Ancestral Y-linked genes were maintained by translocation to the X and Y chromosomes fused to an autosomal pair in the Okinawa spiny rat Tokudaia muenninki

Abstract

Two species of the genus Tokudaia lack the Y chromosome and SRY, but several Y-linked genes have been rescued by translocation or transposition to other chromosomes. Tokudaia muenninki is the only species in the genus that maintains the Y owing to sex chromosome-autosome fusions. According to previous studies, many SRY pseudocopies and other Y-linked genes have evolved by excess duplication in this species. Using RNA-seq and RT-PCR, we found that ZFY, EIF2S3Y, TSPY, UTY, DDX3Y, USP9Y, and RBMY, but not UBA1Y, had high deduced amino acid sequence similarity and similar expression patterns with other rodents, suggesting that these genes were functional. Based on FISH and quantitative real-time PCR, all of the genes except for UTY and DDX3Y were amplified on the X and Y chromosomes with approximately 10-66 copies in the male genome. In a comparative analysis of the 372.4-kb BAC sequence and Y-linked gene transcripts from T. muenninki with the mouse Y genomic sequence, we observed that multiple-copy genes in the ancestral Y genome were nonfunctional, indicating that the gene functions were assumed by amplified copies. We also found a LTR sequence at the distal end of a SRY duplication unit, suggesting that unequal sister chromatid exchange mediated by retrotransposable elements could have been involved in SRY amplification. Our results revealed that the Y-linked genes were rescued from degeneration via translocations to other sex chromosomal regions and amplification events in T. muenninki

Chromosomal Evolution in Mole Voles Ellobius (Cricetidae, Rodentia): Bizarre Sex Chromosomes, Variable Autosomes and Meiosis

“…The short exonic fragment (162 bp) of Eif2s3x , which was sequenced in E. fuscocapillus , carried a single transversion (A–T). The BLAST analyses ( ) for presumably an exonic part of Eif2s3y , revealed up to 88% identity for the studied fragment of Eif2s3y of Muennik’s spiny rat Tokudaia muenninki [ 42 ]. The other sequenced part was highly variable in all studied Ellobius species, but was identical in males and females.…”

Patterns of Sex Chromosome Differentiation in Spiders: Insights from Comparative Genomic Hybridisation

“…Cases of enlargement of sex-limited sex chromosomes due to repetitive DNA accumulation are known in several organisms [8,45,[81][82][83][84][85][86][87][88]. As described in diverse animal taxa, these sequences could even expand from the Y chromosome via ectopic recombination and/or transposition [6,[70][71][72]. In Pholcus, such a scenario might be indicated by the slightly more intense accumulation of male probe at the end of X 2 chromosome; this region is involved in pairing of X 2 and Y chromosomes.…”

“…It may be speculated that this region could have been translocated to the X 1 chromosome from the CSCP by means of ectopic recombination or transposition. These mechanisms are known to give rise to similar transfers between sex chromosomes and autosomes in various animal groups [6,[70][71][72]. Alternatively, since CGH provided different patterns of hybridisation signals between male and female probe even on autosomes, this male-specific signal on the X 1 chromosome might reflect the intraspecific variability in expansion of repeats which might not mirror sex-linked differences.…”

Reorganization of the Y Chromosomes Enhances Divergence in Israeli Mole Rats Nannospalax ehrenbergi (Spalacidae, Rodentia): Comparative Analysis of Meiotic and Mitotic Chromosomes

“…Several possible ways of slowing down the decay of the Y chromosome were hypothesized, for example by gene duplications, adding repeats, doubling and translocating parts of X, or fusing with autosomes or their parts [ 23 , 24 , 25 , 26 ]. If an autosome or some part of it is translocated onto Y, so called ‘neo’ sex chromosomes form, as in spiny mice Tokudaia muenninki [ 27 ], Indian mongoose Herpestes auropunctatus [ 28 , 29 ], and South-American primates Aotus [ 30 , 31 ] and Alouatta [ 32 , 33 ]. A comparison of Y in different primate species made it possible to conclude that there are pericentric inversions in the early stages of the primates’ evolution [ 34 ].…”