Reversal of an ancient sex chromosome to an autosome in Drosophila

Vicoso, Beatriz; Bachtrog, Doris

doi:10.1038/nature12235

Cited by 218 publications

(237 citation statements)

References 35 publications

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“…Basilisks are deeply nested among iguana families with ancestral sex chromosomes [17,19,20]. Therefore, the situation in basilisks may reflect a rare event of dedifferentiation or the turnover of already differentiated sex chromosomes [21]; however, further research is needed to evaluate this possibility.…”

Section: Discussionmentioning

confidence: 99%

Cretaceous park of sex determination: sex chromosomes are conserved across iguanas

et al. 2014

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Many poikilothermic vertebrate lineages, especially among amphibians and fishes, possess a rapid turnover of sex chromosomes, while in endotherms there is a notable stability of sex chromosomes. Reptiles in general exhibit variability in sex-determining systems; as typical poikilotherms, they might be expected to have a rapid turnover of sex chromosomes. However, molecular data which would enable the testing of the stability of sex chromosomes are lacking in most lineages. Here, we provide molecular evidence that sex chromosomes are highly conserved across iguanas, one of the most speciesrich clade of reptiles. We demonstrate that members of the New World families Iguanidae, Tropiduridae, Leiocephalidae, Phrynosomatidae, Dactyloidae and Crotaphytidae, as well as of the family Opluridae which is restricted to Madagascar, all share homologous sex chromosomes. As our sampling represents the majority of the phylogenetic diversity of iguanas, the origin of iguana sex chromosomes can be traced back in history to the basal splitting of this group which occurred during the Cretaceous period. Iguanas thus show a stability of sex chromosomes comparable to mammals and birds and represent the group with the oldest sex chromosomes currently known among amniotic poikilothermic vertebrates.

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Section: Discussionmentioning

confidence: 99%

Cretaceous park of sex determination: sex chromosomes are conserved across iguanas

et al. 2014

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“…However, taking into account the recent evidence for evolutionary turnovers or losses of differentiated sex chromosomes in non-vertebrates [14,15] and reptiles [16,17], as well the fact that cytogenetically similar sex chromosomes may not be homologous [14,15], we cannot exclude a turnover of sex chromosomes even in this highly species-rich lineage. Moreover, it is not known whether snake lineages outside this clade also share homologous sex chromosomes.…”

Section: Introductionmentioning

confidence: 99%

Evolutionary stability of sex chromosomes in snakes

et al. 2015

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Amniote vertebrates possess various mechanisms of sex determination, but their variability is not equally distributed. The large evolutionary stability of sex chromosomes in viviparous mammals and birds was believed to be connected with their endothermy. However, some ectotherm lineages seem to be comparably conserved in sex determination, but previously there was a lack of molecular evidence to confirm this. Here, we document a stability of sex chromosomes in advanced snakes based on the testing of Z-specificity of genes using quantitative PCR (qPCR) across 37 snake species (our qPCR technique is suitable for molecular sexing in potentially all advanced snakes). We discovered that at least part of sex chromosomes is homologous across all families of caenophidian snakes (Acrochordidae, Xenodermatidae, Pareatidae, Viperidae, Homalopsidae, Colubridae, Elapidae and Lamprophiidae). The emergence of differentiated sex chromosomes can be dated back to about 60 Ma and preceded the extensive diversification of advanced snakes, the group with more than 3000 species. The Z-specific genes of caenophidian snakes are (pseudo)autosomal in the members of the snake families Pythonidae, Xenopeltidae, Boidae, Erycidae and Sanziniidae, as well as in outgroups with differentiated sex chromosomes such as monitor lizards, iguanas and chameleons. Along with iguanas, advanced snakes are therefore another example of ectothermic amniotes with a long-term stability of sex chromosomes comparable with endotherms.

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“…The increase of male SNP density on the neo-sex chromosome indicates sequence divergence between the neo-X and neo-Y alleles. dosage compensation mediated by POF [31], which may have been derived from a dosage compensation system in an ancestor of Drosophilidae where the dot was the X chromosome [19]. Here, we collect DNA sequence, transcriptome and chromatin data characteristic of dosage compensation and heterochromatin together with immunostaining of polytene chromosomes, to characterize the formation of a sex chromosome from a heterochromatic ancestor, and also to disentangle the relationship between POF and MSL.…”

Section: Introductionmentioning

confidence: 99%

“…The age, and the extent of sequence, expression and epigenetic divergence of the neosex chromosomes of D. busckii are unknown, but the dot chromosome has an unusual evolutionary history and a unique chromatin structure. It was a sex chromosome in an ancestor of higher Diptera, and only reverted to an autosomal inheritance in the ancestor of the Drosophilidae family [19,20]. Studies on the assembled distal arm (~1.2Mb) of the D. melanogaster dot chromosome have revealed several features that distinguish it from other autosomes: it has a very low recombination rate and a high repeat content [21][22][23], harbors less than 100 genes [24] that have low codon usage bias [25] and which show evidence of reduced levels of positive and purifying selection [26].…”

Section: Introductionmentioning

confidence: 99%

Ancestral chromatin configuration constrains chromatin evolution on differentiating sex chromosomes inDrosophila

Zhou

Bachtrog

2015

Preprint

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Sex chromosomes evolve distinctive types of chromatin from a pair of ancestral autosomes that are usually euchromatic. In Drosophila, the dosage-compensated X becomes enriched for hyperactive chromatin in males (mediated by H4K16ac), while the Y chromosome acquires silencing heterochromatin (enriched for H3K9me2/3). Drosophila autosomes are typically mostly euchromatic but the small dot chromosome has evolved a heterochromatinlike milieu (enriched for H3K9me2/3) that permits the normal expression of dot-linked genes, but which is different from typical pericentric heterochromatin. In Drosophila busckii, the dot chromosomes have fused to the ancestral sex chromosomes, creating a pair of 'neo-sex' chromosomes. Here we collect genomic, transcriptomic and epigenomic data from D. busckii, to investigate the evolutionary trajectory of sex chromosomes from a largely heterochromatic ancestor. We show that the neo-sex chromosomes formed <1 million years ago, but nearly 60% of neo-Y linked genes have already become non-functional. Expression levels are generally lower for the neo-Y alleles relative to their neo-X homologs, and the silencing heterochromatin mark H3K9me2, but not H3K9me3, is significantly enriched on silenced neo-Y genes. Despite rampant neo-Y degeneration, we find that the neo-X is deficient for the canonical histone modification mark of dosage compensation (H4K16ac), relative to autosomes or the compensated ancestral X chromosome, possibly reflecting constraints imposed on evolving hyperactive chromatin in an originally heterochromatic environment. Yet, neo-X genes are transcriptionally more active in males, relative to females, suggesting the evolution of incipient dosage compensation on the neo-X. Our data show that Y degeneration proceeds quickly after sex chromosomes become established through genomic and epigenetic changes, and are consistent with the idea that the evolution of sex-linked chromatin is influenced by its ancestral configuration. Data Availability Statement: All sequencing reads, the genome sequence assembly and annotation generated in this study are deposited at the National Center for Biotechnology Information Short Reads Archive (www.ncbi.nlm.nih.gov/sra) under the Bioproject accession no. PRJNA274996.Funding: This work was funded by NIH grants (R01GM076007, R01GM093182 and R01GM101255) to DB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author SummaryDNA is packaged with proteins into two general types of chromatin: the transcriptionally active euchromatin and repressive heterochromatin. Sex chromosomes typically evolve from a pair of euchromatic autosomes. The Y chromosome of Drosophila is gene poor and almost entirely heterochromatic; the X chromosome, in contrast, has evolved a hyperactive euchromatin structure and globally up-regulates its gene expression, to compensate for loss of activity from the homologous genes on the Y chromosome. The evolutionary trajectory along which sex chromosomes...

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Reversal of an ancient sex chromosome to an autosome in Drosophila

Cited by 218 publications

References 35 publications

Cretaceous park of sex determination: sex chromosomes are conserved across iguanas

Cretaceous park of sex determination: sex chromosomes are conserved across iguanas

Evolutionary stability of sex chromosomes in snakes

Ancestral chromatin configuration constrains chromatin evolution on differentiating sex chromosomes inDrosophila

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