Evolutionary history of novel genes on the tammar wallaby Y chromosome: Implications for sex chromosome evolution

Abstract

We report here the isolation and sequencing of ten Y-specific tammar wallaby (Macropus eugenii) BAC clones, revealing five hitherto undescribed tammar wallaby Y genes (in addition to the five genes already described) and several pseudogenes. Some genes on the wallaby Y display testis-specific expression, but most have low widespread expression. All have partners on the tammar X, along with homologues on the human X. Non-synonymous and synonymous substitution ratios for nine of the tammar XY gene pairs indicate that they are each under purifying selection. All ten were also identified as being on the Y in Tasmanian devil (Sarcophilus harrisii; a distantly related Australian marsupial); however, seven have been lost from the human Y. Maximum likelihood phylogenetic analyses of the wallaby YX genes, with respective homologues from other vertebrate representatives, revealed that three marsupial Y genes (HCFC1X/Y, MECP2X/Y and HUWE1X/Y) were members of the ancestral therian pseudoautosomal region (PAR) at the time of the marsupial/ eutherian split, three XY pairs (SOX3/SRY, RBMX/Y and ATRX/Y) were isolated from each other before the marsupial/ eutherian split, and the remaining three (RPL10X/Y, PHF6X/Y and UBA1/UBE1Y) have a more complex evolutionary history. Thus, the small marsupial Y chromosome is surprisingly rich in ancient genes that are retained in at least Australian marsupials, and evolved from testis-brain expressed genes on the X.