The Role of Transposable Elements in Hybrid Dysgenesis

KEY CONCEPTS
- P elements are transposons that are carried in P strains of Drosophila melanogaster, but not in M strains.
- When a P male is crossed with an M female, transposition is activated.
- The insertion of P elements at new sites in these crosses inactivates many genes and makes the cross infertile.
Certain strains of D. melanogaster encounter difficulties in interbreeding. When flies from two of these strains are crossed, the progeny display “dysgenic traits”—a series of defects including
mutations, chromosomal aberrations, distorted segregation at meiosis, and reduced fertility. The appearance of these correlated defects is called hybrid dysgenesis.
Two systems responsible for hybrid dysgenesis have been identified in D. melanogaster. In the first, flies are divided into the types I (inducer) and R (reactive). Reduced fertility is seen in crosses of I males with R females, but not in the reverse direction.

In the second system, flies are divided into the two types, P (paternal contributing) and M (maternal contributing). FIGURE 1 illustrates the asymmetry of the system; a cross between a P male and an M female causes dysgenesis, but the reverse cross does not.

FIGURE 1. Hybrid dysgenesis is asymmetrical; it is induced by P male × M female crosses, but not by M male × P female crosses.
Dysgenesis is principally a phenomenon of the germ cells. In crosses involving the P-M system, the F1 hybrid flies have normal somatic tissues. Their gonads, however, do not develop normally, and the hybrids are often sterile, particularly at higher temperatures. The morphological defect in gamete development dates from the stage at which rapid cell divisions commence in the germline.
Any one of the chromosomes of a P male can induce dysgenesis in a cross with an M female. The construction of recombinant chromosomes shows that several regions within each P chromosome are able to cause dysgenesis. This suggests that a P male has sequences at many different chromosomal locations that can induce dysgenesis. The locations differ between individual P strains. The P-specific sequences are absent from chromosomes of M flies.
The nature of the P-specific sequences was first identified by mapping the DNA of w mutants found among the dysgenic hybrids. All the mutations result from the insertion of DNA into the white (w) locus. (The insertion inactivates the gene, which is required for red eye color, causing the white-eye phenotype for which the locus is named.) The inserted sequence is called the P element.
The P element insertions form a classic transposable system. Individual elements vary in length but are homologous in sequence. All P elements possess inverted terminal repeats of 31 bp and generate direct repeats of target DNA of 8 bp upon transposition.
The longest P elements are about 2.9 kb long and have four open reading frames. The shorter elements arise, apparently rather frequently, by internal deletions of a full-length P factor. Some of the shorter P elements have lost the capacity to produce the transposase, but they may be activated in trans by the enzyme coded by a complete P element.
A P strain carries 30 to 50 copies of the P element, about one-third of which are full length. The elements are absent from M strains. In a P strain the elements are carried as inert components of the genome, but they become activated to transpose when a P male is crossed with an M female.
Chromosomes from P-M hybrid dysgenic flies have P elements inserted at many new sites. The insertions inactivate the genes in which they are located and often cause chromosomal breaks. The result of the transpositions is therefore to dramatically alter the genome.