Rapid Karyotype Evolution in Lasiopodomys Involved at Least Two Autosome - Sex Chromosome Translocations

PLoS One. 2016 Dec 9;11(12):e0167653. doi: 10.1371/journal.pone.0167653. eCollection 2016.

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.

MeSH terms

  • Animals
  • Arvicolinae / genetics*
  • Cytogenetics
  • Evolution, Molecular*
  • Female
  • Karyotype
  • Karyotyping
  • Male
  • Phylogeny
  • Sex Chromosomes / genetics*
  • Translocation, Genetic*

Grants and funding

The study was funded by the by the Russian Science Foundation (RSF, http://rscf.ru/) under project No. 16-14-10009 to ASG. This work was partially supported by the Programs of the Federal Agency for Scientific Organizations (FASO Russia, http://fano.gov.ru/) No. 01201351185 to FNG for the animals collection and No. 0310-2016-0002 for cell culture collection to ASG. Significant funding was also provided by the Russian Foundation for Basic Research (RFBR, http://www.rfbr.ru/) grants No. 14-04-00451 to SAR, No. 15-04-00962 and No. 15-29-02384 both to ASG, No. 16-04-00983-a to FNG for the animals and tissue cell collections.