P elements and the determinants of hybrid dysgenesis have different dynamics of propagation in Drosophila melanogaster populations

Abstract

Intraspecific hybrid dysgenesis (HD) appears after some strains of D. melanogaster are crossed. The predominant idea is that the movement of transposable P elements causes HD. It is believed that P elements appeared in the D. melanogaster genome in the middle of the last century by horizontal transfer, simultaneously with the appearance of HD determinants. A subsequent simultaneous expansion of HD determinants and P elements occurred. We analyzed the current distribution of HD determinants in natural populations of D. melanogaster and found no evidence of their further spread. However, full-sized P elements were identified in the genomes of all analyzed natural D. melanogaster strains independent of their cytotypes. Thus, the expansion of P elements does not correlate with the expansion of HD determinants. We found that the ovaries of dysgenic females did not contain germ cells despite the equal number of primordial germ cells in early stages in dysgenic and non-dysgenic embryos. We propose that HD does not result from DNA damage caused by P element transposition, but it would be the disruption in the regulation of dysgenic ovarian formation that causes the dysgenic phenotypes.

Paternal Induction of Hybrid Dysgenesis in Drosophila melanogaster Is Weakly Correlated with Both P-Element and hobo Element Dosage

“…These results are unexpected, since hobo inducer strains have been quite rare in previous surveys of natural populations (Pascual and Periquet 1991; Bonnivard et al 1997). Indeed, most studies that have examined hybrid dysgenesis in the offspring of Canton-S females mated to recently collected male genotypes, many of which were published before hobo elements were characterized (Blackman et al 1987; Yannopoulos et al 1987), assume that paternally inherited P -elements are the only causative agents (Kidwell 1983; Anxolabéhère et al 1988; Boussy et al 1988; Itoh et al 2001, 2004; Itoh and Boussy 2002; Ogura et al 2007; Onder and Kasap 2014; Ignatenko et al 2015). Therefore, although studies in which laboratory populations are infected with P -elements unequivocally demonstrate that paternal P -elements can induce hybrid dysgenesis (Bingham et al 1982; Daniels et al 1987), our observations suggest that paternal induction that is exhibited by many recently collected wild-derived genotypes may reflect the combined action of P -elements and hobo elements.…”

Genomic analysis ofPelements in natural populations ofDrosophila melanogaster

“…To better understand the molecular basis of differences in cytotype status among populations, we investigated the relationship between GD phenotypes and P element predictions in whole genome shotgun sequences from three worldwide populations of D. melanogaster . By combining previously published GD assay data (Ignatenko et al, 2015) with P element predictions (this study) from genomic data of the same strains (Bergman & Haddrill, 2015), we show that the number of euchromatic P elements is not correlated with the degree of a GD phenotype exhibited by a strain. Furthermore, we show that populations can differ significantly in their euchromatic P element content, yet show similar distributions of GD phenotypes.…”

“…Other work posits that these phenotypes mostly arise due to RNAi-based repression mediated by piRNAs produced by telomeric P elements and the effects are amplified by RNAs produced by other P elements (Simmons et al, 2014, 2015). More recently, some authors have questioned the classical view that GD phenotypes are caused solely by P elements or whether other factors may be involved (Zakharenko & Ignatenko, 2014; Ignatenko et al, 2015).…”

“…To better understand P element invasion dynamics and the molecular mechanisms that underlie P-M hybrid dysgenesis, many studies have surveyed variation in GD phenotypes across natural populations of D. melanogaster (Kidwell, Frydryk & Novy, 1983; Anxolabehere et al, 1985; Boussy & Kidwell, 1987; Anxolabehere, Kidwell & Periquet, 1988; Anxolabehere et al, 1988; Boussy et al, 1988; Gamo et al, 1990; Matsuura et al, 1993; Itoh et al, 1999; Bonnivard & Higuet, 1999; Itoh et al, 2001, 2004, 2007; Ogura et al, 2007; Onder & Bozcuk, 2012; Onder & Kasap, 2014; Ignatenko et al, 2015). These studies reveal that in most natural strains of D. melanogaster are P, Q, or M’, but that there can be substantial variation in the frequency of GD phenotypes within and between populations.…”

“…A number of studies have also used Southern blotting, in situ hybridization to polytene chromosomes, or PCR to understand how the genomic composition of P elements varies qualitatively in relation to GD phenotypes (Todo et al, 1984; Engels, 1984; Boussy et al, 1988; Itoh et al, 1999, 2001; Itoh & Boussy, 2002; Ruiz & Carareto, 2003; Itoh et al, 2007; Onder & Kasap, 2014; Ignatenko et al, 2015). These studies have revealed that, irrespective of GD phenotype, the majority of D. melanogaster strains harbor multiple copies of full-length P elements (FP) along with multiple copies of the truncated repressor element known as “KP”, suggesting a complex relationship between the presence of different types of P elements in a genome and GD phenotypes.…”