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Copyright 0 1987 by the Genetics Society of America X-Y Exchange and the Coevolution of the X and Y rDNA Arrays in Drosophila melanogaster M. R. Gillings,*?'R. Frankham,' J. Speirst and M. Whalley" "School .f Biological Sciences and tCommonwealth Scientijic and Industrial Research Organization, Division of Food Research, Plant Physiology Group, Macquarie University, New South Wales, 21 09, Australia Manuscript received August 18, 1986 Revised copy accepted March 5, 1987 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 Yare, 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-YLchromosomes must be found in wild populations. We have found such a chromosome. Second, the X.YL chromosome must lose the YLarm, 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. HE ribosomal RNA genes on the X and Y chro- Type 2 (T2) insertions interrupt about 15% of the T mosomes of Drosophila melanogaster show simi- rDNA repeats on both the X and Y chromosomes. larities and differences that pose important problems These insertions are not homologous to T 1 insertions in understanding the evolution of multigene families. and have a slightly different insertion point in the 28s The X and Y chromosomes each carry 200-250 genes rRNA coding region (ROIHA and GLOVER 1980; for the major ribosomal RNAs (TARTOF1975; RI- LONG,REBBERT and DAWID1980). Repeats contain- TOSSA 19'76). These genes are tandemly repeated at ing T1 or T2 insertions do not appear to contribute the nucleolus organizers (RITOSSA and SPIEGELMAN significantly to the production of mature rRNA (LONG 1965). The tandem array consists of alternating spacer and DAWID1979b; LONGet al. 1981). and rRNA coding regions. Spacers vary in size (LONG In the absence of meiotic crossing over in male and DAWID1979a), such variation being found both Drosophila the X and Y chromosomal rDNA arrays among chromosomes, and within single nucleolus or- should be evolutionarily independent and diverge. ganizers (WELLAUER,DAWID and TARTOF1978; BON- Despite the heterogeneity outlined above, the rRNAs CINELLI et al. 1983). A portion of the rDNA repeats is interrupted in the transcribed from the uninterrupted (active) rDNA 28s coding region by one of two types of nonhomolo- repeats on the X and Y chromosomes are very similar. gous insertion sequence. Type 1 (Tl) insertions are The 28s rRNAs are identical (MADENand TARTOF restricted to the X chromosome where they interrupt 1974), and only a single base difference has been about 50% of the rDNA repeats. The DNA sequences reported between the 18s rRNA transcribed from the at rDNA/Tl junctions and the location of sequences X and Y chromosomes (YAGURA,YAGURA and MURA- homologous to T 1 insertions away from the nucleolus MATSU 1979). organizer suggests these elements may be transposable How do the X and Y rDNA arrays coevolve? Re- (KIDDand GLOVER1980; PEACOCKet al. 1981; ROIHA duced rRNA gene copy numbers in the selection lines et al. 1981 ; RAE 1981). of FRANKHAM,BRISCOE and NURTHEN(1978, 1980) were generated by unequal X-Y exchanges (transloca- ' Present address: Biological and Chemical Research Institute, New South Wales Department of Agriculture, Rydalmere, N.S.W., Australia. tions) through the X and Y chromosomal nucleolus Genetics 116: 241-251 (June, 1987) 242 M. R. Gillings et al. organizers (COENand DOVER1983). This has led to LA LC the hypothesis that the coevolution of the X and Y rwr chromosomal rDNA is mediated by X-Y exchange. This hypothesis has the following predictions: 1. X-Y exchange through the nucleolus organizers must occur. 2. The X-YL product of X-Y exchange must be present in natural populations for the mechanism to be generally applicable. 3. To account for the normal karyotype, the X.YL chromosome must be at a selective disadvantage to the normal X chromosome, and/or the X-YL chromosome must be unstable. 4. rDNA variants on the X chromosome should be clustered. The X-Y exchange should result in forms donated by the Y being predominantly on the proximal side of the X nucleolus organizer, while variants specific to the X-chromosomal rDNA should be clus- SELECTION tered distally. IOW - - -- htgh -e- 5. X and Y chromosomes in long-established stocks none - should share some rDNA spacer classes, and should not have fixed differences in rRNA coding sequence variants. cantic spa 6. As TI insertions do not exist on the Y chromo- FIGURE1 .-Family tree of the abdominal bristle number selec- some, they may transpose into X chromosomal rDNA tion lines. Broad arrows indicate major X-Y exchange events and fixation of the resultant X.YL. Small arrows indicate lines that have from the nearby heterochromatin or they might even- subsequently lost all or part of the appended YL. tually be eliminated from X chromosomes by the mechanics of X-Y exchange. C(l)DX,y f/X.YL,In(l)dl-49, vof fB/YS 7. The heterochromatin of the proximal X+ and C(l)DX,yf/X.Ys, In(l)dl-49,v'f f B/YL.y3 C(l)DX,y f/X.Ys, I~(~)sc~~sc~~,y sc-/YL-scS1 proximal Ys must be homologous, as this region of the C(l)DX,yf/X-Ys, y uc wa Ct6f/YL.SCS1 Y chromosome is donated to the X chromosome by X- X*YL,y cv V/Y+ Df(Y) kl-1-/C(l)DX,y f Y exchanges. X.YL,y cv V/y+ Df(Y) kl-2-/C(I)DX,y f This paper is concerned with the evaluation of the X.YL,y cv Df(Y)k1-3-/C(l)DX, y f first four of these predictions. We present evidence X.YL, y cv V/Y+ Df (Y)kl-Z-/C(l)DX, y f X.YLYs,y w,/Y+ Df(Y) k1-3-, 4-/C(l)RM,y v bb for the occurrence of three X-Y exchanges through the rDNA, for the loss of part or all of the YL arm Stocks are described by LINDSLEYand GRELL(1968) and from X-YLchromosomes in some lines, for clustering by KENNISON(1982). rDNA variants on the chromosome and for the Generation of specific genotypes: X*/O males were gen- of X erated by crossing males from the stock of interest to presence of an X-YLchromosome in a wild population. C(l)RM,y v bb/O females. Toanalyze Y chromosomal rDNA, males from the stock of interest were crossed to BSY/C(l)DX, MATERIALS AND METHODS y f bb- := females and female progeny utilized. Y chromosome fertility factor complementation tests: Lines: The control and abdominal bristle selection lines Complementation analysis was used to test for the presence analyzed in this paper all arose from an isogenic stock of Ys or YLchromosome arms appended to the X chromo- (derived from the Canberra population) (LATTER1964) into some (X"). Males from each stock were crossed to C(l)DX/ which the fourth chromosome recessive spapol had been Ys or C(I)DX/YLvirgin females. The resultant X*/Ys or X*/ substituted. These stocks are described in detail by FRANK- YLmales were tested for fertility. HAM, BRISCOEand NURTHEN(1 978, 1980), and FRANKHAM YLfertility factor point testing: Mapping of individual (1 980). Their relationships are shown in Figure 1. CD and fertility factors on X.YL chromosomes was accomplished by CF are unselected control lines. All other lines are derived a procedure similar to that above. C(l)DX/DAY)or C(I)RM/ from the low abdominal bristle selection lines LA or LC by DAY) virgin females were crossed to males from the line of continued selection, reverse selection or relaxation of selec- interest, and the F, male progeny tested for fertility by tion. LA and LC fixed for X chromosomal bb alleles that mating to their sisters. That the FP progeny were fathered arose de novo in the lines. LA fixed for an extreme bb allele by the F1 males was confirmed by the segregation of the between generations 33 and 37, while LC fixed for a mild recessive spapo1marker in the FP. bb allele between generations 14 and 21. Mapping of the Stellate control (Ste') region: The pres- Stocks: The following stocks were used in analyses of the ence of Ste", a Y chromosomal locus mapping between kl-1 lines. and kl-2, was scored by inspection of primary spermatocytes of XI0 or X.YL/Omales.

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