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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

Proportion of male- and female-biased genes on the X and the autosomes, for different tissues of D. melanogaster (A), T. minor (B), E. hians (C), M. destructor (D), and G. morsitans (E). In D. melanogaster, T. minor, E. hians, and G. morsitans, the somatic tissue corresponds to the head; in M. destructor, publicly available antenna reads were used. 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.”
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pbio.1002078.g005: Proportion of male- and female-biased genes on the X and the autosomes, for different tissues of D. melanogaster (A), T. minor (B), E. hians (C), M. destructor (D), and G. morsitans (E). In D. melanogaster, T. minor, E. hians, and G. morsitans, the somatic tissue corresponds to the head; in M. destructor, publicly available antenna reads were used. 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: We performed such an analysis by comparing gene expression on the X chromosomes of several dipteran insects to their corresponding autosomal value in D. melanogaster (a proxy for their pre–sex-linked expression), to detect up- or down-regulation of X-linked genes in males and females relative to their ancestral value (genes that are autosomal in both species were used as controls). We similarly used shore fly (E. hians) expression values to infer ancestral expression of the X in D. melanogaster. Since dosage compensation is likely absent in testis of Drosophila, somatic tissues should be the most informative to investigate the evolution of dosage compensation. We find no reduction in female X-linked gene expression relative to ancestral levels for any of the species analyzed (Fig. 4). Instead, in each of these species, dosage compensation is achieved through up-regulation of the single X chromosome of males, consistent with mechanisms similar to the one found in D. melanogaster [36]. In some of the species, the up-regulation of the male X is not sufficient to fully re-establish ancestral levels of expression, causing a slight female bias observed for somatic tissues (Fig. 5).


Numerous transitions of sex chromosomes in Diptera.

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

Proportion of male- and female-biased genes on the X and the autosomes, for different tissues of D. melanogaster (A), T. minor (B), E. hians (C), M. destructor (D), and G. morsitans (E). In D. melanogaster, T. minor, E. hians, and G. morsitans, the somatic tissue corresponds to the head; in M. destructor, publicly available antenna reads were used. 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.g005: Proportion of male- and female-biased genes on the X and the autosomes, for different tissues of D. melanogaster (A), T. minor (B), E. hians (C), M. destructor (D), and G. morsitans (E). In D. melanogaster, T. minor, E. hians, and G. morsitans, the somatic tissue corresponds to the head; in M. destructor, publicly available antenna reads were used. 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: We performed such an analysis by comparing gene expression on the X chromosomes of several dipteran insects to their corresponding autosomal value in D. melanogaster (a proxy for their pre–sex-linked expression), to detect up- or down-regulation of X-linked genes in males and females relative to their ancestral value (genes that are autosomal in both species were used as controls). We similarly used shore fly (E. hians) expression values to infer ancestral expression of the X in D. melanogaster. Since dosage compensation is likely absent in testis of Drosophila, somatic tissues should be the most informative to investigate the evolution of dosage compensation. We find no reduction in female X-linked gene expression relative to ancestral levels for any of the species analyzed (Fig. 4). Instead, in each of these species, dosage compensation is achieved through up-regulation of the single X chromosome of males, consistent with mechanisms similar to the one found in D. melanogaster [36]. In some of the species, the up-regulation of the male X is not sufficient to fully re-establish ancestral levels of expression, causing a slight female bias observed for somatic tissues (Fig. 5).

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