The evolution of chromosomal sex determination and dosage compensation

Dosage compensation is a mechanism by means of which the activity of X-linked or Z-linked genes is made equal in the two sexes of organisms with an XX compared to XY or ZZ compared to ZW basis of sex determination. In mammals, compensation is achieved by the inactivation of one X chromosome in somatic cells of females. In Drosophila, compensation does not involve inactivation. The two X chromosomes in females as well as the single X in males are regulated, and individual genes are thought to respond independently to the regulatory mechanism. It is proposed that in both groups of organisms the evolution of heteromorphic sex chromosomes was gradual and occurred as the direct result of the evolution of dosage compensation rather than the reverse.

http://science.sciencemag.org/content/sci/202/4369/711.full.pdf

Gene dosage compensation and the evolution of sex chromosomes.

We compare the sequences for the mitochondrial cytochrome oxidase II gene of 13 species of the Drosophila obscura group. The survey includes six members of the D. afinis subgroup, four of the D. pseudoobscura subgroup, and three of the D. obscura subgroup. In all species, the gene is 688 nucleotides in length, encoding a protein of 229 amino acids plus the first position T of the stop codon. The sequences show the typical high-transition bias for closely related species, but that bias is essentially eliminated for species pairs of >5% sequence divergence. The phylogenetic relationships in the species group are inferred using both neighbor-joining and maximum parsimony. The two procedures give comparable results, showing that the D. afinis and D. pseudoobscura subgroups are monophyletic groupings that appear to have closer affinities to one another than either has to the D. obscura subgroup. We use transversion distances to estimate times of divergence, on the basis of three different estimates of the time of separation of the D. obscura species group from the D. melanogaster group. If that event occurred 35 Mya, then we can estimate the origin of the nearctic forms at -22 Mya and the separation of the D. afinis and D. pseudoobscura subgroups at - 17 Mya.

Relationships in the Drosophila obscura species group, inferred from mitochondrial cytochrome oxidase II sequences.

Y chromosome degeneration is characterized by structural changes in the chromosome architecture and expansion of genetic inertness along the Y chromosome. It is generally assumed that the heteromorphic sex chromosome pair has developed from a pair of homologues. Several models have been suggested. We use the unique situation of the secondary sex chromosome pair, neo-Y and neo-X (X2), in Drosophila miranda to analyze molecular mechanisms involved in the evolutionary processes of Y chromosome degeneration. Due to the fusion of one of the autosomes to the Y chromosome (about 2 Mya), a neo-Y chromosome and a neo-X chromosome, designated X2, were formed. Thus, formerly autosomal genes are inherited now on a pair of sex chromosomes in D. miranda. Analyzing DNA sequences from the X2 and neo-Y region, we observed a massive accumulation of DNA insertions on the neo-Y chromosome. From the analysis of several insertion elements, we present compelling evidence that the first step in Y chromosome degeneration is driven by the accumulation of transposable elements, especially retrotransposons. An enrichment of these elements along an evolving Y chromosome could account for the switch from a euchromatic into a heterochromatic chromatin structure.

Enigma of Y chromosome degeneration: Neo-Y and Neo-X chromosomes of Drosophila miranda a model for sex chromosome evolution

Ancient Y-chromosomes of various organisms contain few active genes and an abundance of repetitive DNA. The neo-Y chromosome of Drosophila miranda is in transition from an ordinary autosome to a genetically inert Y-chromosome, while its homolog, the neo-X chromosome, is evolving partial dosage compensation. Here, I compare four large genomic regions located on the neo-sex chromosomes that contain a total of 12 homologous genes. In addition, I investigate the partial coding sequence for 56 more homologous gene pairs from the neo-sex chromosomes. Little modification has occurred on the neo-X chromosome, and genes are highly constrained at the protein level. In contrast, a diverse array of molecular changes is contributing to the observed degeneration of the neo-Y chromosome. In particular, the four large regions surveyed on the neo-Y chromosome harbor several transposable element insertions, large deletions, and a large structural rearrangement. About one-third of all neo-Y-linked genes are nonfunctional, containing either premature stop codons and/or frameshift mutations. Intact genes on the neo-Y are accumulating amino acid and unpreferred codon changes. In addition, both 5'- and 3'-flanking regions of genes and intron sequences are less constrained on the neo-Y relative to the neo-X. Despite heterogeneity in levels of dosage compensation along the neo-X chromosome of D. miranda, the neo-Y chromosome shows surprisingly uniform signs of degeneration.

/pdf/sex-chromosome-evolution-molecular-aspects-of-y-chromosome-3duu94pl6k.pdf

Sex chromosome evolution: Molecular aspects of Y-chromosome degeneration in Drosophila

SERIES of recent papers (DOBZHANSKY 1935; DOBZHANSKY and A TAN 1936; DOBZHANSKY 1937)) has described the unusual and interesting features which characterize the breeding behavior of Drosophila miranda and especially its method of sex determination. These papers have also reported the results of hybridization of miranda with the closely related and better known species, Drosophila pseudoobscura, and have given a detailed description, based on the study of the salivary gland chromosomes of the hybrids, of the similarities and differences in gene arrangement in these two species. In spite of these studies, there remained much that was obscure about the operation of the sex-chromosome mechanism, and particularly about the manner in which such an organization of the sex-determining material could have been derived from the more familiar sort'found in D . pseudoobscura and, indeed, throughout the genus Drosophila. Because of the need for more information on these interesting points, PROF. DOBZHANSKY suggested that I attempt to review and extend his observations. For this, for his kindness in furnishing me with stocks used in the investigation, and for much helpful criticism, I wish to express my gratitude to PROF. DOBZHANSKY. Helpful suggestions for the revision of the manuscript have been kindly given by PROF. F. R. IMMER and PROF. C. R. BURNHAM. To PROF. A. H. STURTEVANT, under whose direction this work was performed, I am deeply indebted for advice and encouragement. The studies here reported have been sufficient to render more understandable the operation of the sex-determining mechanism of Drosophila miranda, and to indicate the manner in which it has been derived from the type present in the common ancestor of pseudoobscura and miranda.

https://www.genetics.org/content/genetics/24/2/180.full.pdf

The Sex-Determining Mechanism of Drosophila Miranda

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The Sex-Determining Mechanism of Drosophila Miranda