Origins and functional evolution of Y chromosomes across mammals.
Y chromosomes underlie sex determination in mammals, but their repeat-rich nature has hampered sequencing and associated evolutionary studies. Here we trace Y evolution across 15 representative mammals on the basis of high-throughput genome and transcriptome sequencing. We uncover three independent sex chromosome originations in mammals and birds (the outgroup). The original placental and marsupial (therian) Y, containing the sex-determining gene SRY, emerged in the therian ancestor approximately 180 million years ago, in parallel with the first of five monotreme Y chromosomes, carrying the probable sex-determining gene AMH. The avian W chromosome arose approximately 140 million years ago in the bird ancestor. The small Y/W gene repertoires, enriched in regulatory functions, were rapidly defined following stratification (recombination arrest) and erosion events and have remained considerably stable. Despite expression decreases in therians, Y/W genes show notable conservation of proto-sex chromosome expression patterns, although various Y genes evolved testis-specificities through differential regulatory decay. Thus, although some genes evolved novel functions through spatial/temporal expression shifts, most Y genes probably endured, at least initially, because of dosage constraints.
1] Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland [2] Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland.
Diego
D
Cortez
1] Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland [2] Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland.
Ray
R
Marin
The Robinson Research Institute, School of Molecular and Biomedical Science, University of Adelaide, Adelaide, South Australia 5005, Australia.
Deborah
D
Toledo-Flores
Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland.
Laure
L
Froidevaux
Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland.
Angélica
A
Liechti
School of Biotechnology and Biomolecular Sciences, UNSW Australia, Sydney, New South Wales 2052, Australia.
Paul D
PD
Waters
The Robinson Research Institute, School of Molecular and Biomedical Science, University of Adelaide, Adelaide, South Australia 5005, Australia.
Frank
F
Grützner
1] Center for Integrative Genomics, University of Lausanne, 1015 Lausanne, Switzerland [2] Swiss Institute of Bioinformatics, 1015 Lausanne, Switzerland.
Henrik
H
Kaessmann
D000818:Animals; D001717:Birds / Q000235:genetics; D017124:Conserved Sequence / Q000235:genetics; D019143:Evolution, Molecular; D005260:Female; D018628:Gene Dosage / Q000235:genetics; D024282:Genes, sry / Q000235:genetics; D023281:Genomics; D059014:High-Throughput Nucleotide Sequencing; D008297:Male; D008322:Mammals / Q000235:genetics*; D008394:Marsupialia / Q000235:genetics; D018000:Receptors, Peptide / Q000235:genetics; D018125:Receptors, Transforming Growth Factor beta / Q000235:genetics; D012641:Selection, Genetic / Q000235:genetics; D012730:Sex Chromosomes / Q000235:genetics; D062211:Spatio-Temporal Analysis; D013091:Spermatogenesis / Q000235:genetics; D013737:Testis / Q000378:metabolism; D059467:Transcriptome / Q000235:genetics; D014998:Y Chromosome / Q000235:genetics*
D018000:Receptors, Peptide; D018125:Receptors, Transforming Growth Factor beta; C084621:anti-Mullerian hormone receptor