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Chromosome Asynapsis Is the Main Cause of Male Sterility in the Interspecies Hybrids of East Asian Voles (Alexandromys, Rodentia, Arvicolinae)

Closely related mammalian species often have differences in chromosome number and morphology, but there is still a debate about how these differences relate to reproductive isolation. To study the role of chromosome rearrangements in speciation, we used the gray voles in the Alexandromys genus as a...

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Autores principales: Bikchurina, Tatiana, Pavlenko, Marina, Kizilova, Elena, Rubtsova, Daria, Sheremetyeva, Irina, Kartavtseva, Irina, Torgasheva, Anna, Borodin, Pavel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10218298/
https://www.ncbi.nlm.nih.gov/pubmed/37239382
http://dx.doi.org/10.3390/genes14051022
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author Bikchurina, Tatiana
Pavlenko, Marina
Kizilova, Elena
Rubtsova, Daria
Sheremetyeva, Irina
Kartavtseva, Irina
Torgasheva, Anna
Borodin, Pavel
author_facet Bikchurina, Tatiana
Pavlenko, Marina
Kizilova, Elena
Rubtsova, Daria
Sheremetyeva, Irina
Kartavtseva, Irina
Torgasheva, Anna
Borodin, Pavel
author_sort Bikchurina, Tatiana
collection PubMed
description Closely related mammalian species often have differences in chromosome number and morphology, but there is still a debate about how these differences relate to reproductive isolation. To study the role of chromosome rearrangements in speciation, we used the gray voles in the Alexandromys genus as a model. These voles have a high level of chromosome polymorphism and substantial karyotypic divergence. We investigated testis histology and meiotic chromosome behavior in the captive-bred colonies of Alexandromys maximowiczii, Alexandromys mujanensis, two chromosome races of Alexandromys evoronensis, and their interracial and interspecies hybrids, to explore the relationship between karyotypic differences and male hybrid sterility. We found that the seminiferous tubules of the males of the parental species and the interracial hybrids, which were simple heterozygotes for one or more chromosome rearrangements, contained germ cells at all stages of spermatogenesis, indicating their potential fertility. Their meiotic cells displayed orderly chromosome synapsis and recombination. In contrast, all interspecies male hybrids, which were complex heterozygotes for a series of chromosome rearrangements, showed signs of complete sterility. Their spermatogenesis was mainly arrested at the zygotene- or pachytene-like stages due to the formation of complex multivalent chains, which caused extended chromosome asynapsis. The asynapsis led to the silencing of unsynapsed chromatin. We suggest that chromosome asynapsis is the main cause of meiotic arrest and male sterility in the interspecies hybrids of East Asian voles.
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spelling pubmed-102182982023-05-27 Chromosome Asynapsis Is the Main Cause of Male Sterility in the Interspecies Hybrids of East Asian Voles (Alexandromys, Rodentia, Arvicolinae) Bikchurina, Tatiana Pavlenko, Marina Kizilova, Elena Rubtsova, Daria Sheremetyeva, Irina Kartavtseva, Irina Torgasheva, Anna Borodin, Pavel Genes (Basel) Article Closely related mammalian species often have differences in chromosome number and morphology, but there is still a debate about how these differences relate to reproductive isolation. To study the role of chromosome rearrangements in speciation, we used the gray voles in the Alexandromys genus as a model. These voles have a high level of chromosome polymorphism and substantial karyotypic divergence. We investigated testis histology and meiotic chromosome behavior in the captive-bred colonies of Alexandromys maximowiczii, Alexandromys mujanensis, two chromosome races of Alexandromys evoronensis, and their interracial and interspecies hybrids, to explore the relationship between karyotypic differences and male hybrid sterility. We found that the seminiferous tubules of the males of the parental species and the interracial hybrids, which were simple heterozygotes for one or more chromosome rearrangements, contained germ cells at all stages of spermatogenesis, indicating their potential fertility. Their meiotic cells displayed orderly chromosome synapsis and recombination. In contrast, all interspecies male hybrids, which were complex heterozygotes for a series of chromosome rearrangements, showed signs of complete sterility. Their spermatogenesis was mainly arrested at the zygotene- or pachytene-like stages due to the formation of complex multivalent chains, which caused extended chromosome asynapsis. The asynapsis led to the silencing of unsynapsed chromatin. We suggest that chromosome asynapsis is the main cause of meiotic arrest and male sterility in the interspecies hybrids of East Asian voles. MDPI 2023-04-30 /pmc/articles/PMC10218298/ /pubmed/37239382 http://dx.doi.org/10.3390/genes14051022 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Bikchurina, Tatiana
Pavlenko, Marina
Kizilova, Elena
Rubtsova, Daria
Sheremetyeva, Irina
Kartavtseva, Irina
Torgasheva, Anna
Borodin, Pavel
Chromosome Asynapsis Is the Main Cause of Male Sterility in the Interspecies Hybrids of East Asian Voles (Alexandromys, Rodentia, Arvicolinae)
title Chromosome Asynapsis Is the Main Cause of Male Sterility in the Interspecies Hybrids of East Asian Voles (Alexandromys, Rodentia, Arvicolinae)
title_full Chromosome Asynapsis Is the Main Cause of Male Sterility in the Interspecies Hybrids of East Asian Voles (Alexandromys, Rodentia, Arvicolinae)
title_fullStr Chromosome Asynapsis Is the Main Cause of Male Sterility in the Interspecies Hybrids of East Asian Voles (Alexandromys, Rodentia, Arvicolinae)
title_full_unstemmed Chromosome Asynapsis Is the Main Cause of Male Sterility in the Interspecies Hybrids of East Asian Voles (Alexandromys, Rodentia, Arvicolinae)
title_short Chromosome Asynapsis Is the Main Cause of Male Sterility in the Interspecies Hybrids of East Asian Voles (Alexandromys, Rodentia, Arvicolinae)
title_sort chromosome asynapsis is the main cause of male sterility in the interspecies hybrids of east asian voles (alexandromys, rodentia, arvicolinae)
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10218298/
https://www.ncbi.nlm.nih.gov/pubmed/37239382
http://dx.doi.org/10.3390/genes14051022
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