Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2017 Nov 3;8(11):306.
doi: 10.3390/genes8110306.

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

Affiliations
Free PMC article

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

Sergey Matveevsky et al. Genes (Basel). .
Free PMC article

Abstract

This study reports on extensive experimental material covering more than 30 years of studying the genetics of mole voles. Sex chromosomes of Ellobius demonstrate an extraordinary case of mammalian sex chromosomes evolution. Five species of mole voles own three types of sex chromosomes; typical for placentals: XY♂/XX♀; and atypical X0♂/X0♀; or XX♂/XX♀. Mechanisms of sex determination in all Ellobius species remain enigmatic. It was supposed that the Y chromosome was lost twice and independently in subgenera Bramus and Ellobius. Previous to the Y being lost, the X chromosome in distinct species obtained some parts of the Y chromosome, with or without Sry, and accumulated one or several copies of the Eif2s3y gene. Along with enormous variations of sex chromosomes, genes of sex determination pathway and autosomes, and five mole vole species demonstrate ability to establish different meiotic mechanisms, which stabilize their genetic systems and make it possible to overcome the evolutionary deadlocks.

Keywords: Eif2s3y; Ellobius; Sry; karyotype evolution; meiosis; sex determination; tetraploid spermatocytes.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Variations of a centromere position in the submetacentric chromosome in the early meiotic prophase I of mole voles. Axial elements were identified using anti-SYCP3 antibodies (green), central element usinganti-SYCP1 (magenta), recombination nodules usinganti-MLH1 (yellow), and anti-CREST for kinetochores (red). The asterisk shows the location of the centromeric signal of the submetacentric homolog (33–35% of the telomere end). The red signal without asterisk marked erratic centromere positions in the submetacentric. (A) spermatocytes from interspecific hybrids F1 of Ellobius talpinus (2n = 54) × Ellobius tancrei (2n = 34). Bar = 5 µm. A submetacentric is in the circle (inset (BC)); (D) heteromorphic bivalent in females and males of the interspecific hybrid of mole voles. One centromeric signal originated from the acrocentric homologue of E. talpinus, the other from the submetacentric homologue of E. tancrei. A submetacentric chromosome from karyotypes of E. tancrei 2n = 54, male (E); E. tancrei 2n = 34, female (F); E. tancrei, intraspecific hybrid 2n = 50, male (G) and female (H); E. tancrei, intraspecific hybrid, 2n = 49, male (I) and female (J). Bar (EJ) = 2 µm.
Figure 2
Figure 2
Ellobius male sex chromosomes behaviour in meiotic prophase I. Electron microscopy (EM), AgNO3-staining (B–D, G–I, L–N). (АD) Ellobius fuscocapillus. (A) sex chromosomes (schematic visualization): ХХ♀/XY♂; (B) during the zygotene stage, X and Y synapsed in a short region; (C) during the pachytene stage, Y fully synapsed with X. The asynaptic part of the X became thicker; (D) during the diplotene stage, X and Y had no synaptic area (desynapsis), chromosomes became thick, irregular and surrounded by an electron-dense cloud; (EH) Ellobius lutescens. (E) sex chromosomes (schematic visualization): Х0♀/X0♂; (F) sex Х-univalent was visible as thin axe, one–two round electron-dense bodies often revealed close to it (green arrow); (G) during the pachytene stage, an Х-univalent became thicker with multi axes and flexures (‘hairpins’) formed. A large hairpin looked like an SC structure (blue arrowheads). A round body was located nearby (green arrow); (H) during the diplotene stage, the X-univalent became thicker; (IL) E. talpinus/E. tancrei/Ellobius alaicus. Meiosis in E. alaicus was still unknown (asterisk). (I) sex chromosomes (schematic visualization): ХХ♀/XX♂; (J) during the zygotene stage a sex (ХХ) bivalent demonstrated non-standard morphology: two telomeric regions of synapsis and large central asynaptic zone; (K) the morphology of ХХ bivalent occurred at the pachytene stage, too. An electron-dense chromatin body (ChB) was visualized clearly (red arrow). A less intense electron-dense cloud (purple arrowheads) spread along the X axis from the round body (ChB) toward the synaptic sites. Thus, the X axes differ from each other, so Xs are marked with different tones of red; Synaptic sites: Ss1, Ss2 (L) during the diplotene stage a sex bivalent rolled up into a tangle and was surrounded by an electron-dense substance. Bar = 5 µm.
Figure 3
Figure 3
Immunostaining of pachytene spermatocytes from E. lutescens (A) and E. tancrei (B). Axial SC elements were identified using anti-SYCP3 antibodies (green), anti-CREST for kinetochores (red) and anti-γH2AFX as marker of chromatin inactivation (magenta). (A) the X-univalent is replaced to the periphery of the meiotic nucleus, formed sex body and shrouded by γH2AFX. A γH2AFX-negative round body is noticeable in the X sex body (green arrow); (B) during the middle pachytene, XX bivalent was replaced to the periphery of the meiotic nucleus, formed sex body and surrounded by γH2AFX. A chromatin body (ChB) was often γH2AFX-negative (green arrow). Bar = 5 µm.
Figure 4
Figure 4
Tetraploid early pachytene spermatocyte from E. talpinus with stable karyotype (2n = 54, NF = 54). Axial SC elements were identified using anti-SYCP3 antibodies (green), anti-CREST for kinetochores (red), DNA double-strand break (DSB) loci immunostained with antibodies against the RAD51 protein (yellow). Chromatin was stained with DAPI (gray). Pseudo-bivalents (tetravalents) at the different stages of synapsis were in the nuclei (A). Four homologous adjusted sequentially, forming double bivalent/pseudo-bivalent (tetravalent) and then individual bivalents (B). RAD51-signals are absent in some fully synaptic bivalents (C). The denser chromatin occupied the central part of the nucleus, where it is assumed a sex tetravalent was located (a black circle, (D)). Bar = 5 µm.
Figure 5
Figure 5
Hypothetical events of chromosome evolution in Ellobius. The scheme explains the evolutionary transformation of the ancestral acrocentric into a submetacentric that was inherited by all chromosomal forms of the E. tancrei. The synaptic structure at the right is based on the SC structure of the interspecific F1 hybrids of E. talpinus (2n = 54, NF = 54) and E. tancrei (2n = 54, NF = 56 or 2n = 34, NF = 56; etc.). The red dots indicate centromeres.
Figure 6
Figure 6
Evolutionary patterns of sex chromosome composition. G-Band: Giemsa band; MSC: meiotic sex chromosome inactivation.

Similar articles

See all similar articles

Cited by 4 articles

References

    1. Matthey R. La formule chromosomique et le problème de la détermination sexuelle chez Ellobius lutescens (Rodentia-Muridae-Microtinae) Arch. Julius Klaus-Stift Vererb. Forsch. 1953;28:65–73.
    1. Castro-Sierra E., Wolf U. Replication patterns of the unpaired chromosome No. 9 of the rodent Ellobius lutescens Th. Cytogenet. Genome Res. 1967;6:268–275. doi: 10.1159/000129947. - DOI - PubMed
    1. Castro-Sierra E., Wolf U. Studies on the male meiosis of Ellobius lutescens Th. Cytogenet. Genome Res. 1968;7:241–248. doi: 10.1159/000129988. - DOI - PubMed
    1. Vorontsov N.N., Lyapunova E.A., Borissov Y.M., Dovgal V.E. Variability of sex chromosomes in mammals. Genetica. 1980;52/53:361–372. doi: 10.1007/BF00121845. - DOI
    1. Vogel W., Steinbach P., Djalali M., Mehnert K., Ali S., Epplen J.T. Chromosome 9 of Ellobius lutescens is the X chromosome. Chromosoma. 1988;96:112–118. doi: 10.1007/BF00331043. - DOI - PubMed
Feedback