Karyotype Reorganisation in the <i>subtilis</i> Group of Birch Mice (Rodentia, Dipodidae, <i>Sicista</i>): Unexpected Taxonomic Diversity within a Limited Distribution

Abstract

Conventional cytogenetic studies of Sicista subtilis and S. severtzovi (Dipodidae, Sicistinae), both attributable to the subtilis group of birch mice, revealed extensive karyotype diversity with 2n = 16–26 and NFa values of 26–46 indicating the overwhelming non-Robertsonian nature of chromosomal reorganization in these species. The numerical and structural chromosome variability was principally found in specimens located within a confined region of the East European (Russian) Plain. The approximately 135,000-km² area occurs in the vicinity of the Don River bend between 49°13’N/43°46’E and 51°32’N/36°16’E. The detection of cytotypes sharing similar 2n and NF values, but having morphologically distinct chromosomes, suggests that these may result from polymorphisms present both within recognized species and in cryptic taxa not hitherto described. We conducted a comprehensive, comparative chromosome banding analysis of 52 birch mice (21 localities) referable to the subtilis group and report the presence of 5 distinct karyotypes, each characterized by a combination of stable, variable, and partly overlapping 2n/NFa values. These karyotypes differed from each other by 10–29 structural chromosomal rearrangements (18.1 ± 6.3) that comprised Rb fusions/fissions (42.2%), pericentric inversions (31.1%), and tandem translocations (22.2%). The composition, and the high numbers of these chromosomal changes, is likely to provide an effective means of post-mating isolation, suggesting that taxonomic diversity within the subtilis group is larger than currently accepted. Additionally, we report the frequent fixation of tandem translocations in sample populations, one of which was found in a polymorphic state representing, as far as we are aware, the first case of an in statu nascendi tandem fusion in wild populations. Moreover, our data revealed that bi-armed chromosomes were involved in fusions detected in some of the subtilis taxa. In each instance, however, fusions were preceded by pericentric inversions that transform one or both bi-armed chromosomes into acrocentrics resulting in either centromere-telomere or Robertsonian translocations. Finally, a phylogenetic scenario inferred from a cladistic analysis of the chromosomal data suggests that the extensive karyotypic diversification within the subtilis group in the south-east region of the Russian Plain most likely results from fragmentation of a continuously distributed, ancestral population. It is thought that this occurred at the last glacial maximum (18,000–14,000 years B.P.), and that the process of isolation has been exacerbated by increasing human activity in the region in modern times.

Non-Sciuromorph Rodent Karyotypes in Evolution

“…Most displayed monobrachial homology and tandem translocations (22%); one was found in a polymorphic state representing, as far as we are aware, the first case of an in statu nascendi tandem fusion in wild populations [Kovalskaya et al, 2011]. It appeared that the PIs, also numerous (28%), played a very special role in karyotype reorganization.…”

“…Pericentric inversions (PIs) are a second class of rearrangements that are particularly frequent in rodents ( Peromyscus : Greenbaum et al [1994] and references herein; Akodon : Fagundes et al [1997], Silva and Yonenaga-Yassuda [1998] and references herein; Mastomys : Volobouev et al [2001, 2002a]; Microtus : Lemskaya et al [2010]; Sicista : Kovalskaya et al [2011]; and many other groups: Trifonov et al [2010a]). PIs change only the number of chromosomal arms and not the diploid chromosome number, one-armed chromosomes can be transformed into bi-armed ones or vice versa.…”

“…Volobouev et al, 2002a;Dobigny et al, 2005;Swier et al, 2009;Ventura et al, 2009]. The relatively rare fixation of tandem translocations in karyotype evolution of mammals and the only documented instance of a polymorphism for this chromosomal change [Kovalskaya et al, 2011] strongly suggests that when they occur and reach a homozygous state, they probably insure an almost instantly and complete reproductive isolation [Dobigny et al, 2005]. For these reasons the fixation of multiple tandem translocations in closely related species remains a rare evolutionary event except in the case of Muntiacus species [Yang et al, 1997;Wang and Lan, 2000].…”

“…For these reasons the fixation of multiple tandem translocations in closely related species remains a rare evolutionary event except in the case of Muntiacus species [Yang et al, 1997;Wang and Lan, 2000]. It was observed only twice: in the gerbils of the genus Taterillus [Dobigny et al, 2002[Dobigny et al, , 2003[Dobigny et al, , 2005 and the birch mice of the genus Sicista [Kovalskaya et al, 2011]. Taking into account that karyotype evolution in these taxa is unusual for a number of aspects, we consider these cases in more details below.…”

“…However, the intrapopulation numeric and/or morphological chromosome variability is regularly much narrower than that observed within the whole species range. In this context, the study of the extensive karyotype reorganization in the species of the genera Taterillus [Dobigny et al, 2005 and references herein] and Sicista [Kovalskaya et al, 2011] contributed significantly to our understanding of the mechanisms of chromosomal evolution and speciation.…”