TY - JOUR

T1 - Chromosome Asynapsis Is the Main Cause of Male Sterility in the Interspecies Hybrids of East Asian Voles (Alexandromys, Rodentia, Arvicolinae)

AU - Bikchurina, Tatiana

AU - Pavlenko, Marina

AU - Kizilova, Elena

AU - Rubtsova, Daria

AU - Sheremetyeva, Irina

AU - Kartavtseva, Irina

AU - Torgasheva, Anna

AU - Borodin, Pavel

N1 - Funding: The research was funded by the Ministry of Science and Higher Education of the Russian Federation grant numbers 2019-0546 (FSUS-2020-0040) and FWNR-2022-0015 and the Ministry of Science and Higher Education of the Russian Federation for the Federal Scientific Center of the East Asia Terrestrial Biodiversity (theme No. 121031500274-4).

PY - 2023/4/30

Y1 - 2023/4/30

N2 - 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.

AB - 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.

KW - Animals

KW - Male

KW - Arvicolinae/genetics

KW - Chromosomes/genetics

KW - Infertility, Male/genetics

UR - https://www.scopus.com/record/display.uri?eid=2-s2.0-85160381313&origin=inward&txGid=64030143b1970bf1acc8132663d658ab

U2 - 10.3390/genes14051022

DO - 10.3390/genes14051022

M3 - Article

C2 - 37239382

VL - 14

JO - Genes

JF - Genes

SN - 2073-4425

IS - 5

M1 - 1022

ER -