Structural and Evolutionary Relationships in the Giant Sex Chromosomes of Three Microtus Species

Abstract

The genus Microtus has high karyotypic diversity. The existence of notable differences in the length of its sex chromosomes contributes to this variation. Variations in size are attributed to the enlargement of their heterochromatin content, which is of such magnitude in some species that they are referred to as “giant sex chromosomes”. Here, we perform an intra- and interspecific analysis of the molecular composition of the heterochromatic blocks in three species with giant sex chromosomes (Microtus chrotorrhinus, M. cabrerae and M. agrestis). Our results show that the heterochromatic content is very similar in both the X and Y chromosomes of M. chrotorrhinus, and that their molecular composition is more closely related to the heterochromatic blocks of M. agrestis than to the sex heterochromatin of M. cabrerae; however, species-specific differences do clearly exist. Interestingly, the euchromatic regions of the X chromosome of all three of these species share a homologous region composed of heterochromatic-related sequences. Our results therefore reinforce the idea that certain similarities in the original organization of these X chromosomes could have facilitated their later enlargement.

Complete Mitochondrial Genome of Three Species of the Genus Microtus (Arvicolinae, Rodentia)

“…Ostensibly, M. cabrerae and M. agrestis share certain unusual genetic features, including the presence of giant sex chromosomes, which could be regarded as additional proof of their phylogenetic proximity. However, several studies have clearly demonstrated that these enlarged sex chromosomes arose and evolved independently in the genus Microtus [ 4 ], and hence, their presence is not a robust criterion for the inclusion of M. cabrerae and M. agrestis in the same subgenus. A previous mitochondrial phylogenetic reconstruction obtained similar results, with M. cabrerae and M. agrestis clustered in the same clade, but the level of genetic divergence indicated that both species could be considered as members of two different subgenera ( Agricola and Iberomys ) [ 29 ].…”

“…A single male specimen of M. cabrerae (Siles, Spain (TOPC-0902)) and one of M. thomasi (Edessa, Greece, (R231)) were used for DNA extraction, while for M. chrotorrhinus (North America), an established cell line from a male individual was employed [ 4 , 40 ]. All capture and sacrifice protocols were approved by the Junta de Andalucía Ethics Committee for Animal Experimentation (code: 04/09/2018/130).…”

“…Some species from the genus Microtus are characterized by a series of unusual sex-related genetic features [ 3 , 4 , 5 , 6 , 7 , 8 , 9 , 10 ]. Moreover, the genus Microtus shows one of the highest rates of karyotype variation of all mammals [ 11 ], with highly variable chromosome numbers ranging from 2n = 18 in M. oregoni [ 12 ] to 2n = 62 in M. duodecimcostatus and M. lusitanicus [ 13 ].…”

“…This genus underwent fast recent radiation about 1.2-2 million years ago (MYA) [2] in what was one of the most explosive speciation events ever recorded in vertebrates [1]. Some species from the genus Microtus are characterized by a series of unusual sex-related genetic features [3][4][5][6][7][8][9][10]. Moreover, the genus Microtus shows one of the highest rates of karyotype variation of all mammals [11], with highly variable chromosome numbers ranging from 2n = 18 in M. oregoni [12] to 2n = 62 in M. duodecimcostatus and M. lusitanicus [13].…”

Molecular Composition of Heterochromatin and Its Contribution to Chromosome Variation in the Microtus thomasi/Microtus atticus Species Complex

“…Karyotype evolution encompassed a series of fusion/fission rearrangements, inversions, and centromeric shifts, accompanied by other cryptic intrachromosomal rearrangements [6,7], leading to extensive variability in chromosome numbers ranging from 2n = 17 in Ellobius lutescens to 2n = 62 in M. duodecimcostatus and M. lusitanicus [8,9]. Some species from the genus Microtus are characterized by atypical sex-related genetic features that range from an unusual sex determination system to extensive sex chromosome polymorphisms [10][11][12][13][14][15][16][17][18][19][20][21][22][23][24]. In the genus Microtus, a numerous collection of variants evolved from an ancestral sex chromosome pair, even within related species or at intraspecific level [8,[25][26][27][28].…”