Limits...
Reversal of an ancient sex chromosome to an autosome in Drosophila.

Vicoso B, Bachtrog D - Nature (2013)

Bottom Line: We date this chromosomal transition to early drosophilid evolution by sequencing the genome of other Drosophilidae.We also show that patterns of biased gene expression of the dot chromosome during early embryogenesis, oogenesis and spermatogenesis resemble that of the current X chromosome.Thus, although sex chromosomes are not necessarily evolutionary end points and can revert back to an autosomal inheritance, the highly specialized genome architecture of this former X chromosome suggests that severe fitness costs must be overcome for such a turnover to occur.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, Center for Theoretical Evolutionary Genomics, University of California Berkeley, Berkeley, California 94720, USA.

ABSTRACT
Although transitions of sex-determination mechanisms are frequent in species with homomorphic sex chromosomes, heteromorphic sex chromosomes are thought to represent a terminal evolutionary stage owing to chromosome-specific adaptations such as dosage compensation or an accumulation of sex-specific mutations. Here we show that an autosome of Drosophila, the dot chromosome, was ancestrally a differentiated X chromosome. We analyse the whole genome of true fruitflies (Tephritidae), flesh flies (Sarcophagidae) and soldier flies (Stratiomyidae) to show that genes located on the dot chromosome of Drosophila are X-linked in outgroup species, whereas Drosophila X-linked genes are autosomal. We date this chromosomal transition to early drosophilid evolution by sequencing the genome of other Drosophilidae. Our results reveal several puzzling aspects of Drosophila dot chromosome biology to be possible remnants of its former life as a sex chromosome, such as its minor feminizing role in sex determination or its targeting by a chromosome-specific regulatory mechanism. We also show that patterns of biased gene expression of the dot chromosome during early embryogenesis, oogenesis and spermatogenesis resemble that of the current X chromosome. Thus, although sex chromosomes are not necessarily evolutionary end points and can revert back to an autosomal inheritance, the highly specialized genome architecture of this former X chromosome suggests that severe fitness costs must be overcome for such a turnover to occur.

Show MeSH

Related in: MedlinePlus

Gene expression in early embryos and adult gonads in outgroup Diptera speciesa. Zygotic transcription is female-biased for genes located on the X-chromosome (element F) of B. oleae, but not the autosomal element A. FPKM values were estimated by RNA-sequencing of male and female stage 5 embryos. b. Over-expression in ovary and under-expression in testis on the X-chromosome (element F) but not the autosomal element A in B. oleae (top) and S. bullata (bottom). FPKM values were estimated through RNA-sequencing of dissected testis and ovaries. Levels of significance (based on Chi-square tests for panel a and using one-tailed Wilcoxon-tests for panels b) are represented by * (p<0.05), ** (p<0.01) and *** (p<0.001). Boxes (panel b) as in Fig. 1.
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC4120283&req=5

Figure 3: Gene expression in early embryos and adult gonads in outgroup Diptera speciesa. Zygotic transcription is female-biased for genes located on the X-chromosome (element F) of B. oleae, but not the autosomal element A. FPKM values were estimated by RNA-sequencing of male and female stage 5 embryos. b. Over-expression in ovary and under-expression in testis on the X-chromosome (element F) but not the autosomal element A in B. oleae (top) and S. bullata (bottom). FPKM values were estimated through RNA-sequencing of dissected testis and ovaries. Levels of significance (based on Chi-square tests for panel a and using one-tailed Wilcoxon-tests for panels b) are represented by * (p<0.05), ** (p<0.01) and *** (p<0.001). Boxes (panel b) as in Fig. 1.

Mentions: Certain features of their genome architecture distinguish X chromosomes from autosomes: they contain sex-determining factors (Sxl in Drosophila)10, show a non-random gene content (a deficiency of male and excess of female genes in Drosophila)14, are transcriptionally inactivated during spermatogenesis15, chromosome haploidy is not lethal, and chromosome-wide regulatory mechanisms ensure balanced levels of gene expression in the heterogametic sex (the MSL-complex in Drosophila)16. Interestingly, the dot chromosome of D. melanogaster harbors several peculiar characteristics that have puzzled drosophilists for decades, but can now be understood as possible remnants of its history as an X chromosome. Specifically, the dot has a minor role in sex determination and contains feminizing factors5, with increased dosage of the dot chromosome shifting 2X:3A (autosome) intersex individuals towards female development5. Consistent with its feminizing effect, genes located on the dot chromosome generally show higher expression in female compared to male embryos during early development, similar to X-linked genes (Fig. 2a). There is also a deficit of testis and an excess of ovary expression on the dot, resembling sex-biased expression profiles of the current Drosophila X (Fig. 2b). In addition, genes on the dot chromosome are down-regulated during male meiosis (Fig 2c), mimicking the phenomenon of male germline X inactivation. Furthermore, flies with only one copy of the dot chromosome are viable and fertile, and the dot is targeted by the chromosome-specific protein POF6 (Painting of fourth), which is involved in transcriptional regulation of genes located on the dot chromosome6. This resembles the MSL-complex, the only other known protein complex that specifically targets a chromosome, and POF may be part of a putative ancestral mechanisms of dosage compensation17,18 (Fig. 2d). In some Drosophila species, POF shows male-specific binding to the X chromosome in addition to binding to the dot, further supporting its involvement in dosage compensation17. Some components of the MSL complex are necessary for normal expression of genes located on the dot19, consistent with interactions of the regulatory network for the current and former sex chromosome of Drosophila (Fig. 2e). Thus, many features of the dot chromosome in Drosophila resemble unique characteristics of the current X chromosome that distinguish it from autosomes, and can be interpreted as signatures of its former life as a differentiated X chromosome. Female-biased expression during early embryogenesis, an excess of ovary genes and a deficiency of testis genes on Muller F (but not Muller A) are observed in Diptera species were the dot segregates as the X (Fig. 3). This confirms that these peculiarities of the dot were present in the X-linked ancestor, and also shows that Muller A only acquired them once it became sex-linked in the lineage leading to Drosophila.


Reversal of an ancient sex chromosome to an autosome in Drosophila.

Vicoso B, Bachtrog D - Nature (2013)

Gene expression in early embryos and adult gonads in outgroup Diptera speciesa. Zygotic transcription is female-biased for genes located on the X-chromosome (element F) of B. oleae, but not the autosomal element A. FPKM values were estimated by RNA-sequencing of male and female stage 5 embryos. b. Over-expression in ovary and under-expression in testis on the X-chromosome (element F) but not the autosomal element A in B. oleae (top) and S. bullata (bottom). FPKM values were estimated through RNA-sequencing of dissected testis and ovaries. Levels of significance (based on Chi-square tests for panel a and using one-tailed Wilcoxon-tests for panels b) are represented by * (p<0.05), ** (p<0.01) and *** (p<0.001). Boxes (panel b) as in Fig. 1.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4120283&req=5

Figure 3: Gene expression in early embryos and adult gonads in outgroup Diptera speciesa. Zygotic transcription is female-biased for genes located on the X-chromosome (element F) of B. oleae, but not the autosomal element A. FPKM values were estimated by RNA-sequencing of male and female stage 5 embryos. b. Over-expression in ovary and under-expression in testis on the X-chromosome (element F) but not the autosomal element A in B. oleae (top) and S. bullata (bottom). FPKM values were estimated through RNA-sequencing of dissected testis and ovaries. Levels of significance (based on Chi-square tests for panel a and using one-tailed Wilcoxon-tests for panels b) are represented by * (p<0.05), ** (p<0.01) and *** (p<0.001). Boxes (panel b) as in Fig. 1.
Mentions: Certain features of their genome architecture distinguish X chromosomes from autosomes: they contain sex-determining factors (Sxl in Drosophila)10, show a non-random gene content (a deficiency of male and excess of female genes in Drosophila)14, are transcriptionally inactivated during spermatogenesis15, chromosome haploidy is not lethal, and chromosome-wide regulatory mechanisms ensure balanced levels of gene expression in the heterogametic sex (the MSL-complex in Drosophila)16. Interestingly, the dot chromosome of D. melanogaster harbors several peculiar characteristics that have puzzled drosophilists for decades, but can now be understood as possible remnants of its history as an X chromosome. Specifically, the dot has a minor role in sex determination and contains feminizing factors5, with increased dosage of the dot chromosome shifting 2X:3A (autosome) intersex individuals towards female development5. Consistent with its feminizing effect, genes located on the dot chromosome generally show higher expression in female compared to male embryos during early development, similar to X-linked genes (Fig. 2a). There is also a deficit of testis and an excess of ovary expression on the dot, resembling sex-biased expression profiles of the current Drosophila X (Fig. 2b). In addition, genes on the dot chromosome are down-regulated during male meiosis (Fig 2c), mimicking the phenomenon of male germline X inactivation. Furthermore, flies with only one copy of the dot chromosome are viable and fertile, and the dot is targeted by the chromosome-specific protein POF6 (Painting of fourth), which is involved in transcriptional regulation of genes located on the dot chromosome6. This resembles the MSL-complex, the only other known protein complex that specifically targets a chromosome, and POF may be part of a putative ancestral mechanisms of dosage compensation17,18 (Fig. 2d). In some Drosophila species, POF shows male-specific binding to the X chromosome in addition to binding to the dot, further supporting its involvement in dosage compensation17. Some components of the MSL complex are necessary for normal expression of genes located on the dot19, consistent with interactions of the regulatory network for the current and former sex chromosome of Drosophila (Fig. 2e). Thus, many features of the dot chromosome in Drosophila resemble unique characteristics of the current X chromosome that distinguish it from autosomes, and can be interpreted as signatures of its former life as a differentiated X chromosome. Female-biased expression during early embryogenesis, an excess of ovary genes and a deficiency of testis genes on Muller F (but not Muller A) are observed in Diptera species were the dot segregates as the X (Fig. 3). This confirms that these peculiarities of the dot were present in the X-linked ancestor, and also shows that Muller A only acquired them once it became sex-linked in the lineage leading to Drosophila.

Bottom Line: We date this chromosomal transition to early drosophilid evolution by sequencing the genome of other Drosophilidae.We also show that patterns of biased gene expression of the dot chromosome during early embryogenesis, oogenesis and spermatogenesis resemble that of the current X chromosome.Thus, although sex chromosomes are not necessarily evolutionary end points and can revert back to an autosomal inheritance, the highly specialized genome architecture of this former X chromosome suggests that severe fitness costs must be overcome for such a turnover to occur.

View Article: PubMed Central - PubMed

Affiliation: Department of Integrative Biology, Center for Theoretical Evolutionary Genomics, University of California Berkeley, Berkeley, California 94720, USA.

ABSTRACT
Although transitions of sex-determination mechanisms are frequent in species with homomorphic sex chromosomes, heteromorphic sex chromosomes are thought to represent a terminal evolutionary stage owing to chromosome-specific adaptations such as dosage compensation or an accumulation of sex-specific mutations. Here we show that an autosome of Drosophila, the dot chromosome, was ancestrally a differentiated X chromosome. We analyse the whole genome of true fruitflies (Tephritidae), flesh flies (Sarcophagidae) and soldier flies (Stratiomyidae) to show that genes located on the dot chromosome of Drosophila are X-linked in outgroup species, whereas Drosophila X-linked genes are autosomal. We date this chromosomal transition to early drosophilid evolution by sequencing the genome of other Drosophilidae. Our results reveal several puzzling aspects of Drosophila dot chromosome biology to be possible remnants of its former life as a sex chromosome, such as its minor feminizing role in sex determination or its targeting by a chromosome-specific regulatory mechanism. We also show that patterns of biased gene expression of the dot chromosome during early embryogenesis, oogenesis and spermatogenesis resemble that of the current X chromosome. Thus, although sex chromosomes are not necessarily evolutionary end points and can revert back to an autosomal inheritance, the highly specialized genome architecture of this former X chromosome suggests that severe fitness costs must be overcome for such a turnover to occur.

Show MeSH
Related in: MedlinePlus