Unusual Ways to Lose a Y Chromosome and Survive with Changed Autosomes: a Story of Mole Voles Ellobius (Mammalia, Rodentia)

Abstract

Species of mole volesEllobius demonstrate a broad variation in sex chromosomes and autosomes, which is unique among mammals. In four species, a Y chromosome was lost, and X0 or XX sex chromosomes in both sexes were obtained. The key testis-determining Sry (Sexdetermining Region on Y) gene is absent in these species, and the regulation of its target, the Sox9 (SRY -box 9) gene, is questionable due to deletion in the key enhancer. In a single species, E. fuscocapillus, with routine XX-XY, the same deletion is present alongside fragments of Sry in the female genome. Presumably, a Y chromosome was lost twice in two phylogenetic lineages of mole rats; before the event, a few male-specific genes escaped on X chromosomes. Translocations of Y chromosome fragments were made independently, resulting in different changes in species without a Y chromosome and the presence of the Ylinked Sry gene in females of E. fuscocapillus, a species retaining the Y chromosome. One more exceptional phenomenon is high autosomal variability in E. tancrei. This species might be used as an exclusive model for studying meiotic mechanisms providing balanced gametes in complex heterozygous hybrids. Sterility is the only destiny for hybrids, whose parents carry Robertsonian translocations with partial homology. Contrary to that, E. tancrei possess different Robertsonian translocations and successfully overcome the hybrid incompatibility. Here, we overview the research to date of sex determination and meiosis in Ellobius.

Meiotic Chromosome Contacts as a Plausible Prelude for Robertsonian Translocations

“…Several mammalian species have demonstrated natural variability's in chromosomal numbers, including Rbs. Mus, Sorex, Ellobius species, and some others exhibit changes in diploid numbers, along with stable fundamental numbers due to whole branch fusions [45][46][47][48]. Recently, using chromosome painting, we described karyotype structures in three cryptic Ellobius species, E. talpinus, E. tancrei, and E. alaicus; we demonstrated a homology of re-arranged chromosomes, and showed the existence of XX sex chromosomes in males and females [49][50][51].…”

Meiosis reveals the early steps in the evolution of a neo-XY sex chromosome pair in the African pygmy mouse Mus minutoides

“…For instance, although most eutherians still conserve a small segment of the PAR, in several groups such as gerbils [ 11 , 12 ], voles [ 13 – 15 ] and pygmy mice [ 16 ], the X and Y chromosomes are completely differentiated (and have no PAR). A few species have even completely lost the Y chromosome, including voles of the genus Ellobius [ 17 ] and the Ryukyu spiny rat Tokudaia osimensis [ 18 ]. In contrast, in some bats [ 19 ], bovids [ 20 ], primates [ 21 ] and rodents [ 16 , 22 ], new autosomal translocations have, once again, restored a large section of the PAR, which can initiate a new differentiation process.…”

Rapid chromosomal evolution in enigmatic mammal with XX in both sexes, the Alay mole vole Ellobius alaicus Vorontsov et al., 1969 (Mammalia, Rodentia)

“…E.talpinus , E.tancrei , and E.alaicus are unique in mammals. Along with autosomal changes, the species lost the Y chromosome, the Sry gene, and obtained isomorphic XX chromosomes in both males and females (Lyapunova and Vorontsov 1978, Vorontsov et al 1980, Kolomiets et al 1991, Just et al 1995, Romanenko et al 2007, Bakloushinskaya et al 2012, Bakloushinskaya and Matveevsky 2018). The study of E.lutescens and E.talpinus whole genomes was not able to reveal any sex determining factors (Mulugeta et al 2016).…”