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Review
, 44, 91-112

Evolution of Sex Chromosomes in Insects

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Review

Evolution of Sex Chromosomes in Insects

Vera B Kaiser et al. Annu Rev Genet.

Abstract

Sex chromosomes have many unusual features relative to autosomes. Y (or W) chromosomes lack genetic recombination, are male- (female-) limited, and show an abundance of genetically inert heterochromatic DNA but contain few functional genes. X (or Z) chromosomes also show sex-biased transmission (i.e., X chromosomes show female-biased and Z-chromosomes show male-biased inheritance) and are hemizygous in the heterogametic sex. Their unusual ploidy level and pattern of inheritance imply that sex chromosomes play a unique role in many biological processes and phenomena, including sex determination, epigenetic chromosome-wide regulation of gene expression, the distribution of genes in the genome, genomic conflict, local adaptation, and speciation. The vast diversity of sex chromosome systems in insects--ranging from the classical male heterogametic XY system in Drosophila to ZW systems in Lepidoptera or mobile genes determining sex as found in house flies--implies that insects can serve as unique model systems to study various functional and evolutionary aspects of these different processes.

Figures

Figure 1
Figure 1
Model of the evolution of sex chromosomes from a hermaphroditic state (40, 44). (a) A homologous pair of autosomes acquires two sex-determining loci, thereby turning into a proto-X and proto-Y chromosome; the proto-Y carries a dominant female suppressor (SuF) and male fertility locus (M), and the proto-X carries a female fertility (F) and male sterility (m) locus. Recombination becomes restricted between these loci (dark gray) to prevent the production of infertile neuter individuals. (b) Recombination suppression extends as a result of the insertion of transposable elements (TEs) and other noncoding sequences on the Y, chromosomal rearrangements, and the acquisition of sexually antagonistic genes (SA) that carry different alleles on the X and Y chromosomes. The X and Y only recombine in a small region, the pseudoautosomal region (PAR). (c) The Y chromosome accumulates further male fertility genes (M2), whereas the X accumulates sexually antagonistic (female-beneficial or male-beneficial) genes (SA).
Figure 2
Figure 2
Evolution of neo-sex chromosomes in Drosophila. (a) The karyotype of the male is XY AA, and the female is XX AA. (b) The Y chromosome fuses with one of the autosomes, creating a neo-Y chromosome that segregates from the neo-X in males. The neo-X behaves like a normal autosome in females. The lack of recombination in male Drosophila ensures that the neo-Y chromosome is genetically isolated from the neo-X; i.e., there is no genetic exchange between these chromosomes (which implies that the neo-Y chromosome is completely sheltered from recombination). (c) After some time, the nonrecombining neo-Y will degenerate, just like the original Y chromosome did.
Figure 3
Figure 3
Two-step model of dosage compensation in Drosophila melanogaster. In males, high-affinity sites (HAS) on the X chromosome are bound by the MSL complex in a sequence-specific manner. Binding of the complex spreads in cis from the entry site and activates transcription of X-linked genes by acetylation of their histone proteins. A higher rate of transcription from the X in males is indicated by larger amounts of mRNA produced ( green lines). In females, the male-specific lethal (MSL) complex is not assembled.

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