Sex chromosome variability outlines the pathway to the chromosomal evolution in Microtus thomasi (Rodentia, Arvicolinae)

Abstract

The underground vole Microtus thomasi, a Balkan endemic, displays remarkable variability in sex chromosome size and morphology. In the present study, we demonstrate this variability in two of its chromosomal races with 2n = 44 (i.e. 'thomasi' and 'atticus') with the use of C-banding on a sample of 189 individuals from 50 localities of Greece. In 'thomasi', five different, acrocentric X chromosome variants (X0-X4) are described, which differ significantly in size, due to heterochromatin addition. Also, three Y chromosome variants are described (Y0-Y2), ranging in size from very small (Y0) to large (Y2). The 'atticus' race displays three subtelocentric variants of the X chromosome (Xst0-Xst2), which differ in arm length ratio and heterochromatin content. In Peloponnesus, males of this race exhibit Y0 and Y1, whereas, in Attiki (south-east Sterea Ellada), males carry the small metacentric, Ym. Overall, there is a trend towards sex chromosome size increase in a south to north direction. We propose that the last glaciation must have restricted M. thomasi to a refugium in southern Peloponnesus. During post-glacial colonization, limited northward expansion of its distribution area must have been accompanied by consecutive heterochromatin addition, which is proven today by comparatively larger sex chromosomes in the northern populations of 'thomasi' and 'atticus' in Greece than in their southern populations.

A new pericentromeric repeated DNA sequence in <i>Microtus thomasi</i>

“…These clones showed length differences as . All X and Y chromosomes are from 'thomasi' and 'atticus' specimens from Greece as described by Mitsainas et al (2008), with the exception of X alb and Y alb , which are from a 'thomasi' specimen from Albania.…”

“…The sex chromosome constitutions of all the individuals analyzed by FISH were previously determined by C-banding (see Mitsainas et al, 2008). We have analyzed the distribution of this repeat in four acrocentric X chromosomes (X 0 , X 1 , X 2 , X 3 ) and in two acrocentric Y chromosomes (Y 0 , Y 2 ) from 'thomasi' specimens of Greece.…”

“…Two alternative hypotheses have been proposed to explain the origin of the subtelocentric X st0 and X st1 chromosomes of 'atticus' from the acrocentric X chromosomes of 'thomasi': a) a pericentric inversion in one acrocentric X chromosome from the karyomorph 'thomasi' (supposed to be X 1 ), followed by heterochromatin amplification; b) a chromosomal translocation on one of the acrocentric 'tho masi' X chromosomes, followed by heterochromatin amplification (Giagia-Athanasopoulou and Stamatopoulos, 1997;Mitsainas et al, 2008). Both hypotheses imply that the short and long arm heterochromatic blocks of 'atticus' subtelocentric X chromosomes have independent origin, and also that the heterochromatic block of the long arm of these chromosomes originated de novo by amplification of repeat sequences.…”

Comparative Analysis by Chromosome Painting of the Sex Chromosomes in Arvicolid Rodents

“…Regarding the genus Microtus, 60 different species have evolved since the radiation of the genus which occurred approximately 1.6 million years ago [Chaline and Graf, 1988], presenting one of the most remarkable rates of karyotype variability [Maruyama and Imai, 1981]. As examples of rapid karyotype evolution in arvicolids the species Microtus thomasi and Microtus savii could be mentioned where 5 chromosomal races and 4 subspecies are described respectively [Castiglia et al, 2008;Mitsainas et al, 2009].…”

Molecular and Physical Characterization of the Complex Pericentromeric Heterochromatin of the Vole Species Microtus thomasi

“…The sex chromosomes vary in morphology (from acrocentric to metacentric) and size due to variation in the amount of constitutive heterochromatin [Modi, 1987a, b;Burgos et al, 1988a, b;Mitsainas et al, 2009]. The sibling vole species M. thomasi and M. atticus are remarkable models for studies on the chromosomal evolution, since they probably demonstrate the highest rate of karyotypic diversity among Microtus species.…”