Abstract
The formation of hybrid sterility is an important stage of speciation. The voles of the genus Microtus, which is the most speciose genus of rodents, provide a good model for studying the cytological mechanisms of hybrid sterility. The voles of the “mystacinus” group of the subgenus Microtus (2n = 54) comprising several recently diverged forms with unclear taxonomic status are especially interesting. To resolve the taxonomic status of Microtus mystacinus and Microtus kermanensis, we crossed both with Microtus rossiaemeridionalis, and M. kermanensis alone with Microtus arvalis “obscurus” and M. transcaspicus and examined the reproductive performance of their F1 hybrids. All interspecies male hybrids were sterile. Female M. kermanensis × M. arvalis and M. kermanensis × M. transcaspicus hybrids were sterile as well. Therefore, M. mystacinus, M. kermanensis, and M. rossiaemeridionalis could be considered valid species. To gain an insight into the cytological mechanisms of male hybrid sterility, we carried out a histological analysis of spermatogenesis and a cytological analysis of chromosome synapsis, recombination, and epigenetic chromatin modifications in the germ cells of the hybrids using immunolocalization of key meiotic proteins. The hybrids showed wide variation in the onset of spermatogenesis arrest stage, from mature (although abnormal) spermatozoa to spermatogonia only. Chromosome asynapsis was apparently the main cause of meiotic arrest. The degree of asynapsis varied widely across cells, individuals, and the crosses—from partial asynapsis of several small bivalents to complete asynapsis of all chromosomes. The asynapsis was accompanied by a delayed repair of DNA double-strand breaks marked by RAD51 antibodies and silencing of unpaired chromatin marked by γH2A.X antibodies. Overall, the severity of disturbances in spermatogenesis in general and in chromosome synapsis in particular increased in the hybrids with an increase in the phylogenetic distance between their parental species.
Highlights
The concept of biological species lays stress on reproductive isolation as the main discriminant of species (Mayr, 1970; Coyne and Orr, 2004)
To clarify the taxonomic status of the “mystacinus” group (M. mystacinus, M. kermanensis, and M. rossiaemeridionalis) and their relation to the other species of the subgenus Microtus (M. arvalis and M. transcaspicus), which differ from each other both genetically and chromosomally, we examined the reproductive performance of their male and female hybrids
In order to estimate the fertility of the hybrids, we crossed them with the parental species
Summary
The concept of biological species lays stress on reproductive isolation as the main discriminant of species (Mayr, 1970; Coyne and Orr, 2004). Tests for reproductive isolation combined with detailed molecular genetic and cytogenetic analyses have been successfully applied to resolve taxonomical issues with the gray voles Microtus (Rodentia; Arvicolinae), one of the most speciose rodent genera This integrated approach made it possible to establish the species status of two sibling forms Microtus arvalis and Microtus rossiaemeridionalis and to confirm the species status of some controversial forms, such as M. ilaeus and M. transcaspicus (Meyer et al, 1985, 1996; Malygin and Sablina, 1994; Meyer, 1994; Torgasheva and Borodin, 2016). According to a recent revision (Shenbrot and Krasnov, 2005; Pavlinov and Lissovsky, 2012; Golenishchev et al, 2019), the subgenus Microtus comprises six nominal forms: M. arvalis (Pallas, 1778) (with two karyoforms, “arvalis” and “obscurus”), M. rossiaemeridionalis (Ognev, 1924), M. ilaeus (Thomas, 1912), M. transcaspicus (Satunin, 1905), Microtus kermanensis (Roguin, 1988), and Microtus mystacinus (De Filippi, 1865) The former two sibling species occupy vast areas in Eurasia, cohabitating in most of them.
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