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 10 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 homologs on the human X. Nonsynonymous and synonymous substitution ratios for nine of the tammar XY gene pairs indicate that they are each under purifying selection. All 10 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 homologs 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.

Chromosome-wide profiling of X-chromosome inactivation and epigenetic states in fetal brain and placenta of the opossum, Monodelphis domestica

“…No extensive sequence data from the opossum Y chromosome have been published, but Atrx and Rsp4 each have X-and Y-linked homologs in M. domestica (Jegalian and Page 1998;Carvalho-Silva et al 2004), and 10 Y-linked homologs of X-linked genes have been detected in the tammar wallaby, Macropus eugenii (Murtagh et al 2012). In our study, six of these marsupial X/Y homologous gene pairs (Atrx, Phf6, Hcfc1 Rbmx, Mecp2, and Rpl10) were found to have informative SNPs, and all six escaped pXCI in both fetal brain and EEM.…”

The pig X and Y Chromosomes: structure, sequence, and evolution

“…These few assemblies, and several partial sequence assemblies, have permitted the elucidation of chromosome topology and gene order in human , chimpanzee (Hughes et al 2010), rhesus macaque (Hughes et al 2012), wallaby (Murtagh et al 2012), mouse (Soh et al 2014), marmoset, rat, and opossum (Bellott et al 2014), cattle (Elsik et al 2009), horse (Paria et al 2011), and cat and dog (Li et al 2013a). These works show divergence in gene content, order, structure, and sequence between Y Chromosomes from different mammalian species.…”

Efficient identification of Y chromosome sequences in the human and Drosophila genomes

“…Analysis of their origin and evolution has revealed unexpected biological phenomena (Rozen et al 2003;Carvalho and Clark 2005;Koerich et al 2008;Lemos et al 2008;Murtagh et al 2012), as well as general principles of evolutionary genetics, including the role of recombination and sex-antagonistic genes (Rice 1996;Charlesworth and Charlesworth 2000;Zhou and Bachtrog 2012). However, despite their importance, little is known about Y chromosomes because in many species they are heterochromatic, being composed of highly repetitive DNA that cannot be fully assembled with current technologies (Carvalho et al 2003;Hoskins et al 2007).…”