X-chromosomal localization of mammalian Y-linked genes in two XO species of the Ryukyu spiny rat

Abstract

Ryukyu spiny rats (genus Tokudaia), which are endemic to the central part of the Nansei Shoto archipelago in Japan, have unique karyotypes with odd numbers of chromosomes and no cytologically recognizable Y chromosome. The chromosome numbers of Tokudaia osimensis from Amamioshima and of Tokudaia sp. from Tokunoshima are 2n = 25 and 2n = 45, respectively, with a putative single X chromosome. The mouse X probe hybridized to the unpaired X chromosome, except for the distal part of the short arm in a female specimen of T. osimensis and in one male and one female of Tokudaia sp. Fluorescence in situ hybridization with the Tspy (testis-specific protein, Y-encoded) gene from both male and female cells of Tokudaia sp. by PCR localized Tspy to the distal part of the long arm of the X chromosome. Another Y-related gene, Zfy, from Tokudaia sp. was also localized to the same region in both species. Although the Sry gene is absent in this species, the present results suggest that the Y-chromosome segment carrying functional Y-linked genes, such as Tspy and Zfy, is translocated onto the distal part of the long arm of the X chromosome.

Estimating Tempo and Mode of Y Chromosome Turnover: Explaining Y Chromosome Loss With the Fragile Y Hypothesis

“…In D. pseudoobscura the existing Y is homologous with an ancestral autosome, suggesting that the sex chromosomes fused with an autosome and the ancestral Y region was subsequently lost (Carvalho and Clark 2005). Even among taxa with generally persistent XY chromosome systems such as those in mammals, there is precedent for Y dispensability; both mole voles (Just et al 1995) and spiny rats (Arakawa et al 2002) have lost the ancestral Y chromosome.…”

“…Second, within the largest family of mammals, Muridae, we find additional origins of achiasmatic male meiosis and Y chromosome loss. The subfamily Gerbillinae has evolved achiasmatic sex chromosomes and Y losses are not reported, whereas in a related subfamily Murinae, which has not evolved achiasmatic meiosis, the spiny rat genus Tokudaia has three species, two of which have lost the Y chromosome (Arakawa et al 2002), and a third whose Y chromosome is fused with an autosome, rejuvenating the PAR and escaping potential difficulty in segregation during male meiosis (Murata et al 2012). While this is a small sample, it is worth noting that in mammals the Y often carries genes essential for male viability and, all else being equal, is thus likely to be under stronger selection to be retained than in Coleoptera.…”

Comparative chromosome painting map between two Ryukyu spiny rat species, Tokudaia osimensis and Tokudaia tokunoshimensis (Muridae, Rodentia)

“…Chromosome banding is a conventional method to compare the karyotypes between different species, and has been extensively used for studying the karyotypic evolution of vertebrates. Q-banding and G-banding analyses have been 4 performed for T. osimensis and T. tokunoshimensis (Arakawa et al 2002, Kobayashi et al 2007, and the G-banded ideograms of the two species have been established (Kobayashi et al 2007). Chromosome banding is effective for the comparison of morphological similarities of chromosomes between relatively closely related species;…”

Chromosome homology between mouse and three Muridae species, Millardia meltada, Acomys dimidiatus and Micromys minutus, and conserved chromosome segments in murid karyotypes

“…The diploid chromosome number of T. muenninki is 2n=44 with the XX/XY type of sex chromosomes (Tsuchiya et al 1989), whereas the diploid numbers of T. osimensis and T. tokunoshimensis are 2n=25 and 2n=45, respectively, both of which have a unique X0/X0 sex determining system without a Y chromosome or a Sry gene (Honda et al 1977, 1978, Soullier et al 1998, Sutou et al 2001, Arakawa et al 2002, Kobayashi et al 2007. The homology of the T. osimensis and T. tokunoshimensis X chromosomes with the mouse X chromosome has been revealed by comparative chromosome painting with a mouse X probe (Arakawa et al 2002). The remarkable difference of the diploid chromosome number between T. osimensis and T. tokunoshimensis indicates that frequent chromosome rearrangements have occurred between the two species in less than 2 million years since they diverged from the common ancestor.…”

“…Chromosome banding is a conventional method to compare the karyotypes between different species, and has been extensively used for studying the karyotypic evolution of vertebrates. Q-banding and G-banding analyses have been performed for T. osimensis and T. tokunoshimensis (Arakawa et al 2002, Kobayashi et al 2007, and the G-banded ideograms of the two species have been established (Kobayashi et al 2007). Chromosome banding is effective for the comparison of morphological similarities of chromosomes between relatively closely related species;…”