Yankovskaya - REPORTS between Drosophila melanogaster and...

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between Drosophila melanogaster and Anoph- eles gambiae , although the X chromosome of the latter is smaller ( 18 ). Thus, we can test the idea of preferential loss of male-biased genes from the X chromosome. It is noteworthy that there have been translocations from X chromo- some to autosome (and vice versa) in the two lineages, which have allowed us to determine if movement to an autosome “rescues” X-chro- mosome male-biased genes from loss. When we plotted the ratio of sex-biased expression in Drosophila gonads against the probability that a homolog exists in Anopheles , two clear corre- lations were observed. In agreement with tradi- tional comparative studies on limited numbers of genes ( 19 ), genes highly expressed in males appear to change rapidly. More surprising is the strikingly tight correlation between degree of sex-biased expression and conservation. Overall, 60% (8513) of the Drosophila tran- scripts represented on the array have homologs in Anopheles ( 18 ). When we tracked changes in linkage between the species, we found that conservation is directly related to sex-biased expression ratios and to chromosomal location. The poorest conservation is between Drosoph- ila X-chromosome male-biased genes and the Anopheles X chromosome (Fig. 4A). Indeed, none of the X-chromosome genes showing greater than eightfold overexpression in Dro- sophila males are found on the Anopheles X chromosome, but this is not restricted to highly male-biased genes. There is a smooth inverse relationship between degree of male-biased ex- pression and conservation. Translocation to an autosome clearly increases the probability of conservation. The only homologs of Drosoph- ila genes with highly male-biased expression found on the Anopheles X chromosome are autosomal in Drosophila (Fig. 4B), and nearly 30% of Drosophila X chromosome, male-bi- ased genes are conserved on an Anopheles au- tosome (Fig. 4C). The best-conserved male- biased genes are autosomal in both species (Fig. 4D). Thus, continued X linkage of a gene with male-biased expression in both lineages, pre- sumably reflecting the configuration of the an- cestral X chromosome, is highly disfavored. These data unambiguously indicate that X link- age lowers the effective “life-span” of a gene with male-biased expression. Movement to the autosomes can occur by translocation or by preferential retrotransposition of male-biased genes as has been recently shown ( 20 ). It has been postulated that the X chromo- some is a favored location for evolution of male advantage alleles because of the lack of a less advantageous second allele at that locus in hem- izygotes ( 3 ). Indeed, in mammals it appears that the X chromosome is the favored location for male-biased expression, at least for a few genes expressed in primary spermatocytes ( 4 ). How- ever, this may be because of compensation, in advance, for the precocious inactivation of those X chromosomes in preparation for meiosis ( 20 ).
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Yankovskaya - REPORTS between Drosophila melanogaster and...

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