TY - JOUR

T1 - Reproductive Isolation Between Taxonomically Controversial Forms of the Gray Voles (Microtus, Rodentia; Arvicolinae): Cytological Mechanisms and Taxonomical Implications

AU - Bikchurina, Tatiana I.

AU - Golenishchev, Fedor N.

AU - Kizilova, Elena A.

AU - Mahmoudi, Ahmad

AU - Borodin, Pavel M.

N1 - Funding Information: Animal trapping, maintenance of the breeding colonies, collection, and analysis of breeding data were supported by the Russian Foundation for Basic Research (grant #19-04-00557a) and by the Ministry of Science and Higher Education of the Russian Federation via the Zoological Institute (grant #AAAA-A19-119032590102-7). Collection and analysis of cytological and histological data were supported by the Ministry of Science and Higher Education of the Russian Federation via the Institute of Cytology and Genetics [grants #0259-2021-0011 and # 2019-0546 (FSUS-2020-0040)]. Microscopy was carried out at the Core Facility for Microscopy of Biologic Objects, SB RAS, Novosibirsk, Russia (regulation no. 3054). The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results. Funding Information: We would like to thank Yu. M. Kowalskaya (Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences), E. A. Markova (Institute of Plant and Animal Ecology, Ural Branch, Russian Academy of Sciences), and V. M. Malygin (Moscow State University) for providing the founders of the breeding colonies (M. transcaspicus and M. arvalis ?obscurus?), V. G. Malikov and S. V. Sablina (Zoological Institute) for their help in keeping experimental animals, and V. V. Filonenko for English editing. Funding. Animal trapping, maintenance of the breeding colonies, collection, and analysis of breeding data were supported by the Russian Foundation for Basic Research (grant #19-04-00557a) and by the Ministry of Science and Higher Education of the Russian Federation via the Zoological Institute (grant #AAAA-A19-119032590102-7). Collection and analysis of cytological and histological data were supported by the Ministry of Science and Higher Education of the Russian Federation via the Institute of Cytology and Genetics [grants #0259-2021-0011 and # 2019-0546 (FSUS-2020-0040)]. Microscopy was carried out at the Core Facility for Microscopy of Biologic Objects, SB RAS, Novosibirsk, Russia (regulation no. 3054). The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results. Publisher Copyright: © Copyright © 2021 Bikchurina, Golenishchev, Kizilova, Mahmoudi and Borodin. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/5/10

Y1 - 2021/5/10

N2 - 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.

AB - 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.

KW - hybrid sterility

KW - meiotic abnormalities

KW - reproductive isolation

KW - taxonomic status

KW - voles

UR - http://www.scopus.com/inward/record.url?scp=85107080240&partnerID=8YFLogxK

U2 - 10.3389/fgene.2021.653837

DO - 10.3389/fgene.2021.653837

M3 - Article

C2 - 34040633

AN - SCOPUS:85107080240

VL - 12

JO - Frontiers in Genetics

JF - Frontiers in Genetics

SN - 1664-8021

M1 - 653837

ER -