Multigene Family of Ribosomal DNA in Drosophila melanogaster Reveals Contrasting Patterns of Homogenization for IGS and ITS Spacer Regions: A Possible Mechanism to Resolve This Paradox

Genetics ◽  
1998 ◽  
Vol 149 (1) ◽  
pp. 243-256 ◽  
Author(s):  
Carlos Polanco ◽  
Ana I González ◽  
Álvaro de la Fuente ◽  
Gabriel A Dover

Abstract The multigene family of rDNA in Drosophila reveals high levels of within-species homogeneity and between-species diversity. This pattern of mutation distribution is known as concerted evolution and is considered to be due to a variety of genomic mechanisms of turnover (e.g., unequal crossing over and gene conversion) that underpin the process of molecular drive. The dynamics of spread of mutant repeats through a gene family, and ultimately through a sexual population, depends on the differences in rates of turnover within and between chromosomes. Our extensive molecular analysis of the intergenic spacer (IGS) and internal transcribed spacer (ITS) spacer regions within repetitive rDNA units, drawn from the same individuals in 10 natural populations of Drosophila melanogaster collected along a latitudinal cline on the east coast of Australia, indicates a relatively fast rate of X-Y and X-X interchromosomal exchanges of IGS length variants in agreement with a multilineage model of homogenization. In contrast, an X chromosome-restricted 24-bp deletion in the ITS spacers is indicative of the absence of X-Y chromosome exchanges for this region that is part of the same repetitive rDNA units. Hence, a single lineage model of homogenization, coupled to drift and/or selection, seems to be responsible for ITS concerted evolution. A single-stranded exchange mechanism is proposed to resolve this paradox, based on the role of the IGS region in meiotic pairing between X and Y chromosomes in D. melanogaster.

Genetics ◽  
2000 ◽  
Vol 155 (3) ◽  
pp. 1221-1229
Author(s):  
Carlos Polanco ◽  
Ana I González ◽  
Gabriel A Dover

Abstract Detailed analysis of variation in intergenic spacer (IGS) and internal transcribed spacer (ITS) regions of rDNA drawn from natural populations of Drosophila melanogaster has revealed contrasting patterns of homogenization although both spacers are located in the same rDNA unit. On the basis of the role of IGS regions in X-Y chromosome pairing, we proposed a mechanism of single-strand exchanges at the IGS regions, which can explain the different evolutionary trajectories followed by the IGS and the ITS regions. Here, we provide data from the chromosomal distribution of selected IGS length variants, as well as the detailed internal structure of a large number of IGS regions obtained from specific X and Y chromosomes. The variability found in the different internal subrepeat regions of IGS regions isolated from X and Y chromosomes supports the proposed mechanism of genetic exchanges and suggests that only the “240” subrepeats are involved. The presence of a putative site for topoisomerase I at the 5′ end of the 18S rRNA gene would allow for the exchange between X and Y chromosomes of some 240 subrepeats, the promoter, and the ETS region, leaving the rest of the rDNA unit to evolve along separate chromosomal lineages. The phenomenon of localized units (modules) of homogenization has implications for multigene family evolution in general.


Genetics ◽  
1989 ◽  
Vol 122 (3) ◽  
pp. 617-624 ◽  
Author(s):  
S M Williams ◽  
J A Kennison ◽  
L G Robbins ◽  
C Strobeck

Abstract The role of reciprocal recombination in the coevolution of the ribosomal RNA gene family on the X and Y chromosomes of Drosophila melanogaster was assessed by determining the frequency and nature of such exchange. In order to detect exchange events within the ribosomal RNA gene family, both flanking markers and restriction fragment length polymorphisms within the tandemly repeated gene family were used. The vast majority of crossovers between flanking markers were within the ribosomal RNA gene region, indicating that this region is a hotspot for heterochromatic recombination. The frequency of crossovers within the ribosomal RNA gene region was approximately 10(-4) in both X/X and X/Y individuals. In conjunction with published X chromosome-specific and Y chromosome-specific sequences and restriction patterns, the data indicate that reciprocal recombination alone cannot be responsible for the observed variation in natural populations.


Genetics ◽  
1987 ◽  
Vol 115 (1) ◽  
pp. 143-151
Author(s):  
Andrew G Clark

ABSTRACT Functional variation among Y chromosomes in natural populations of Drosophila melanogaster was assayed by a segregation study. A total of 36 Y chromosomes was extracted and ten generations of replacement backcrossing yielded stocks with Y chromosomes in two different genetic backgrounds. Eleven of the Y chromosomes were from diverse geographic origins, and the remaining 25 were from locally captured flies. Segregation of sexes in adult offspring was scored for the four possible crosses among the two backgrounds with each Y chromosome. Although the design confounds meiotic drive and effects on viability, statistical partitioning of these effects reveals significant variation among lines in Y chromosome segregation. Results are discussed in regards to models of Y-linked segregation and viability effects, which suggest that Y-linked adaptive polymorphism is unlikely.


Genetics ◽  
1992 ◽  
Vol 132 (2) ◽  
pp. 529-544 ◽  
Author(s):  
B D McKee ◽  
L Habera ◽  
J A Vrana

Abstract In Drosophila melanogaster males, X-Y meiotic chromosome pairing is mediated by the nucleolus organizers (NOs) which are located in the X heterochromatin (Xh) and near the Y centromere. Deficiencies for Xh disrupt X-Y meiotic pairing and cause high frequencies of X-Y nondisjunction. Insertion of cloned rRNA genes on an Xh- chromosome partially restores normal X-Y pairing and disjunction. To map the sequences within an inserted, X-linked rRNA gene responsible for stimulating X-Y pairing, partial deletions were generated by P element-mediated destabilization of the insert. Complete deletions of the rRNA transcription unit did not interfere with the ability to stimulate X-Y pairing as long as most of the intergenic spacer (IGS) remained. Within groups of deletions that lacked the entire transcription unit and differed only in length of residual IGS material, pairing ability was proportional to the dose of 240-bp intergenic spacer repeats. Deletions of the complete rRNA transcription unit or the 28S sequences alone blocked nucleolus formation, as determined by binding of an antinucleolar antibody, yet did not interfere with pairing ability, suggesting that X-Y pairing may not be mechanistically related to nucleolus formation. A model for achiasmatic pairing in Drosophila males based upon the combined action of topoisomerase I and a strand transferase is proposed.


Pteridines ◽  
1993 ◽  
Vol 4 (3) ◽  
pp. 131-137
Author(s):  
J.M. Millán ◽  
C. Nájera

SummaryIn order to carry out a genetic and biochemical analysis of pteridin pathway eye colour loci, sixteen strains of five eye colour mutants of Drosophila melanogaster (2 dke, 7 sf. 3 se, 3 Hnr and 1 bw) from natural populations were used. Four EMS mutagenesis experiments were carried out to produce induced mutants of the same loci. 54 mutants (mosaics and completes) were obtained but only 7 (4 sf, 1 bw, 1 Hnr and I dke) could be isolated. The 40.48% of the mutations were mosaics. The percentage of mutants appeared during the four first days (85.19%) was significatively higher to the percentage of mutants appeared during the four following (14.18%). Viabilities of EMS-induced mutants were similar to that of the natural ones. For the induced mutants viability at 25°C was higher than at 16°C and heterozygotes had a higher Viability than mutant homozygotes. The low mutagenesis frequencies and the lack of some metabolites for Hnr and se mutants suggest an important role of these mutants in the pteridine pathway.


Genetics ◽  
1990 ◽  
Vol 125 (3) ◽  
pp. 527-534 ◽  
Author(s):  
A G Clark

Abstract Deficiency mapping with Y autosome translocations has shown that the Y chromosome of Drosophila melanogaster carries genes that are essential to male fertility. While the qualitative behavior of these lesions provides important insight into the physiological importance of the Y chromosome, quantitative variation in effects on male fertility among extant Y chromosomes in natural populations may have a significant effect on the evolution of the Y chromosome. Here a series of 36 Y chromosome replacement lines were tested in two ways designed to detect subtle variation in effects on male fertility and total male fitness. The first test involved crossing males from the 36 lines to an excess of females in an attempt to measure differences in male mating success (virility) and male fecundity. The second test challenged males bearing each of the 36 Y chromosomes to competition in populations with males bearing a standard, phenotypically marked (BsY) chromosome. These tests indicated that the Y chromosome lines did not differ significantly in either male fertility or total fitness, but that interactions with autosomes approached significance. A deterministic population genetic model was developed allowing Y autosome interaction in fertility, and it is shown that, consistent with the experimental observations, this model cannot protect Y-linked polymorphism.


Author(s):  
Ana Marquez-Rosado ◽  
Clara García-Có ◽  
Claudia Londoño-Nieto ◽  
Pau Carazo

Sexual selection frequently promotes the evolution of aggressive behaviours that help males compete against their rivals, but which may harm females and hamper their fitness. Kin selection theory predicts that optimal male-male competition levels can be reduced when competitors are more genetically related to each other than to the population average, contributing to resolve this sexual conflict. Work in Drosophila melanogaster has spearheaded empirical tests of this idea, but studies so far have been conducted in lab-adapted populations in homogeneous rearing environments that may hamper kin recognition, and used highly skewed sex ratios that may fail to reflect average natural conditions. Here, we performed a fully factorial design with the aim of exploring how rearing environment (i.e. familiarity) and relatedness affect male-male aggression, male harassment, and overall male harm levels in a natural population of Drosophila melanogaster, under more natural conditions. Namely, we: a) manipulated relatedness and familiarity so that larvae reared apart were raised in different environments, as is common in the wild, and b) studied the effects of relatedness and familiarity under average levels of male-male competition in the field. We show that, contrary to previous findings, groups of unrelated-unfamiliar males were as likely to fight with each other and harass females than related-familiar males, and that overall levels of male harm to females were similar across treatments. Our results suggest that the role of kin selection in modulating sexual conflict is yet unclear in Drosophila melanogaster, and call for further studies that focus on natural populations and realistic socio-sexual and ecological environments.


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