Molecular aspects of intron evolution in dynein encoding mega-genes on theheterochromatic Y chromosome of Drosophila sp.

Fertility genes on the heterochromatic Y chromosome of various Drosophila s pecies are unique for several reasons. Most of them are megabase-sized. The ir expression is restricted to premeiotic spermatocytes and often associate d with unfolding of huge species-specific lampbrush loops. Molecular analys is of the orthologous dynein genes Dhc-Yh3, DhDhc7(Y) and DeDhc7(Y) on the Y chromosome of the three species D. melanogaster, D. hydei and D. eohydei, respectively, revealed that the megabase gene size as well as the species- specific morphology of the corresponding lampbrush loops kl-5, Threads and diffuse loops result from huge introns and their specific sequence composit ion, whereas the majority of all 20 introns in each of the three genes is i n a size of 45-72 bp. The loop-specifying introns are extreme exceptions du e to extended assemblies of degenerated transposable elements and/or large clusters of satellite DNAs. Here we use sequence information from the compl ete intron sets of three orthologous Y chromosomal dynein genes to deduce a scenario for an evolutionary pathway leading to the megabase-sized genes o n the heterochromatic Y chromosome of Drosophila. The obvious bias between very small and species-specific mega introns is explained as the result of an autocatalytic mode of intron growth. An initial coincidental hit by a si ngle transposable element extends the size of a 50 bp intron for about two orders of magnitude and determines it for preferential extension by similar insertion events. This phase of continuous moderate growth is followed by rapid size enlargements by repeating amplifications generating extended clu sters of satellite DNA. Size control by recombination, on the other hand, i s suppressed in Drosophila males by achiasmatic meiosis.