piRNAs Are Associated with Diverse Transgenerational Effects on Gene and Transposon Expression in a Hybrid Dysgenic Syndrome of D. virilis

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.

Specific down-regulation of spermatogenesis genes targeted by 22G RNAs in hybrid sterile males associated with an X-Chromosome introgression

“…Our results support a genetic interaction between the X Chromosome and autosomes and suggest a role of the endogenous RNAi pathway in mediating the interaction. It is widely held that misregulation of piRNAs and their associated TEs is one of the major contributors to HI, especially in F1 hybrids (Erwin et al 2015). However, this is apparently not the case for the hybrid that carries a homogenous genetic background except for an Xlinked introgression fragment because we detected few changes in expression for both piRNAs and TEs in the two hybrid lines (Figs.…”

“…Few TEs show aberrant expression in the hybrid sterile males compared with C. nigoni males Overexpression of TEs is frequently found in F1 hybrids and is associated with male sterility (Rozhkov et al 2013;Erwin et al 2015). We wondered whether misregulation of TEs might be associated with the observed male sterility in the introgression lines despite the fact that they were subjected to backcrossing for at least 15 generations (Bi et al 2015).…”

“…TEs may become aberrantly activated when introduced into a new host that lacks a specific control mechanism, leading to a widespread invasion of the host genome and hybrid sterility or lethality. For example, TE mobilizations have been observed in hybrids between different marsupial species (Metcalfe et al 2007) and between Drosophila species (Shpiz et al 2014;Erwin et al 2015), though whether the TE activation is the only cause of HI remains to be determined. Two HI genes, Hmr and Lhr, genetically interact to cause hybrid lethality between D. melanogaster and D. simulans (Brideau et al 2006).…”

Reexamining the P-Element Invasion of Drosophila melanogaster Through the Lens of piRNA Silencing

“…In these examples, cotransmission through females of the two alternate alleles initiated piRNA production from the quiescent allele, which then persisted over multiple generations of maternal transmission ( Figure 6A; de Vanssay et al 2012;Erwin et al 2015). In D. melanogaster, epimutated piRNA cluster alleles have been demonstrated to maintain piRNA production for .50 generations, suggesting that some piRNA cluster epialleles are very stable (de Vanssay et al 2012).…”

“…Recent studies reveal that piRNAs act as agents of epimutation, promoting regions of the genome that are quiescent with respect to piRNA production to emerge as novel piRNA clusters (de Vanssay et al 2012;Erwin et al 2015). Therefore, in addition to the random insertion of P elements into existing piRNA clusters, novel piRNA-producing, P-element insertions could also be produced through epimutation; further facilitating the evolution to repression.…”