A Comparative Analysis of the Mole Vole Sibling Species <i>Ellobius tancrei</i> and <i>E. talpinus</i> (Cricetidae, Rodentia) through Chromosome Painting and Examination of Synaptonemal Complex Structures in Hybrids

Abstract

A comparative genomic analysis was carried out in the mole vole sibling species Ellobius tancrei and E. talpinus. Performing fluorescent in situ hybridisation (Zoo-FISH) using chromosome paints from the field vole Microtus agrestis showed no differences in the allocation of syntenic groups in the karyotypes of these sibling species. The only difference between their karyotypes was the position of the centromere in one pair of chromosomes, which is assumed to be the result of an inversion. To verify this hypothesis, we analysed chromosome synapsis in prophase I of meiosis. We utilised a synaptonemal complex (SC) surface-spreading technique to visualise the process of chromosome synapsis in the spermatocytes and oocytes of first-generation hybrids and back-crosses of these sibling species. In prophase I of meiosis, immunocytochemical and electron microscopy analyses revealed that all bivalents had been fully adjusted. Even in the case of a submetacentric-acrocentric bivalent with different centromere locations, synapsis of SC lateral elements was fulfilled along the entire length of the chromosomes and the formation of an inversion loop was not observed. We hypothesise that a possible mechanism leading to the change in centromere position is the repositioning and/or generation of a neocentromere. Despite the great similarity in the karyotypes of these sibling species, they exhibited significant genomic diversification, which manifested as hybrid sterility and parous female death.

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

“…It is important that neither differences for male and female chromosomal sets, nor the signal for the Y chromosome probes were revealed. The same results were obtained for species with two X chromosomes in males and females of Е. talpinus and E. tancrei [38]. These results proved the total loss of a Y chromosome, but chromosome painting has a restriction because a fluorescent signal might be unrecognizable in the case of a small fragment, whereas the screening for specific genes is more precise.…”

“…50% of newborns are males, and 50% are females. The structures of autosomes and sex chromosomes were studied by chromosome painting of 4 species lacking Y chromosomes; the X chromosome is typical for rodents, and no parts of the Y chromosome were revealed [37,38]. To date, only E. fuscocapillus was not studied by molecular cytogenetic methods.…”

Meiotic Chromosome Contacts as a Plausible Prelude for Robertsonian Translocations

“…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]. We hypothesized that a neocentromere origin in one pair of chromosomes was an initial disturbance event for the E. tancrei (2n = 54-30) genome, in contrast to stable E. talpinus (2n = 54) [49,52].…”

“…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]. We hypothesized that a neocentromere origin in one pair of chromosomes was an initial disturbance event for the E. tancrei (2n = 54-30) genome, in contrast to stable E. talpinus (2n = 54) [49,52]. E. alaicus is very close to E. tancrei, a translocation Rb(2.11) emerged in both species; other Rbs are species-specific ones.…”

Sex chromosome repeats tip the balance towards speciation

“…It is unclear what could have destabilized the sex chromosomes in E. lutescens , E. tancrei and E. talpinus . F1 hybrids have been identified between E. talpinus and E. tancrei that are sterile, implicating the emergence of reproductive barriers (Bakloushinskaya et al., ; Table ). Fluorescence in situ hybridization revealed that some mammalian Y‐derived genes known to be essential for male fertility have moved to the X chromosome in these two species (Mulugeta et al., ).…”