Abstract

The mandarin vole, Lasiopodomys mandarinus, is one of the most intriguing species among mammals with non-XX/XY sex chromosome system. It combines polymorphism in diploid chromosome numbers, variation in the morphology of autosomes, heteromorphism of X chromosomes, and several sex chromosome systems the origin of which remains unexplained. Here we elucidate the sex determination system in Lasiopodomys mandarinus vinogradovi using extensive karyotyping, crossbreeding experiments, molecular cytogenetic methods, and single chromosome DNA sequencing. Among 205 karyotyped voles, one male and three female combinations of sex chromosomes were revealed. The chromosome segregation pattern and karyomorph-related reproductive performances suggested an aberrant sex determination with almost half of the females carrying neo-X/neo-Y combination. The comparative chromosome painting strongly supported this proposition and revealed the mandarin vole sex chromosome systems originated due to at least two de novo autosomal translocations onto the ancestral X chromosome. The polymorphism in autosome 2 was not related to sex chromosome variability and was proved to result from pericentric inversions. Sequencing of microdissection derived of sex chromosomes allowed the determination of the coordinates for syntenic regions but did not reveal any Y-specific sequences. Several possible sex determination mechanisms as well as interpopulation karyological differences are discussed.

Highlights

  • Most therian mammals have a conventional XX/XY sex chromosome system with the Y-borne testis-determining SRY gene

  • Karyomorph II (KII, 47% of the studied females) corresponded to the sex chromosome system described by Gladkikh et al [10] and had 2n = 47 with neo-X1, neo-X2, and neo-X3

  • The fascinating sex chromosome polymorphism of the mandarin vole raises three closely related questions: (1) How is such an unusual system maintained in a population? (2) How did the system evolve, that is, what chromosome rearrangements led to the polymorphism of sex chromosomes?

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Summary

Introduction

Most therian mammals have a conventional XX/XY sex chromosome system with the Y-borne testis-determining SRY gene. Several dozen species with nonstandard systems of chromosomal sex determination have been described among mammals [1]. Most species of mammals with aberrant sex chromosome systems belong to the subfamily Arvicolinae (Myomorpha, Rodentia). One such example is the mandarin vole, Lasiopodomys mandarinus. The first karyotype descriptions of L. mandarinus made in the 1970s and further works showed the variability of chromosomal numbers among and within populations of this species. In the mandarin voles from Mongolia and Buryatia (Lasiopodomys mandarinus vinogradovi) the diploid chromosome number (2n) is 47–48 [3], whereas Chinese populations display 2n = 49–52

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