X-Y Exchange and the Coevolution of the X and Y rDNA Arrays in Drosophila melanogaster

Abstract

The nucleolus organizers on the X and Y chromosomes of Drosophila melanogaster are the sites of 200-250 tandemly repeated genes for ribosomal RNA. As there is no meiotic crossing over in male Drosophila, the X and Y chromosomal rDNA arrays should be evolutionarily independent, and therefore divergent. The rRNAs produced by X and Y are, however, very similar, if not identical. Molecular, genetic and cytological analyses of a series of X chromosome rDNA deletions (bb alleles) showed that they arose by unequal exchange through the nucleolus organizers of the X and Y chromosomes. Three separate exchange events generated compound X·YL chromosomes carrying mainly Y-specific rDNA. This led to the hypothesis that X-Y exchange is responsible for the coevolution of X and Y chromosomal rDNA. We have tested and confirmed several of the predictions of this hypothesis: First, X·YL chromosomes must be found in wild populations. We have found such a chromosome. Second, the X·YL chromosome must lose the YL arm, and/or be at a selective disadvantage to normal X+ chromosomes, to retain the normal morphology of the X chromosome. Six of seventeen sublines founded from homozygous X·YLbb stocks have become fixed for chromosomes with spontaneous loss of part or all of the appended YL. Third, rDNA variants on the X chromosome are expected to be clustered within the X+ nucleolus organizer, recently donated ("Y") forms being proximal, and X-specific forms distal. We present evidence for clustering of rRNA genes containing Type 1 insertions. Consequently, X-Y exchange is probably responsible for the coevolution of X and Y rDNA arrays.

Clustering of rDNA containing type 1 insertion sequence in the distal nucleolus organiser ofDrosophila melanogaster: implications for the evolution of X and Y rDNA arrays

“…Sample volumes used for loading the gels described herein were adjusted correspondingly to achieve equal concentrations of DNA. Details of all the methods can be found in Gillings et al (1987).…”

“…Conversely, De Cicco & Glover (1983), Hawley & Tartof (1983), Palumbo, Endow & Hawley (1984) and Dutton & Krider (1984) have all claimed that rRNA genes containing Tl insertions are randomly dispersed throughout the X chromosomal nucleolus organizer. Gillings et al (1987) pointed out shortcomings in interpretations in the latter studies. reported that about 90% of Tl insertions were clustered in the distal nucleolus organizer and heterochromatin of the In(l)sc v2 chromosome.…”

“…Evidence for the clustering of variants within the X nucleolus organizer is equivocal. Renkawitz-Pohl, Glatzer & Kunz (1981), Sharp, Gandhi & Procunier (1983), Kalumuck & Procunier (1984), Salzano & Malva (1984), Terracol & Prud'homme (1986) and Gillings et al (1987) have reported evidence for clustering of rDNA containing Tl insertions in D. melanogaster and D. hydei, but they did not determine the location of the clusters. Conversely, De Cicco & Glover (1983), Hawley & Tartof (1983), Palumbo, Endow & Hawley (1984) and Dutton & Krider (1984) have all claimed that rRNA genes containing Tl insertions are randomly dispersed throughout the X chromosomal nucleolus organizer.…”

“…1, two compound chromosomes are generated: a Y S X. which functions neither as an X nor a Y, and an X. Y L which behaves like an A'chromosome. These X-Y exchange products have been detected by Coen & Dover (1983) and Gillings et al (1987) in Drosophila lines selected for low abdominal bristle number (Frankham, Briscoe Nurthen, 1978, 1980Frankham, 1980). The X-Y exchange results in Y chromosomal rDNA being donated to the X chromosome but not vice versa.…”

“…The X-Y exchange results in Y chromosomal rDNA being donated to the X chromosome but not vice versa. This Y chromosomal rDNA can enter cytologically ' normal' X chromosomes by the X. Y L chromosome losing the Y L arm, as observed by Gillings et al (1987). Alternatively, exchange between X. Y L and normal X chromosomes may result in such transfer.…”