Characterization of natural populations of Drosophila melanogaster with regard to the hobo system: a new hypothesis on the invasion

Abstract

Until now, with regard to the hobo system of hybrid dysgenesis, natural populations of Drosophila melanogaster have been investigated using only two criteria: at the molecular level, the presence or absence of XhoI fragments 2.6 kb long or smaller; and/or at the genetic level, the ability to induce gonadal dysgenesis sterility in crosses A (females of an E reference strain crossed with males under test) and A* (females under test crossed with males of an H reference strain). Recently, analyses of laboratory strains using these criteria as well as the mobilization of two reporter genes, the male recombination and the number of 'TPE' repeats in the S region, revealed a lack of correlation between the different dysgenic parameters themselves, and also between these parameters and the molecular characteristics of the strains. Thirteen current strains derived from world populations were therefore investigated with regard to all these dysgenic traits, to determine discriminating criteria providing a robust method of classifying natural populations and deducing the dynamics of hobo elements in these populations. We show, as in laboratory strains, a lack of correlation between the parameters studied. Therefore, the significance of each of them as well as the nature of hobo hybrid dysgenesis are discussed, to propose an analysis method of the hobo system applicable to natural populations. According to the geographical distribution of hobo activities in world populations and to the variable polymorphism of the number of 'TPE' repeats, we propose a new scenario for the invasion of D. melanogaster by hobo elements.

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

“…Indeed, the odds of hybrid dysgenesis among F1 females were best predicted by models that considered the paternal abundance of both P -elements and hobo elements (Table S8). 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).…”

“…In particular, ovarian atrophy can also occur in the hobo element dysgenesis syndrome (Yannopoulos et al 1986, 1987; Blackman et al 1987). In addition to lacking P -elements, many sublines of Canton-S lack canonical hobo elements ( hobo -empty) and produce dysgenic offspring in crosses with males from certain strains bearing active hobo copies (H strains, Blackman et al 1987; Pascual and Periquet 1991; Bonnivard et al 1997; Rahman et al 2015). We confirmed via PCR that canonical hobo elements are absent from our Canton-S subline, indicating that they are hobo -empty (Figure S2).…”

Genomic environment influences the dynamics of thetirantLTR retrotransposon inDrosophila

“…The only shared site among the genomes of the 3 natural populations analyzed in the present study corresponded to an insertion into the Maupiti Islands centromeric DNA, which is an A ϩ T-rich region displaying many insertions of TEs, mainly non-LTR retrotransposons, which showed a high degree of similarity with the F and doc elements (9). Of the other 18 insertions of tirant identified in the 3 genomes, 7 were found within other TEs, such as hobo (20), frogger (21), MAX (21), diver2 (22), R1 (23), and Rt1b (24). Five of the 18 insertions were heterochromatic, and the remaining 6 were found in unannotated DNA which probably corresponds to noncoding DNA.…”

hobo-induced rearrangements are responsible for mutation bursts at the yellow locus in a natural population of Drosophila melanogaster

“…The hobo element appears to have invaded the D. melanogaster genome at the beginning of this century (Periquet et al 1994;Carmena and Gonzalez 1995;Pimpinelli et al 1995;Bonnivard et al 1997). Sequences with homology to the hobo element have been found in other representatives of the melanogaster subgroup.…”