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Open Access Research article

De novo transcriptome assembly reveals sex-specific selection acting on evolving neo-sex chromosomes in Drosophila miranda

Vera B Kaiser12 and Doris Bachtrog1*

Author Affiliations

1 Department of Integrative Biology, Center for Theoretical Evolutionary Genomics, University of California, Berkeley, Berkeley, CA 94720, USA

2 Current Address: MRC Human Genetics Unit, MRC Institute of Genetics and Molecular Medicine, University of Edinburgh, Western General Hospital, Edinburgh EH4 2XU, UK

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BMC Genomics 2014, 15:241  doi:10.1186/1471-2164-15-241

Published: 27 March 2014

Abstract

Background

The Drosophila miranda neo-sex chromosome system is a useful resource for studying recently evolved sex chromosomes. However, the neo-Y genomic assembly is fragmented due to the accumulation of repetitive sequence. Furthermore, the separate assembly of the neo-X and neo-Y chromosomes into genomic scaffolds has proven to be difficult, due to their low level of sequence divergence, which in coding regions is about 1.5%. Here, we de novo assemble the transcriptome of D. miranda using RNA-seq data from several male and female tissues, and develop a bioinformatic pipeline to separately reconstruct neo-X and neo-Y transcripts.

Results

We obtain 2,141 transcripts from the neo-X and 1,863 from the neo-Y. Neo-Y transcripts are generally shorter than their homologous neo-X transcripts (N50 of 2,048-bp vs. 2,775-bp) and expressed at lower levels. We find that 24% of expressed neo-Y transcripts harbor nonsense mutation within their open reading frames, yet most non-functional neo-Y genes are expressed throughout all of their length. We find evidence of gene loss of male-specific genes on the neo-X chromosome, and transcriptional silencing of testis-specific genes from the neo-X.

Conclusions

Nonsense mediated decay (NMD) has been implicated to degrade transcripts containing pre-mature termination codons (PTC) in Drosophila, but rampant description of neo-Y genes with pre-mature stop codons suggests that it does not play a major role in down-regulating transcripts from the neo-Y. Loss or transcriptional down-regulation of genes from the neo-X with male-biased function provides evidence for beginning demasculinization of the neo-X. Thus, evolving sex chromosomes can rapidly shift their gene content or patterns of gene expression in response to their sex-biased transmission, supporting the idea that sex-specific or sexually antagonistic selection plays a major role in the evolution of heteromorphic sex chromosomes.

Keywords:
Sex chromosomes; Drosophila; Transcriptome; Gene loss; Nonsense mediated decay