Sex chromosomes of basal placental mammals

Abstract

Placental (eutherian) mammals are currently classified into four superordinal clades (Afrotheria, Xenarthra, Laurasiatheria and Supraprimates) of which one, the Afrotheria (a unique lineage of African origin), is generally considered to be basal. Therefore, Afrotheria provide a pivotal evolutionary link for studying fundamental differences between the sex chromosomes of human/mouse (both representatives of Supraprimates and the index species for studies of sex chromosomes) and those of the distantly related marsupials. In this study, we use female fibroblasts to investigate classical features of X chromosome inactivation including replication timing of the X chromosomes and Barr body formation. We also examine LINE-1 accumulation on the X chromosomes of representative afrotherians and look for evidence of a pseudoautosomal region (PAR). Our results demonstrate that asynchronous replication of the X chromosomes is common to Afrotheria, as with other mammals, and Barr body formation is observed across all Placentalia, suggesting that mechanisms controlling this evolved before their radiation. Finally, we provide evidence of a PAR (which marsupials lack) and demonstrate that LINE1 is accumulated on the afrotherian and xenarthran X, although this is probably not due to transposition events in a common ancestor, but rather ongoing selection to retain recently inserted LINE1 on the X.

The Eutherian Pseudoautosomal Region

“…The PAR is also reported in some of the species of Afrotheria and Xenarthra -the 2 basal eutherian orders [Meredith et al, 2011]. This is evidenced by immunocytological analysis of meiotic prophase chromosomes in the spermatocytes of Cape rock elephant shrew [Waters et al, 2007a] and 3 armadillo species [Sciurano et al, 2012] and by mapping the XG locus to both sex chromosomes in elephants [Delgado et al, 2009]. Finally, based on the size of XY synaptonemal complex in armadillos and the fact that almost the entire Y chromosome synapses with the X, it is thought that Xenarthrans may have the largest known PAR (8.4-13.6 Mb) among eutherians [Sciurano et al, 2012].…”

Physical mapping of the elephant X chromosome: conservation of gene order over 105 million years

“…However, gene order is not conserved within these autosomal blocks of homology when compared between human, cat, and dog, whereas gene order is conserved on the X (Murphy et al 2007a). Mapping the elephant X chromosome enabled us to test the hypotheses that: (1) the addition to the X and Y chromosomes occurred before eutherian radiation; and (2) gene order is conserved on the afrotherian X, which shares features of eutherian XCI (Waters et al 2007b), including the XIST gene (Duret et al 2006), and is therefore expected to undergo chromosomewide X inactivation.…”

“…PARs from boreoeutherians (human, mouse, cow, and horse, the only species studied in any depth) have been shown to differ in size and gene content. The PAR of afrotherian mammals has been identified using cytological evidence in Cape rock elephant shrew (Waters et al 2007b), but its gene content is completely unknown. We therefore included the XG gene, which straddles the PAR boundary (PAB) in humans (Weller et al 1995), and is pseudoautosomal in both horse and dog, and likely in cattle too Chowdhary 2008, Young et al 2008;Van Laere et al 2008).…”

“…Also, in female cells of afrotherian mammals, the X chromosome displays features of human and mouse X chromosome inactivation (asynchronous replication of the two X chromosomes in female cells, Barr body formation, and L1 accumulation; Waters et al 2007b).…”

Dissection of a Y-autosome translocation in Cryptomys hottentotus (Rodentia, Bathyergidae) and implications for the evolution of a meiotic sex chromosome chain

“…We followed Waters et al (2007) for this aspect of our investigation. In brief, testis samples were dissected for immediate analysis or frozen in liquid nitrogen for later experimentation.…”