Origins and functional evolution of Y chromosomes across mammals

Abstract

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.

Did sex chromosome turnover promote divergence of the major mammal groups?

“…Sequence comparisons between X‐Y shared genes revealed that the large X 5 and tiny Y 5 that terminate the chain are the most diverged, and therefore the oldest members of the chain 54, suggesting that they represent the original mammalian sex chromosomes. X 5 is largely homologous to the bird Z 52.…”

“…There is no trace of a Y‐borne DMRT1 variant that could act as a male‐determining gene. The most convincing candidate is an AMH orthologue that lies with syntenic markers on the tiny Y 5 chromosome 54. This suggests that translocation of the ancestral sex pair with an autosome provided a novel sex gene in an ancestral monotreme.…”

The genetic contribution to sex determination and number of sex chromosomes vary among populations of common frogs (Rana temporaria)

“…The former is thought to determine sex in birds (Smith et al, 2009), whereas paralogs play this role in species of fish and frogs (Matsuda et al, 2002;Nanda et al, 2002;Yoshimoto et al, 2010). The antiMullerian hormone Amh likely determines sex in platypus (Cortez et al, 2014), whereas a paralog has been shown to play this role in a fish (Hattori et al, 2012).…”

Radical remodeling of the Y chromosome in a recent radiation of malaria mosquitoes

“…In animals with morphologically distinct (heterogametic) sex chromosomes, the Y has ceased crossing over with the X across some or all of its length and the nonrecombining region is transmitted clonally by males (4,5). The absence of recombination initiates progressive genetic decaygene loss and accumulation of repetitive sequences-but there is increasing recognition that even relatively old and otherwise highly degenerate Y chromosomes retain functional importance not only for sexual reproduction but for their contributions to global gene regulation, affecting health and survival (6)(7)(8)(9)(10). Notwithstanding these critical roles, the Y chromosome remains one of the most recalcitrant and poorly characterized portions of any genome more than a decade into the postgenomic era, with current knowledge resting largely on only two animal groups: mammals and Drosophila (2,11).…”