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

Abstract

Evolutionary history and taxonomic position for cryptic species may be clarified by using molecular and cytogenetic methods. The subterranean rodent, the Alay mole vole Ellobiusalaicus Vorontsov et al., 1969 is one of three sibling species constituting the subgenus Ellobius Fischer, 1814, all of which lost the Y chromosome and obtained isomorphic XX sex chromosomes in both males and females. E.alaicus is evaluated by IUCN as a data deficient species because their distribution, biology, and genetics are almost unknown. We revealed specific karyotypic variability (2n = 52–48) in E.alaicus due to different Robertsonian translocations (Rbs). Two variants of hybrids (2n = 53, different Rbs) with E.tancrei Blasius, 1884 were found at the Northern slopes of the Alay Ridge and in the Naryn district, Kyrgyzstan. We described the sudden change in chromosome numbers from 2n = 50 to 48 and specific karyotype structure for mole voles, which inhabit the entrance to the Alay Valley (Tajikistan), and revealed their affiliation as E.alaicus by cytochrome b and fragments of nuclear XIST and Rspo1 genes sequencing. To date, it is possible to expand the range of E.alaicus from the Alay Valley (South Kyrgyzstan) up to the Ferghana Ridge and the Naryn Basin, Tien Shan at the north-east and to the Pamir-Alay Mountains (Tajikistan) at the west. The closeness of E.tancrei and E.alaicus is supported, whereas specific chromosome and molecular changes, as well as geographic distribution, verified the species status for E.alaicus. The case of Ellobius species accented an unevenness in rates of chromosome and nucleotide changes along with morphological similarity, which is emblematic for cryptic species.

Meiotic Chromosome Contacts as a Plausible Prelude for Robertsonian Translocations

“…In the middle pachytene, the XX-bivalent was usually shifted to the periphery of the meiotic nucleus and had two telomeric synaptic regions, a wide asynaptic region, and chromatin bodies on axial elements (Figure 2f). It should be noted that sometimes chromatin (nucleolus-like) bodies in sex bivalents were SYCP3-positive ( Figure 1, Figure 2e,f), which has not been previously observed for the other two cryptic species and E. alaicus (2n = 48) from the Pamir-Alay [50]. axial elements of homologous chromosomes began to contact each other ( Figure S3), and synapsed more frequently from telomere areas to the central part ( Figure 2c), less often in the opposite way ( Figure 2d).…”

“…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].…”

“…All animals demonstrated normal for E. alaicus karyotypes; 2n = 52. the fundamental number of chromosome arms (NF) was 56 ( Figure S1a-f), consisting of one pair of submetacentrics (№7), characteristic of E. tancrei and E. alaicus, and one pair of large Robertsonian metacentrics 2(Rb2.11), typical of E. alaicus [50]. Mitotic metaphases from bone marrow suspensions showed no visible alterations ( Figure S1b).…”

“…For example, chromosome №1, which was the most regularly seen in all three types of true interactions ('touching', 'anchoring/tethering', and 'fusion'). Rb(1.3) was described in E. alaicus with 2n = 50 [50].…”

“…E. alaicus is very close to E. tancrei, a translocation Rb(2.11) emerged in both species; other Rbs are species-specific ones. E. alaicus demonstrates rapid chromosomal changes in nature, such as the fixation of Rbs in the large population in the Pamir-Alay [50]. In this study, we analyzed the meiotic sustainability of species with rapidly evolving genome.…”