Limits...
Numerous transitions of sex chromosomes in Diptera.

Vicoso B, Bachtrog D - PLoS Biol. (2015)

Bottom Line: Transcriptome analysis shows that dosage compensation has evolved multiple times in flies, consistently through up-regulation of the single X in males.However, X chromosomes generally show a deficiency of genes with male-biased expression, possibly reflecting sex-specific selective pressures.These species thus provide a rich resource to study sex chromosome biology in a comparative manner and show that similar selective forces have shaped the unique evolution of sex chromosomes in diverse fly taxa.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of California Berkeley, Berkeley, California, United States of America.

ABSTRACT
Many species groups, including mammals and many insects, determine sex using heteromorphic sex chromosomes. Diptera flies, which include the model Drosophila melanogaster, generally have XY sex chromosomes and a conserved karyotype consisting of six chromosomal arms (five large rods and a small dot), but superficially similar karyotypes may conceal the true extent of sex chromosome variation. Here, we use whole-genome analysis in 37 fly species belonging to 22 different families of Diptera and uncover tremendous hidden diversity in sex chromosome karyotypes among flies. We identify over a dozen different sex chromosome configurations, and the small dot chromosome is repeatedly used as the sex chromosome, which presumably reflects the ancestral karyotype of higher Diptera. However, we identify species with undifferentiated sex chromosomes, others in which a different chromosome replaced the dot as a sex chromosome or in which up to three chromosomal elements became incorporated into the sex chromosomes, and others yet with female heterogamety (ZW sex chromosomes). Transcriptome analysis shows that dosage compensation has evolved multiple times in flies, consistently through up-regulation of the single X in males. However, X chromosomes generally show a deficiency of genes with male-biased expression, possibly reflecting sex-specific selective pressures. These species thus provide a rich resource to study sex chromosome biology in a comparative manner and show that similar selective forces have shaped the unique evolution of sex chromosomes in diverse fly taxa.

No MeSH data available.


Related in: MedlinePlus

Assessing dosage compensation in Diptera using RNA-seq:Log2 of the male to female ratio of expression for the X (brown) and autosomes (grey) of several fly species. All boxplots represent whole-body male-to-female comparisons. Two approaches were used to identify X-linked and autosomal genes: (1) Genes were considered X-linked if their reciprocal-best-hit in D. melanogaster was located on the Muller element(s) that correspond to the X in the species, as shown in Fig. 1B and C, and (2) genes were classified as X-linked if they were located on a scaffold that had reduced male/female coverage, as shown on panel B. Scaffolds in the brown rectangles were classified as X-linked; scaffolds in the grey rectangles were classified as autosomal. The first classification was used to compare the male to female ratio of expression of genes on the X and autosomes in panel A and the second classification was used in panel C. Asterisks denote significant differences between the male to female ratio of expression on the X and the autosomes: * p < 0.05, *** p < 0.001, estimated using a Wilcoxon test. Data to generate this graph are to be found in file “S3 Data.”
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4400102&req=5

pbio.1002078.g003: Assessing dosage compensation in Diptera using RNA-seq:Log2 of the male to female ratio of expression for the X (brown) and autosomes (grey) of several fly species. All boxplots represent whole-body male-to-female comparisons. Two approaches were used to identify X-linked and autosomal genes: (1) Genes were considered X-linked if their reciprocal-best-hit in D. melanogaster was located on the Muller element(s) that correspond to the X in the species, as shown in Fig. 1B and C, and (2) genes were classified as X-linked if they were located on a scaffold that had reduced male/female coverage, as shown on panel B. Scaffolds in the brown rectangles were classified as X-linked; scaffolds in the grey rectangles were classified as autosomal. The first classification was used to compare the male to female ratio of expression of genes on the X and autosomes in panel A and the second classification was used in panel C. Asterisks denote significant differences between the male to female ratio of expression on the X and the autosomes: * p < 0.05, *** p < 0.001, estimated using a Wilcoxon test. Data to generate this graph are to be found in file “S3 Data.”

Mentions: Drosophila melanogaster has evolved dosage compensation by up-regulating the expression levels of the single-copy X-linked genes in males relative to females, thereby equalizing expression of the X chromosome between the sexes. To systematically test for the presence of dosage compensation in Diptera, we compared male to female expression ratios (M/F) of X-linked genes relative to autosomes in whole body samples in eight of our fly species, and we found that in all taxa where one of the large rods (elements A–E) has become a sex chromosome, some level of dosage compensation has also evolved, as the log2(M/F) expression of X-linked genes is well over -1, and often close to 0 (Fig. 3).


Numerous transitions of sex chromosomes in Diptera.

Vicoso B, Bachtrog D - PLoS Biol. (2015)

Assessing dosage compensation in Diptera using RNA-seq:Log2 of the male to female ratio of expression for the X (brown) and autosomes (grey) of several fly species. All boxplots represent whole-body male-to-female comparisons. Two approaches were used to identify X-linked and autosomal genes: (1) Genes were considered X-linked if their reciprocal-best-hit in D. melanogaster was located on the Muller element(s) that correspond to the X in the species, as shown in Fig. 1B and C, and (2) genes were classified as X-linked if they were located on a scaffold that had reduced male/female coverage, as shown on panel B. Scaffolds in the brown rectangles were classified as X-linked; scaffolds in the grey rectangles were classified as autosomal. The first classification was used to compare the male to female ratio of expression of genes on the X and autosomes in panel A and the second classification was used in panel C. Asterisks denote significant differences between the male to female ratio of expression on the X and the autosomes: * p < 0.05, *** p < 0.001, estimated using a Wilcoxon test. Data to generate this graph are to be found in file “S3 Data.”
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4400102&req=5

pbio.1002078.g003: Assessing dosage compensation in Diptera using RNA-seq:Log2 of the male to female ratio of expression for the X (brown) and autosomes (grey) of several fly species. All boxplots represent whole-body male-to-female comparisons. Two approaches were used to identify X-linked and autosomal genes: (1) Genes were considered X-linked if their reciprocal-best-hit in D. melanogaster was located on the Muller element(s) that correspond to the X in the species, as shown in Fig. 1B and C, and (2) genes were classified as X-linked if they were located on a scaffold that had reduced male/female coverage, as shown on panel B. Scaffolds in the brown rectangles were classified as X-linked; scaffolds in the grey rectangles were classified as autosomal. The first classification was used to compare the male to female ratio of expression of genes on the X and autosomes in panel A and the second classification was used in panel C. Asterisks denote significant differences between the male to female ratio of expression on the X and the autosomes: * p < 0.05, *** p < 0.001, estimated using a Wilcoxon test. Data to generate this graph are to be found in file “S3 Data.”
Mentions: Drosophila melanogaster has evolved dosage compensation by up-regulating the expression levels of the single-copy X-linked genes in males relative to females, thereby equalizing expression of the X chromosome between the sexes. To systematically test for the presence of dosage compensation in Diptera, we compared male to female expression ratios (M/F) of X-linked genes relative to autosomes in whole body samples in eight of our fly species, and we found that in all taxa where one of the large rods (elements A–E) has become a sex chromosome, some level of dosage compensation has also evolved, as the log2(M/F) expression of X-linked genes is well over -1, and often close to 0 (Fig. 3).

Bottom Line: Transcriptome analysis shows that dosage compensation has evolved multiple times in flies, consistently through up-regulation of the single X in males.However, X chromosomes generally show a deficiency of genes with male-biased expression, possibly reflecting sex-specific selective pressures.These species thus provide a rich resource to study sex chromosome biology in a comparative manner and show that similar selective forces have shaped the unique evolution of sex chromosomes in diverse fly taxa.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, University of California Berkeley, Berkeley, California, United States of America.

ABSTRACT
Many species groups, including mammals and many insects, determine sex using heteromorphic sex chromosomes. Diptera flies, which include the model Drosophila melanogaster, generally have XY sex chromosomes and a conserved karyotype consisting of six chromosomal arms (five large rods and a small dot), but superficially similar karyotypes may conceal the true extent of sex chromosome variation. Here, we use whole-genome analysis in 37 fly species belonging to 22 different families of Diptera and uncover tremendous hidden diversity in sex chromosome karyotypes among flies. We identify over a dozen different sex chromosome configurations, and the small dot chromosome is repeatedly used as the sex chromosome, which presumably reflects the ancestral karyotype of higher Diptera. However, we identify species with undifferentiated sex chromosomes, others in which a different chromosome replaced the dot as a sex chromosome or in which up to three chromosomal elements became incorporated into the sex chromosomes, and others yet with female heterogamety (ZW sex chromosomes). Transcriptome analysis shows that dosage compensation has evolved multiple times in flies, consistently through up-regulation of the single X in males. However, X chromosomes generally show a deficiency of genes with male-biased expression, possibly reflecting sex-specific selective pressures. These species thus provide a rich resource to study sex chromosome biology in a comparative manner and show that similar selective forces have shaped the unique evolution of sex chromosomes in diverse fly taxa.

No MeSH data available.


Related in: MedlinePlus