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

Lucas W Hemmer,Brittny Smith,Guilherme B Dias,Kelley Van Vaerenberghe,Casey M Bergman,Ashley Howard,Justin P Blumenstiel

doi:10.1186/s13100-020-0205-0

Lucas W Hemmer, Brittny Smith + Show 5 more

Open Access

https://doi.org/10.1186/s13100-020-0205-0

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Abstract

BackgroundTransposable 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.ResultsUsing 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.ConclusionsOverall, 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.

Highlights

Transposable elements (TEs) are endogenous mutagens and their harmful effects are especially evident in syndromes of hybrid dysgenesis
There is a subset of F1 dysgenic progeny that do not have gonadal atrophy or decreased fertility associated with the dysgenesis phenotype
This provides a natural three-way comparison of recombination rates in F1 progeny with no TE activation, TE activation and severe germline damage, and TE activation with germline recovery

Summary

Introduction

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. When P strain males carrying multiple copies of the P element DNA transposon are mated with M strain females that lack P elements, P elements transpose in the germline, cause DNA breaks and gonadal atrophy [13, 19,20,21] These events primarily happen during early development of the offspring [22, 23], but can happen at any stage [24]. The I-R system of hybrid dysgenesis in D. melanogaster is associated with perturbation of meiosis in females and failure for eggs to hatch [25]

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