Rare three-chromosome fusion reveals hidden complexity in Russian vole

A chromosome study of the Evoron vole, Alexandromys evoronensis, has uncovered an unusual genetic configuration in which three autosomes fuse into a single large chromosome. Researchers examining two isolated populations in the Russian Far East found the fusion in a heterozygous state, meaning each affected animal carried the rearranged chromosome alongside its normal counterparts. The discovery expands the known karyotypic diversity of this endemic vole, revealing a total of 20 chromosome variants across two broadly recognized chromosomal races. The findings also show how rapidly structural chromosome changes can accumulate within geographically separated populations and provide a new case for studying the molecular mechanics of chromosome fusion.

The research focused on voles belonging to the “Argi” chromosomal race, which occurs in the mountainous landscapes of the southern Russian Far East. The team analyzed 17 wild animals from the Urgal River valley in the Upper Bureya Depression of Khabarovsk Territory and the Argi River valley in the Upper Zeya Plain of Amur Region. They also examined 22 laboratory-bred descendants of animals from the second population. Chromosomes were prepared from bone-marrow cells and examined using G-banding, C-banding and staining for nucleolar organizer regions. At least 20 chromosome plates per animal were analyzed so that chromosome number and structural differences could be assessed accurately.

Across the two wild populations, the researchers identified eight karyotype variants: two with 34 chromosomes, four with 36 and two with 37. The diploid chromosome number in the Argi race therefore spans 34 to 37, while the number of chromosome arms ranges from 51 to 56. Most of the wild voles, 76.5% of the sample, carried the 36-chromosome form, which the researchers identified as the principal karyotype of the race. Variation was concentrated in particular chromosome pairs rather than being distributed evenly across the genome. Nine chromosomes were involved in multiple structural rearrangements in the Argi race, compared with four in the geographically distinct Evoron race.

The most unusual discovery was a large biarmed chromosome designated Mev6/7/14. It formed through tandem fusion of two metacentric autosomes, Mev6 and Mev7, and one acrocentric autosome, Mev14. One wild female from the Urgal River population and one wild male from the Argi River population carried the fusion. In both cases, Mev6/7/14 was heterozygous, while the three chromosomes from which it had formed remained in their normal form on the other homolog. A karyotype with 32 chromosomes would be theoretically possible if the fused element occurred in both homologs, but that configuration was not observed.

That arrangement is particularly important because tandem fusions can place chromosome ends together in ways that interfere with the production of balanced gametes. Earlier work has associated such heterozygous fusions with reductions of at least 50% in balanced gamete production, making them potentially more disruptive than some conventional chromosome fusions. The Evoron vole therefore provides an unusual opportunity to examine how a three-chromosome tandem fusion persists in natural populations, whether it affects reproduction and how its telomeric regions are converted during rearrangement. The authors call for further study of the DNA transformation system at the chromosome ends, including possible recombination hot spots that could facilitate fusion.

The Argi race also displayed recurring variation involving chromosomes Mev11, Mev13, Mev15, Mev17, Mev18 and Mev19. A fusion of Mev11 and Mev19 was consistently present in a homozygous state in all specimens from both populations, suggesting that this rearrangement had already stabilized. By contrast, Mev13/15 and the Robertsonian product Mev13.15 appeared in different combinations, including matched acrocentric or metacentric pairs and heteromorphic pairs containing one chromosome of each type. The same pattern occurred for Mev17/18 and its metacentric Robertsonian counterpart Mev17.18. The researchers interpret this as evidence that these fusions had not reached fixation and that centromere repositioning may be involved.

Breeding results showed that the unstable-looking Mev13/15 and Mev13.15 combination did not have an apparent effect on offspring viability. During 16 months of breeding, the animals produced 18 litters and 92 young in the first and second generations. Among 22 first-generation laboratory voles with 36 chromosomes, the three morphological combinations of the relevant chromosomes occurred in a 1:2:1 ratio. This distribution was consistent with the rearrangement having little or no measurable effect on fertility or survival under the laboratory conditions. Animals with a different total chromosome number were not bred, so the reproductive consequences of the rarer Mev6/7/14 fusion remain unknown.

Comparison with the Evoron race showed that both groups share particular forms of rearrangement involving Mev17 and Mev18, including the tandem fusion Mev17/18 and the metacentric Robertsonian product Mev17.18. The races nevertheless differ in overall chromosome number and in their broader combination of structural changes. The Evoron race, first identified around Lake Evoron, has diploid numbers from 38 to 41 and arm numbers from 54 to 59. The Argi race has lower totals, from 34 to 37, with arm numbers of 51 to 56. Both populations sampled for the Argi race contained the same broad set of variants despite being separated by mountain ranges and roughly 500 kilometers, indicating that the observed polymorphisms are not confined to a single local population.

The results broaden the species-level picture to 20 karyotype variants, with 11 chromosomes participating in multiple structural rearrangements. The Evoron race includes rearrangements involving Mev1, Mev4, Mev17 and Mev18, whereas the Argi race includes Mev6, Mev7, Mev14, Mev13, Mev11, Mev15, Mev17, Mev18 and Mev19. Taken together with earlier mitochondrial-DNA evidence, the chromosome data suggest recent population-level divergence rather than a deeply separated evolutionary history. The study also illustrates the speed of karyotype evolution in Alexandromys: five structural transformations appear to have occurred in A. evoronensis over a relatively short geological interval, while related vole lineages also exhibit numerous fusions and other rearrangements.

For researchers studying speciation, the central implication is that chromosomes can remain variable even when mitochondrial variation indicates that populations have only recently diverged. The same major rearrangements may persist across isolated mountain habitats, while other fusions remain unstable and generate multiple forms within a single population. Future work will need to test whether the remarkable Mev6/7/14 fusion affects mating success or reproductive output in the wild, determine how the participating centromeres and telomeres reorganize, and establish whether chromosome painting can map the rearrangements at the level of genome segments. The study turns an unusual-looking chromosome into a natural experiment for watching structural change unfold in real time.

Subject of Research: Chromosomal polymorphism and rare tandem fusion in the Evoron vole

Article Title: Intraspecies multiple chromosomal variations including rare tandem fusion in the Russian Far Eastern endemic evoron vole Alexandromys evoronensis ( Rodentia , Arvicolinae )

Article References: Kartavtseva, I. V., Sheremetyeva, I. N., & Pavlenko, M. V. (2021). Intraspecies multiple chromosomal variations including rare tandem fusion in the Russian Far Eastern endemic evoron vole Alexandromys evoronensis (Rodentia, Arvicolinae). Comparative Cytogenetics, 15(4), 393-411. https://doi.org/10.3897/compcytogen.v15.i4.67112

Image Credits: AI Generated

DOI: 10.3897/compcytogen.v15.i4.67112

Keywords: Evoron vole, chromosome fusion, karyotype variation, tandem fusion, Robertsonian translocation, centromere repositioning, Russian Far East, Alexandromys evoronensis, chromosomal polymorphism, mammalian evolution, Intraspecies, multiple