Research

Neo-sex chromosomes in the black muntjac recapitulate incipient evolution of mammalian sex chromosomes

Qi Zhou^1,2* , Jun Wang^3,4,5* , Ling Huang^2,6* , Wenhui Nie⁶ , Jinhuan Wang⁶ , Yan Liu^2,6 , Xiangyi Zhao¹ , Fengtang Yang⁷ and Wen Wang¹

¹  CAS-Max Planck Junior Research Group, State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences (CAS), 32# Jiao-chang Road, Kunming, Yunnan 650223, People's Republic of China

²  Graduate School of Chinese Academy Sciences, 19# Yu-quan Road, Beijing 100039, People's Republic of China

³  The Institute of Human Genetics, University of Aarhus, Nordre Ringgade 1, DK-8000 Aarhus C, Denmark

⁴  Department of Biochemistry and Molecular Biology, University of Southern Denmark, Campusvej 55, DK-5230, Odense M, Denmark

⁵  Beijing Genomics Institute, Bei-shan Road, Shenzhen 518083, People's Republic of China

⁶  Kunming Cell Bank, State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, 32# Jiao-chang Road, Kunming, Yunnan 650223, People's Republic of China

⁷  Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Ickleton Road, Hinxton, Cambridge, CB10 1SA, UK

author email corresponding author email* Contributed equally

Genome Biology 2008, 9:R98doi:10.1186/gb-2008-9-6-r98

Published:	14 June 2008

Subject areas: Evolution, Genetics

Abstract

Background

The regular mammalian X and Y chromosomes diverged from each other at least 166 to 148 million years ago, leaving few traces of their early evolution, including degeneration of the Y chromosome and evolution of dosage compensation.

Results

We studied the intriguing case of black muntjac, in which a recent X-autosome fusion and a subsequent large autosomal inversion within just the past 0.5 million years have led to inheritance patterns identical to the traditional X-Y (neo-sex chromosomes). We compared patterns of genome evolution in 35-kilobase noncoding regions and 23 gene pairs on the homologous neo-sex chromosomes. We found that neo-Y alleles have accumulated more mutations, comprising a wide variety of mutation types, which indicates cessation of recombination and is consistent with an ongoing neo-Y degeneration process. Putative deleterious mutations were observed in coding regions of eight investigated genes as well as cis-regulatory regions of two housekeeping genes. In vivo assays characterized a neo-Y insertion in the promoter of the CLTC gene that causes a significant reduction in allelic expression. A neo-Y-linked deletion in the 3'-untranslated region of gene SNX22 abolished a microRNA target site. Finally, expression analyses revealed complex patterns of expression divergence between neo-Y and neo-X alleles.

Conclusion

The nascent neo-sex chromosome system of black muntjacs is a valuable model in which to study the evolution of sex chromosomes in mammals. Our results illustrate the degeneration scenarios in various genomic regions. Of particular importance, we report - for the first time - that regulatory mutations were probably able to accelerate the degeneration process of Y and contribute to further evolution of dosage compensation.