Chromosome Synapsis and Recombination in Male Hybrids between Two Chromosome Races of the Common Shrew (Sorex araneus L., Soricidae, Eulipotyphla)

Abstract

Hybrid zones between chromosome races of the common shrew (Sorex araneus) provide exceptional models to study the potential role of chromosome rearrangements in the initial steps of speciation. The Novosibirsk and Tomsk races differ by a series of Robertsonian fusions with monobrachial homology. They form a narrow hybrid zone and generate hybrids with both simple (chain of three chromosomes) and complex (chain of eight or nine) synaptic configurations. Using immunolocalisation of the meiotic proteins, we examined chromosome pairing and recombination in males from the hybrid zone. Homozygotes and simple heterozygotes for Robertsonian fusions showed a low frequency of synaptic aberrations (<10%). The carriers of complex synaptic configurations showed multiple pairing abnormalities, which might lead to reduced fertility. The recombination frequency in the proximal regions of most chromosomes of all karyotypes was much lower than in the other regions. The strong suppression of recombination in the pericentromeric regions and co-segregation of race specific chromosomes involved in the long chains would be expected to lead to linkage disequilibrium between genes located there. Genic differentiation, together with the high frequency of pairing aberrations in male carriers of the long chains, might contribute to maintenance of the narrow hybrid zone.

Natural male hybrid common shrews with a very long chromosomal multivalent at meiosis appear not to be completely sterile

“…Nevertheless, the latter one and F 1 hybrids differed significantly ( p < 0.001). Our results are consistent with previously published data from the Tomsk–Novosibirsk hybrid zone (Belonogova et al, 2017).…”

“…Nonetheless, in cases of normal centromeres, the number of recombination nodules in multivalents was close to normal (approaching the expected value). Similar results have been reported about the Drnholec-Białowieża (Jadwiszczak & Banaszek, 2006) and Tomsk-Novosibirsk F 1 hybrids (Belonogova et al, 2017).…”

“…Short centromeric lines were observed in intraspecific hybrids of mole voles (Matveevsky et al, 2020), somewhat similar to the stretched centromeres of Moscow–Seliger F1 hybrids. It is worth mentioning that in Tomsk–Novosibirsk heterozygous shrews, the SC multivalent (CIX) has gaps (Belonogova et al, 2017; Karamysheva et al, 2007). Some of these gaps may have had stretched centromeres.…”

“…The use of immunocytochemical tools to examine multivalents in prophase I of meiosis makes it possible to reveal patterns of chromosome synapsis as well as organization of centromeres, recombination features, the distribution of epigenetic markers, structural features of chromatin and nuclear architecture (Berrios, 2017; Manterola et al, 2009; Matveevsky et al, 2015; Ribagorda et al, 2019). Until now, to the best of our knowledge, immunocytochemical data on meiotic divisions of heterozygous shrew males have been obtained only from two hybrid zones out of 36 known: Novosibirsk–Tomsk (chain‐of‐nine, CXI) in Siberia and Moscow–Neroosa (ring‐of‐four, RIV) in central European Russia (Belonogova et al, 2017; Karamysheva et al, 2007; Matveevsky et al, 2012). Chain‐of‐five (CV) heterozygotes from the Oxford‐Wirral hybrid zone in England have also been examined immunocytochemically, but the article does not provide images of spermatocytes with heterozygous configurations (Borodin et al, 2008).…”

Karyotypes of Manatees: New Insights into Hybrid Formation (Trichechus inunguis × Trichechus m. manatus) in the Amazon Estuary

“…We propose that these chromosomal alterations result from the formation of multivalent associations during meiosis I of specimens of the F1 generation (females). Interspecific hybrids resulting from the crossing of highly divergent species in relation to chromosomal structure, commonly present high structural heterozygosity, and formation of chains and meiotic rings [ 35 , 36 ]. Probably, F1 hybrids originated by crossing the two Trichechus species analyzed in this article fit this context, since our G-banding comparison between TIN and TMM showed that these sirenians are divergent by at least five Robertsonian rearrangement events and by the pericentric inversion of pair 1.…”