Abstract

To make insight into the cytological basis of reproductive isolation, we examined chromosome synapsis and recombination in sterile male and female hybrids between Microtus arvalis and M. levis. These sibling species differ by a series of chromosomal rearrangements (fusions, inversions, centromere shifts and heterochromatin insertions). We found that meiosis in male hybrids was arrested at leptotene with complete failure of chromosome pairing and DNA double-strand breaks repair. In the female hybrids meiosis proceeded to pachytene; however, the oocytes varied in the degree of pairing errors. Some of them demonstrated almost correct chromosome pairing, while most of them contained a varying number of univalents and multivalents with extensive regions of asynapsis and non-homologous synapsis. Variation between oocytes was probably caused by stochasticity in the ratio of homologous to non-homologous pairing initiations. We suggest that substantial chromosomal and genetic divergence between the parental species affects preliminary alignment of homologues, homology search and elimination of ectopic interhomologue interactions that are required for correct homologous pairing. Apparently, pairing failure in male and aberrant synapsis in female vole hybrids followed by meiotic silencing of unsynapsed chromatin cause apoptosis of gametocytes and sterility.

Highlights

  • By synaptic aberrations of autosomes and sex chromosomes has been widely reported in hybrids of chromosomally divergent mammalian species, subspecies and local populations[3,11,12,13,14,15,16,17,18,19]

  • To make insight into the cytological basis of hybrid sterility, we examined chromosome synapsis and recombination in male and female sterile hybrids between two sibling species of the grey vole, Microtus arvalis and M. levis

  • This study supports breeding records and histological assessments showing the sterility of hybrids between M. arvalis and M. levis[35,36,37,38,39,41]

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Summary

Introduction

By synaptic aberrations of autosomes and sex chromosomes has been widely reported in hybrids of chromosomally divergent mammalian species, subspecies and local populations[3,11,12,13,14,15,16,17,18,19]. To make insight into the cytological basis of hybrid sterility, we examined chromosome synapsis and recombination in male and female sterile hybrids between two sibling species of the grey vole, Microtus arvalis (dams) and M. levis (sires). These species diverged from 0.5 to 4.3 MYA32,33, differ by a series of chromosomal rearrangements[33,34], yet remain morphologically indistinguishable[35]. The number and distribution of recombination events were estimated by immunolocalisation of MLH144 This analysis allowed us to detect meiotic aberrations leading to hybrid sterility

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