Major Regularities of Transformation of the Small Mammal Ovaries in Unfavourable Environmental Conditions: Ecological and Morphological Aspects

The aim of the study was to determine the patterns of structural and functional organization of the ovaries of female small mammals inhabiting technogenically altered ecosystems.Material and methods. We studied the ovaries of small mammal species belonging to the insectivore and rodent families (common shrew, field and pygmy wood mice, common and bank voles, mole vole, steppe pied) that live in anthropogenically altered ecosystems (zones of influence of ferrous and nonferrous metallurgy, as well as gas processing factory). The resulting material was processed using observational histological, histochemical, immunohistochemical and morphometric tests.Results. The results obtained demonstrated that in technogenically altered ecosystems the intensified reproduction results in a complex of morphofunctional reactive and adaptive changes in the ovaries of females of the studied species. The size of the ovaries was reduced; the area of the cortical substance was reduced. In the cortex, there was revealed a decrease in the number of follicles varying over a wide range - from a moderate decrease to their almost complete absence. There was found a decrease in the area of the vessels of the microvasculature; this was one of the major reasons for the increased follicular atresia. In follicles of various types, there was an increase in the proportion of cells expressing the proapoptotic protein P53. A decrease in the number of follicles resulted in the connective tissue overgrowth. The presence of cysts lined with epithelium of various heights was revealed in the cortex and medulla. Conclusion. The results obtained evidence that in technogenically altered ecosystems a decreased ovarian reserve is observed in the ovaries of female small mammals; it is associated with a more rapid depletion of the follicle reserve in the cortex due to both - intensification of reproduction and more rapid death of follicles in unfavourable environmental conditions.

Meiotic Nuclear Architecture in Distinct Mole Vole Hybrids with Robertsonian Translocations: Chromosome Chains, Stretched Centromeres, and Distorted Recombination

Genome functioning in hybrids faces inconsistency. This mismatch is manifested clearly in meiosis during chromosome synapsis and recombination. Species with chromosomal variability can be a model for exploring genomic battles with high visibility due to the use of advanced immunocytochemical methods. We studied synaptonemal complexes (SC) and prophase I processes in 44-chromosome intraspecific (Ellobius tancrei × E. tancrei) and interspecific (Ellobius talpinus × E. tancrei) hybrid mole voles heterozygous for 10 Robertsonian translocations. The same pachytene failures were found for both types of hybrids. In the intraspecific hybrid, the chains were visible in the pachytene stage, then 10 closed SC trivalents formed in the late pachytene and diplotene stage. In the interspecific hybrid, as a rule, SC trivalents composed the SC chains and rarely could form closed configurations. Metacentrics involved with SC trivalents had stretched centromeres in interspecific hybrids. Linkage between neighboring SC trivalents was maintained by stretched centromeric regions of acrocentrics. This centromeric plasticity in structure and dynamics of SC trivalents was found for the first time. We assume that stretched centromeres were a marker of altered nuclear architecture in heterozygotes due to differences in the ancestral chromosomal territories of the parental species. Restructuring of the intranuclear organization and meiotic disturbances can contribute to the sterility of interspecific hybrids, and lead to the reproductive isolation of studied species.

Meiotic nuclear architecture in distinct mole vole hybrids with Robertsonian translocations: chromosome chains, stretched centromeres, and distorted recombination

Genome functioning in hybrids faces inconsistency. This mismatch is manifested clearly in meiosis during chromosome synapsis and recombination. Species with chromosomal variability can be a model for exploring genomic battles with high visibility due to the use of advanced immunocytochemical methods. We studied synaptonemal complexes (SC) and prophase I processes in 44-chromosome intraspecific (Ellobius tancrei × E. tancrei) and interspecific (Ellobius talpinus × E. tancrei) hybrid mole voles heterozygous for 10 Robertsonian translocations. The same pachytene failures were found for both types of hybrids. In the intraspecific hybrid, the chains were visible in the pachytene stage, then 10 closed SC trivalents formed in the late pachytene and diplotene stage. In the interspecific hybrid, as a rule, SC trivalents composed the SC chains and rarely could form closed configurations. Metacentrics involved with SC trivalents had stretched centromeres in interspecific hybrids. Linkage between neighboring SC trivalents was maintained by stretched centromeric regions of acrocentrics. This centromeric plasticity in structure and dynamics of SC trivalents was found for the first time. We assume that stretched centromeres were a marker of altered nuclear architecture in heterozygotes due to differences in the ancestral chromosomal territories of the parental species. Restructuring of the intranuclear organization and meiotic disturbances can contribute to the sterility of interspecific hybrids, and lead to the reproductive isolation of studied species.Author summaryMeiosis is essential for sexual reproduction to produce haploid gametes. Prophase I represents a crucial meiotic stage because key processes such as chromosomal pairing, synapsis and desynapsis, recombination, and transcriptional silencing occur at this time. Alterations in each of these processes can activate meiotic checkpoints and lead to the elimination of meiocytes. Here we have shown that two groups of experimental hybrids, intraspecific and interspecific—which were heterozygous for 10 identical Robertsonian translocations—had pachytene irregularities and reduced recombination. However, intraspecific and interspecific hybrids exhibited different patterns of synaptonemal complex (SC) trivalent behavior. In the former, open SC trivalents comprised SC chains due to heterosynapsis of short arms of acrocentrics in early and mid-pachytene and were then able to form 2–4 and even 7 and 10 closed SC trivalents in the late pachytene and diplotene stages. In the second mole voles, SC trivalents had stretched centromeres of the metacentrics, and chains of SC trivalents were formed due to stretched centromeres of acrocentrics. Such compounds could not lead to the formation of separate closed SC trivalents. The distant ancestral points of chromosome attachment with a nuclear envelope in the heterozygous nuclei probably lead to stretching of SC trivalents and their centromeric regions, which can be regarded as an indicator of the reorganization of the intranuclear chromatin landscape. These abnormalities, which were revealed in in prophase I, contribute to a decrease the fertility of intraspecific mole voles and promote the sterility of interspecific mole voles.

Meiotic Chromosome Contacts as a Plausible Prelude for Robertsonian Translocations

Robertsonian translocations are common chromosomal alterations. Chromosome variability affects human health and natural evolution. Despite the significance of such mutations, no mechanisms explaining the emergence of such translocations have yet been demonstrated. Several models have explored possible changes in interphase nuclei. Evidence for non-homologous chromosomes end joining in meiosis is scarce, and is often limited to uncovering mechanisms in damaged cells only. This study presents a primarily qualitative analysis of contacts of non-homologous chromosomes by short arms, during meiotic prophase I in the mole vole, Ellobius alaicus, a species with a variable karyotype, due to Robertsonian translocations. Immunocytochemical staining of spermatocytes demonstrated the presence of four contact types for non-homologous chromosomes in meiotic prophase I: (1) proximity, (2) touching, (3) anchoring/tethering, and (4) fusion. Our results suggest distinct mechanisms for chromosomal interactions in meiosis. Thus, we propose to change the translocation mechanism model from ‘contact first’ to ‘contact first in meiosis’.