et al 2019).…”

Section: Discussionmentioning

confidence: 99%

“…Therefore, we looked at relationships between candidate TEs and Penelope across D. virilis genomes, to determine which of these TEs had similar copy number distribution as Penelope. We specifically focused on Penelope, Polyphemus, Paris, Helena, Skippy, and Slicemaster, given their greater mapping abundance in inducer vs non-inducer strains (Funikov et al 2018). We used hierarchical clustering to determine the correspondence of copy number of each candidate TE and Penelope across strains.…”

Section: Estimating Copy Number Of Dysgenic Causing Elementsmentioning

confidence: 99%

“…Dysgenesis was first described within D. virilis by Lozovskaya and colleagues (Lozovskaya et al 1990) when they observed gonadal atrophy and sterility in males and females in crosses between strains that vary in transposable elements. Initially one major element, Penelope, was implicated in the dysgenic phenotype (Evgenev et al 1997), but more recent studies have inferred that Penelope cannot be the causal agent and have proposed other specific elements as the primary cause of dysgenesis (Rozhkov et al 2013;Funikov et al 2018;Hemmer et al 2019). Therefore dysgenesis in D. virilis may be more complex than described in D. melanogaster (Petrov et al 1995) because several elements might contribute to the phenotype.…”

Section: Introductionmentioning

confidence: 99%

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Hybrid incompatibility between D. virilis and D. lumei is stronger in the presence of transposable elements

Castillo

Moyle

2019

Preprint

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Although hybrid incompatibilities are readily observed in interspecific crosses, the genetic basis of most incompatibilities is still unknown. One persistent hypothesis is that hybrid dysfunction is due to a mismatch between parental genomes in selfish elements and the genes that regulate the proliferation of these elements. In this study, we evaluated the potential role of transposable elements in hybrid incompatibilities by examining hybrids between Drosophila virilis, a species that is polymorphic for the transposable element Penelope, and a closely related species, Drosophila lummei, that lacks active Penelope elements. Given the established role of Penelope elements in hybrid dysgenesis among D. virilis strains, we predicted that interspecies crosses that involve D. virilis with Penelope elements will exhibit greater hybrid incompatibility than crosses involving D. virilis without Penelope. We observed both prezygotic and postzygotic isolation, the magnitude of which was dependent on the specific cross. Using F1 and backcross experiments to rule out alternative genetic incompatibilities, we demonstrated that amplified reproductive isolation in the interspecific cross involving Penelope-carrying D. virilis can be explained by the action of TEs that induce dysgenesis within D. virilis. These experiments demonstrate that TEs can contribute to the expression of hybrid incompatibilities via presence/absence polymorphisms. Further, our data indicate that the same TEs can cause distinct incompatible phenotypes in intraspecific crosses (male sterility) compared to interspecific hybrid crosses (inviability).

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Section: Estimates Of Copy Number and Divergence In Dysgenic Causing Tessupporting

confidence: 80%

Section: Discussionmentioning

confidence: 99%

Section: Estimating Copy Number Of Dysgenic Causing Elementsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Hybrid incompatibility between D. virilis and D. lumei is stronger in the presence of transposable elements

Castillo

Moyle

2019

Preprint

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“…At least four elements are proposed to contribute to dysgenesis. Penelope and Helena are retrotransposons and Paris and Polyphemus are DNA transposons [30][31][32][33][34]. Three of these TEs (Penelope, Helena and Paris) have been previously shown to transpose and cause mutation in the germline of dysgenic progeny.…”

Section: Introductionmentioning

confidence: 99%

Hybrid dysgenesis in Drosophila virilis results in clusters of mitotic recombination and loss-of-heterozygosity but leaves meiotic recombination unaltered

et al. 2020

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Background: Transposable elements (TEs) are endogenous mutagens and their harmful effects are especially evident in syndromes of hybrid dysgenesis. In Drosophila virilis, hybrid dysgenesis is a syndrome of incomplete gonadal atrophy that occurs when males with multiple active TE families fertilize females that lack active copies of the same families. This has been demonstrated to cause the transposition of paternally inherited TE families, with gonadal atrophy driven by the death of germline stem cells. Because there are abundant, active TEs in the male inducer genome, that are not present in the female reactive genome, the D. virilis syndrome serves as an excellent model for understanding the effects of hybridization between individuals with asymmetric TE profiles. Results: Using the D. virilis syndrome of hybrid dysgenesis as a model, we sought to determine how the landscape of germline recombination is affected by parental TE asymmetry. Using a genotyping-by-sequencing approach, we generated a high-resolution genetic map of D. virilis and show that recombination rate and TE density are negatively correlated in this species. We then contrast recombination events in the germline of dysgenic versus non-dysgenic F1 females to show that the landscape of meiotic recombination is hardly perturbed during hybrid dysgenesis. In contrast, hybrid dysgenesis in the female germline increases transmission of chromosomes with mitotic recombination. Using a de novo PacBio assembly of the D. virilis inducer genome we show that clusters of mitotic recombination events in dysgenic females are associated with genomic regions with transposons implicated in hybrid dysgenesis. Conclusions: Overall, we conclude that increased mitotic recombination is likely the result of early TE activation in dysgenic progeny, but a stable landscape of meiotic recombination indicates that either transposition is ameliorated in the adult female germline or that regulation of meiotic recombination is robust to ongoing transposition. These results indicate that the effects of parental TE asymmetry on recombination are likely sensitive to the timing of transposition.

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In-Depth Satellitome Analyses of 37 Drosophila Species Illuminate Repetitive DNA Evolution in the Drosophila Genus

Ruiz‐Ruano

2022

Genome Biology and Evolution

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Satellite DNAs (SatDNA) are ubiquitously present in eukaryotic genomes and have been recently associated with several biological roles. Understanding the evolution and significance of SatDNA requires an extensive comparison across multiple phylogenetic depths. We combined the RepeatExplorer pipeline and cytogenetic approaches to conduct a comprehensive identification and analysis of the satellitome in 37 species from the genus Drosophila. We identified 188 SatDNA-like families, 112 of them being characterized for the first time. Repeat analysis within a phylogenetic framework has revealed the deeply divergent nature of SatDNA sequences in the Drosophila genus. The SatDNA content varied from 0.54% of the D. arizonae genome to 38.8% of the D. albomicans genome, with the SatDNA content often following a phylogenetic signal. Monomer size and GC-content also showed extreme variation ranging 2-570 bp and 9.1-71.4%, respectively. SatDNA families are shared among closely related species, consistent with the SatDNA library hypothesis. However, we uncovered the emergence of species-specific SatDNA families through amplification of unique or low abundant sequences in a lineage. Finally, we found that genome sizes of the Sophophora subgenus are positively correlated with transposable element content, whereas genome size in the Drosophila subgenus is positively correlated with SatDNA. This finding indicates genome size could be driven by different categories of repetitive elements in each subgenus. Altogether, we conducted the most comprehensive satellitome analysis in Drosophila from a phylogenetic perspective and generated the largest catalog of SatDNA sequences to date, enabling future discoveries in SatDNA evolution and Drosophila genome architecture.

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Spontaneous gain of susceptibility suggests a novel mechanism of resistance to hybrid dysgenesis in Drosophila virilis

Cited by 6 publications

References 37 publications

Hybrid incompatibility between D. virilis and D. lumei is stronger in the presence of transposable elements

Hybrid incompatibility between D. virilis and D. lumei is stronger in the presence of transposable elements

Hybrid dysgenesis in Drosophila virilis results in clusters of mitotic recombination and loss-of-heterozygosity but leaves meiotic recombination unaltered

In-Depth Satellitome Analyses of 37 Drosophila Species Illuminate Repetitive DNA Evolution in the Drosophila Genus

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