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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

Sex chromosomes in Diptera, mapped along a fly phylogeny [13].Different chromosomal elements (designated elements A–F) have become sex-linked in different families of Diptera (indicated by different colors along the phylogeny). Elements were classified as X-linked when they were over-represented among our candidate X scaffolds, based on their male/female coverage (see Materials and Methods and S1–S3 Figs.) or if they showed an excess of SNPs in the heterogametic sex (Figs. 2 and S5). Bold lines indicate a transition of a sex chromosome at a particular branch of the tree and was inferred using parsimony. Dashed lines indicate instances where partial Muller elements segregate as a sex chromosome (see Figs. 2 and S5, S6 and S1 Table for more details). Data to generate the phylogeny are to be found in file “S2 Text” and “S3 Text.” Images drawn by Doris Bachtrog.
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pbio.1002078.g001: Sex chromosomes in Diptera, mapped along a fly phylogeny [13].Different chromosomal elements (designated elements A–F) have become sex-linked in different families of Diptera (indicated by different colors along the phylogeny). Elements were classified as X-linked when they were over-represented among our candidate X scaffolds, based on their male/female coverage (see Materials and Methods and S1–S3 Figs.) or if they showed an excess of SNPs in the heterogametic sex (Figs. 2 and S5). Bold lines indicate a transition of a sex chromosome at a particular branch of the tree and was inferred using parsimony. Dashed lines indicate instances where partial Muller elements segregate as a sex chromosome (see Figs. 2 and S5, S6 and S1 Table for more details). Data to generate the phylogeny are to be found in file “S2 Text” and “S3 Text.” Images drawn by Doris Bachtrog.

Mentions: We use whole-genome analysis in 37 species belonging to 22 different families of Diptera to infer the presence and identity of sex chromosomes (Table 1). While the identification of sex chromosomes traditionally involved the creation of labor-intensive genetic or physical maps, we have previously developed a bioinformatics approach to detect X-derived sequences based on their male and female genomic coverage using next-generation sequencing data [10,11]. We therefore independently sequenced males and females from each species to roughly a similar sequencing depth and used sequence coverage information to identify the absence or presence of differentiated sex chromosomes. In particular, when the Y is fully differentiated, X-linked genes show only half as many reads from genomic DNA in males, where they are present in one copy only, relative to females; autosomes or undifferentiated regions of the sex chromosomes have similar coverage in male and female samples (see Materials and Methods). Additionally, analysis of single nucleotide polymorphisms (SNPs) in males versus females was utilized to identify recently formed sex chromosomes where the X and Y still share considerable homology, through increased SNP density (early X-Y differentiation) at nascent sex chromosomes in the heteromorphic sex, relative to autosomal SNPs (see section “Young Sex Chromosomes”). It should be noted that sequences derived from differentiated Y-chromosomes are notoriously difficult to assemble and generally have much lower mapping scores to known genes than X-derived sequences [12], so that they are not found in our analysis. We further use comparative mapping (to either the D. melanogaster genome for Brachycera species, or to both the D. melanogaster and the Anopheles gambiae genomes for Nematocera; see Materials and Methods for details), to identify which Muller element(s) segregate(s) as sex chromosomes in each species (S1–S3 Figs.). Muller elements that had a significant excess of X-candidate scaffolds (based on sequence coverage) were classified as sex-linked (S3 Fig.). This was combined with SNP information to identify young sex chromosomes (see section “Young sex chromosomes”). Using this approach, we identify over a dozen different sex chromosome configurations in the species investigated (Fig. 1).


Numerous transitions of sex chromosomes in Diptera.

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

Sex chromosomes in Diptera, mapped along a fly phylogeny [13].Different chromosomal elements (designated elements A–F) have become sex-linked in different families of Diptera (indicated by different colors along the phylogeny). Elements were classified as X-linked when they were over-represented among our candidate X scaffolds, based on their male/female coverage (see Materials and Methods and S1–S3 Figs.) or if they showed an excess of SNPs in the heterogametic sex (Figs. 2 and S5). Bold lines indicate a transition of a sex chromosome at a particular branch of the tree and was inferred using parsimony. Dashed lines indicate instances where partial Muller elements segregate as a sex chromosome (see Figs. 2 and S5, S6 and S1 Table for more details). Data to generate the phylogeny are to be found in file “S2 Text” and “S3 Text.” Images drawn by Doris Bachtrog.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4400102&req=5

pbio.1002078.g001: Sex chromosomes in Diptera, mapped along a fly phylogeny [13].Different chromosomal elements (designated elements A–F) have become sex-linked in different families of Diptera (indicated by different colors along the phylogeny). Elements were classified as X-linked when they were over-represented among our candidate X scaffolds, based on their male/female coverage (see Materials and Methods and S1–S3 Figs.) or if they showed an excess of SNPs in the heterogametic sex (Figs. 2 and S5). Bold lines indicate a transition of a sex chromosome at a particular branch of the tree and was inferred using parsimony. Dashed lines indicate instances where partial Muller elements segregate as a sex chromosome (see Figs. 2 and S5, S6 and S1 Table for more details). Data to generate the phylogeny are to be found in file “S2 Text” and “S3 Text.” Images drawn by Doris Bachtrog.
Mentions: We use whole-genome analysis in 37 species belonging to 22 different families of Diptera to infer the presence and identity of sex chromosomes (Table 1). While the identification of sex chromosomes traditionally involved the creation of labor-intensive genetic or physical maps, we have previously developed a bioinformatics approach to detect X-derived sequences based on their male and female genomic coverage using next-generation sequencing data [10,11]. We therefore independently sequenced males and females from each species to roughly a similar sequencing depth and used sequence coverage information to identify the absence or presence of differentiated sex chromosomes. In particular, when the Y is fully differentiated, X-linked genes show only half as many reads from genomic DNA in males, where they are present in one copy only, relative to females; autosomes or undifferentiated regions of the sex chromosomes have similar coverage in male and female samples (see Materials and Methods). Additionally, analysis of single nucleotide polymorphisms (SNPs) in males versus females was utilized to identify recently formed sex chromosomes where the X and Y still share considerable homology, through increased SNP density (early X-Y differentiation) at nascent sex chromosomes in the heteromorphic sex, relative to autosomal SNPs (see section “Young Sex Chromosomes”). It should be noted that sequences derived from differentiated Y-chromosomes are notoriously difficult to assemble and generally have much lower mapping scores to known genes than X-derived sequences [12], so that they are not found in our analysis. We further use comparative mapping (to either the D. melanogaster genome for Brachycera species, or to both the D. melanogaster and the Anopheles gambiae genomes for Nematocera; see Materials and Methods for details), to identify which Muller element(s) segregate(s) as sex chromosomes in each species (S1–S3 Figs.). Muller elements that had a significant excess of X-candidate scaffolds (based on sequence coverage) were classified as sex-linked (S3 Fig.). This was combined with SNP information to identify young sex chromosomes (see section “Young sex chromosomes”). Using this approach, we identify over a dozen different sex chromosome configurations in the species investigated (Fig. 1).

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