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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.

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Turnover of sex chromosomes in DrosophilaHypothetical transition from an ancestral karyotype with element F segregating as a sex chromosome, to the karyotype observed in Drosophila where element A is the sex chromosome. In outgroup species, maleness is determined by the presence of a factor on the Y chromosome (M-factor). Element A could either have acquired a new, epistatic M*-factor (scenario I), or the existing M-factor could have transposed to element A (scenario II). This transition could also have been initiated by a fusion of the ancestral Y to element A (scenario III). Degeneration of the male-limited, non-recombining element A, followed by recruitment of Sxl for sex determination would create the ancestral karyotype of Drosophila.
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Figure 4: Turnover of sex chromosomes in DrosophilaHypothetical transition from an ancestral karyotype with element F segregating as a sex chromosome, to the karyotype observed in Drosophila where element A is the sex chromosome. In outgroup species, maleness is determined by the presence of a factor on the Y chromosome (M-factor). Element A could either have acquired a new, epistatic M*-factor (scenario I), or the existing M-factor could have transposed to element A (scenario II). This transition could also have been initiated by a fusion of the ancestral Y to element A (scenario III). Degeneration of the male-limited, non-recombining element A, followed by recruitment of Sxl for sex determination would create the ancestral karyotype of Drosophila.

Mentions: How could this transition have happened? Sex in most outgroup species of Drosophila is determined by the presence of a factor on the Y chromosome (M-factor) causing maleness20. Such a dominant-Y system with element F as the sex chromosome could evolve into the Drosophila system (dose-dependent sex determination with element A as the sex chromosome), through various intermediate steps1, and we outline three possible paths that involve mutational events that have been observed in Diptera. This sex chromosome transition could be initiated by a single epistatic mutation on element A (M*) that makes individuals male regardless of their sex chromosome karyotype, or through a translocation of the existing male-determining factor (M) onto element A (Fig. 4). Novel sex determining genes occurring on different chromosomes or translocations of M-factors onto autosomes have been observed in houseflies21 or humpbacked flies22. The fixation of the new male-determining gene on element A would lead to reversal of the ancestral X (Muller F) to an autosome, and the ancestral Y would be completely lost. Loss of the Y is only possible if the ancestral Y chromosome carried no essential male-fertility genes, as seems to be the case in several Diptera species21, or if those male-fertility genes move to another chromosome23. The emergence of a male-determining gene on element A would cause male-limited transmission of this chromosome and - since higher Diptera males generally lack recombination24 - set in motion genome-wide degeneration of the non-recombining proto-Y. Eventually, Sxl was recruited as a dose-dependent sex determination gene in Drosophila, and MSL-mediated dosage compensation evolved on element A16. The current karyotype of Drosophila could also have evolved through a chromosomal fusion between the ancestral Y chromosome and element A (Fig. 4). This would create a male-limited neo-Y (the fused element A) that initially is identical to the neo-X (the unfused element A). The non-recombining neo-Y would undergo chromosome-wide degeneration, and Y-autosome fusions coupled with neo-Y degeneration have happened repeatedly in several Drosophila species and other Diptera12,25. This fused neo-Y chromosome would form the current Y of Drosophila, and male-fertility genes, if present on the ancestral Y, could be preserved on the chimeric Y. Both element F and element A would simultaneously segregate as X chromosomes, and eventually Sxl would take over the sex determining function on element A, and a non-disjunction event could restore diploidy for element F in both sexes. Thus, under both the translocation of an existing or the emergence of a new M-factor scenario, the current Y chromosome of Drosophila shares no homology to the Y of its ancestor, while under the chromosomal fusion model, the current Drosophila Y is a chimera of the ancestral Y and the degenerated element A and may thus harbor some genes that are also Y-linked in outgroup species. We detect no Y-linked protein-coding genes that are shared between Drosophila and Diptera where Muller F is the sex chromosome (Table S3–S5, Fig S8–S10), providing some support against a fusion between the new and ancestral Y. However, it should be noted that the gene content of the Y is generally poorly conserved even within Drosophila26, and the high turnover of Y-linked genes may obscure any homology between the Y-chromosome of Drosophilids and that of their outgroups.


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

Vicoso B, Bachtrog D - Nature (2013)

Turnover of sex chromosomes in DrosophilaHypothetical transition from an ancestral karyotype with element F segregating as a sex chromosome, to the karyotype observed in Drosophila where element A is the sex chromosome. In outgroup species, maleness is determined by the presence of a factor on the Y chromosome (M-factor). Element A could either have acquired a new, epistatic M*-factor (scenario I), or the existing M-factor could have transposed to element A (scenario II). This transition could also have been initiated by a fusion of the ancestral Y to element A (scenario III). Degeneration of the male-limited, non-recombining element A, followed by recruitment of Sxl for sex determination would create the ancestral karyotype of Drosophila.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4120283&req=5

Figure 4: Turnover of sex chromosomes in DrosophilaHypothetical transition from an ancestral karyotype with element F segregating as a sex chromosome, to the karyotype observed in Drosophila where element A is the sex chromosome. In outgroup species, maleness is determined by the presence of a factor on the Y chromosome (M-factor). Element A could either have acquired a new, epistatic M*-factor (scenario I), or the existing M-factor could have transposed to element A (scenario II). This transition could also have been initiated by a fusion of the ancestral Y to element A (scenario III). Degeneration of the male-limited, non-recombining element A, followed by recruitment of Sxl for sex determination would create the ancestral karyotype of Drosophila.
Mentions: How could this transition have happened? Sex in most outgroup species of Drosophila is determined by the presence of a factor on the Y chromosome (M-factor) causing maleness20. Such a dominant-Y system with element F as the sex chromosome could evolve into the Drosophila system (dose-dependent sex determination with element A as the sex chromosome), through various intermediate steps1, and we outline three possible paths that involve mutational events that have been observed in Diptera. This sex chromosome transition could be initiated by a single epistatic mutation on element A (M*) that makes individuals male regardless of their sex chromosome karyotype, or through a translocation of the existing male-determining factor (M) onto element A (Fig. 4). Novel sex determining genes occurring on different chromosomes or translocations of M-factors onto autosomes have been observed in houseflies21 or humpbacked flies22. The fixation of the new male-determining gene on element A would lead to reversal of the ancestral X (Muller F) to an autosome, and the ancestral Y would be completely lost. Loss of the Y is only possible if the ancestral Y chromosome carried no essential male-fertility genes, as seems to be the case in several Diptera species21, or if those male-fertility genes move to another chromosome23. The emergence of a male-determining gene on element A would cause male-limited transmission of this chromosome and - since higher Diptera males generally lack recombination24 - set in motion genome-wide degeneration of the non-recombining proto-Y. Eventually, Sxl was recruited as a dose-dependent sex determination gene in Drosophila, and MSL-mediated dosage compensation evolved on element A16. The current karyotype of Drosophila could also have evolved through a chromosomal fusion between the ancestral Y chromosome and element A (Fig. 4). This would create a male-limited neo-Y (the fused element A) that initially is identical to the neo-X (the unfused element A). The non-recombining neo-Y would undergo chromosome-wide degeneration, and Y-autosome fusions coupled with neo-Y degeneration have happened repeatedly in several Drosophila species and other Diptera12,25. This fused neo-Y chromosome would form the current Y of Drosophila, and male-fertility genes, if present on the ancestral Y, could be preserved on the chimeric Y. Both element F and element A would simultaneously segregate as X chromosomes, and eventually Sxl would take over the sex determining function on element A, and a non-disjunction event could restore diploidy for element F in both sexes. Thus, under both the translocation of an existing or the emergence of a new M-factor scenario, the current Y chromosome of Drosophila shares no homology to the Y of its ancestor, while under the chromosomal fusion model, the current Drosophila Y is a chimera of the ancestral Y and the degenerated element A and may thus harbor some genes that are also Y-linked in outgroup species. We detect no Y-linked protein-coding genes that are shared between Drosophila and Diptera where Muller F is the sex chromosome (Table S3–S5, Fig S8–S10), providing some support against a fusion between the new and ancestral Y. However, it should be noted that the gene content of the Y is generally poorly conserved even within Drosophila26, and the high turnover of Y-linked genes may obscure any homology between the Y-chromosome of Drosophilids and that of their outgroups.

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