Abstract
Sexual reproduction allows transposable elements (TEs) to proliferate, leading to rapid divergence between populations and species. A significant outcome of divergence in the TE landscape is evident in hybrid dysgenic syndromes, a strong form of genomic incompatibility that can arise when (TE) family abundance differs between two parents. When TEs inherited from the father are absent in the mother's genome, TEs can become activated in the progeny, causing germline damage and sterility. Studies in Drosophila indicate that dysgenesis can occur when TEs inherited paternally are not matched with a pool of corresponding TE silencing PIWI-interacting RNAs (piRNAs) provisioned by the female germline. Using the D. virilis syndrome of hybrid dysgenesis as a model, we characterize the effects that divergence in TE profile between parents has on offspring. Overall, we show that divergence in the TE landscape is associated with persisting differences in germline TE expression when comparing genetically identical females of reciprocal crosses and these differences are transmitted to the next generation. Moreover, chronic and persisting TE expression coincides with increased levels of genic piRNAs associated with reduced gene expression. Combined with these effects, we further demonstrate that gene expression is idiosyncratically influenced by differences in the genic piRNA profile of the parents that arise though polymorphic TE insertions. Overall, these results support a model in which early germline events in dysgenesis establish a chronic, stable state of both TE and gene expression in the germline that is maintained through adulthood and transmitted to the next generation. This work demonstrates that divergence in the TE profile is associated with diverse piRNA-mediated transgenerational effects on gene expression within populations.
Highlights
In sexually reproducing species, two unique haploid genomes join together in syngamy to establish each generation
Studies in the fruit flies Drosophila melanogaster and D. virilis have been important in demonstrating a role for RNA silencing by PIWI-interacting RNAs in protecting the genome against these harmful elements
They are transmitted by the female germline to offspring in order to maintain a stable genome across generations
Summary
Two unique haploid genomes join together in syngamy to establish each generation. Because syngamy can introduce selfish elements to new genomes and recombination can separate selfish elements from their harmful consequences, selfish elements such as transposable elements (TEs) can proliferate [2,3] This is exemplified by the P element in Drosophila melanogaster. Because TEs can be harmful and drive a rapid accumulation of differences between species, they have been proposed to contribute to reproductive isolation While their proliferative nature makes it very unlikely that TEs are drivers of speciation itself [6,7], TE misregulation has been observed in a variety of interspecific hybrids. Interspecific hybrids between D. simulans and D. melanogaster (which are more distantly related compared to those in previous crosses examining this question [6,7]) do show increased expression of TEs [15] and this is attributed to adaptive divergence in components of the TE regulatory machinery. Since species may differ significantly both in TE profile and regulatory machinery protein function, it is challenging to determine how divergence in TE profile alone contributes to TE activation in interspecific hybrids
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