Abstract

The generic status of Lasiopodomys and its division into subgenera Lasiopodomys (L. mandarinus, L. brandtii) and Stenocranius (L. gregalis, L. raddei) are not generally accepted because of contradictions between the morphological and molecular data. To obtain cytogenetic evidence for the Lasiopodomys genus and its subgenera and to test the autosome to sex chromosome translocation hypothesis of sex chromosome complex origin in L. mandarinus proposed previously, we hybridized chromosome painting probes from the field vole (Microtus agrestis, MAG) and the Arctic lemming (Dicrostonyx torquatus, DTO) onto the metaphases of a female Mandarin vole (L. mandarinus, 2n = 47) and a male Brandt's vole (L. brandtii, 2n = 34). In addition, we hybridized Arctic lemming painting probes onto chromosomes of a female narrow-headed vole (L. gregalis, 2n = 36). Cross-species painting revealed three cytogenetic signatures (MAG12/18, 17a/19, and 22/24) that could validate the genus Lasiopodomys and indicate the evolutionary affinity of L. gregalis to the genus. Moreover, all three species retained the associations MAG1bc/17b and 2/8a detected previously in karyotypes of all arvicolins studied. The associations MAG2a/8a/19b, 8b/21, 9b/23, 11/13b, 12b/18, 17a/19a, and 5 fissions of ancestral segments appear to be characteristic for the subgenus Lasiopodomys. We also validated the autosome to sex chromosome translocation hypothesis on the origin of complex sex chromosomes in L. mandarinus. Two translocations of autosomes onto the ancestral X chromosome in L. mandarinus led to a complex of neo-X1, neo-X2, and neo-X3 elements. Our results demonstrate that genus Lasiopodomys represents a striking example of rapid chromosome evolution involving both autosomes and sex chromosomes. Multiple reshuffling events including Robertsonian fusions, chromosomal fissions, inversions and heterochromatin expansion have led to the formation of modern species karyotypes in a very short time, about 2.4 MY.

Highlights

  • Rodentia is the most species-rich mammalian order and includes several important laboratory model species

  • According to the analysis of nuclear genes the genus Lasiopodomys originated within the tribe Arvicolini Gray, 1821, approximately 2.4 million years ago (MYA), and the division of that genus into subgenera Stenocranius and Lasiopodomys occurred about 1.8 MYA [3,10]

  • One female L. mandarinus, one male L. brandtii, and one female L. gregalis specimens used in this study were obtained from the laboratory colonies housed at the Leningrad Zoo and the Institute of Zoology of Russian Academy of Sciences (L. mandarinus originated from Selenginsky District, Buryatia; L. brandtii–from Cape Telly, Torey Lake, Borzinskiy District, Chita region, Zabaikalsky Kray; L. gregalis–from River Kadala, Chitinsky District, Zabaikalsky Kray)

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Summary

Introduction

Rodentia is the most species-rich mammalian order and includes several important laboratory model species. Molecular data have indicated a kinship between Lasiopodomys and Stenocranius [2,3,4,5], while L. fuscus has been considered part of the large clade of East Asian voles of genus Neodon Hodgson, 1849 [6]. Based on these findings Pavlinov and Lissovsky [7] subdivided Lasiopodomys into two subgenera with three species: subgenus Lasiopodomys (L. mandarinus and L. brandtii) and subgenus Stenocranius (L. gregalis Pallas, 1779). According to the analysis of nuclear genes the genus Lasiopodomys originated within the tribe Arvicolini Gray, 1821, approximately 2.4 million years ago (MYA), and the division of that genus into subgenera Stenocranius and Lasiopodomys occurred about 1.8 MYA [3,10]

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