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Meiotic Behavior of Achiasmate Sex Chromosomes in the African Pygmy Mouse Mus mattheyi Offers New Insights into the Evolution of Sex Chromosome Pairing and Segregation in Mammals

1
Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid, 28049 Madrid, Spain
2
Institut des Sciences de l’Evolution, ISEM UMR 5554 (CNRS/Université Montpellier/IRD/EPHE), 34090 Montpellier, France
*
Author to whom correspondence should be addressed.
Academic Editor: Juan Del Coso
Genes 2021, 12(9), 1434; https://doi.org/10.3390/genes12091434
Received: 24 August 2021 / Revised: 13 September 2021 / Accepted: 15 September 2021 / Published: 17 September 2021
(This article belongs to the Special Issue Sex Chromosome Evolution and Meiosis)
X and Y chromosomes in mammals are different in size and gene content due to an evolutionary process of differentiation and degeneration of the Y chromosome. Nevertheless, these chromosomes usually share a small region of homology, the pseudoautosomal region (PAR), which allows them to perform a partial synapsis and undergo reciprocal recombination during meiosis, which ensures their segregation. However, in some mammalian species the PAR has been lost, which challenges the pairing and segregation of sex chromosomes in meiosis. The African pygmy mouse Mus mattheyi shows completely differentiated sex chromosomes, representing an uncommon evolutionary situation among mouse species. We have performed a detailed analysis of the location of proteins involved in synaptonemal complex assembly (SYCP3), recombination (RPA, RAD51 and MLH1) and sex chromosome inactivation (γH2AX) in this species. We found that neither synapsis nor chiasmata are found between sex chromosomes and their pairing is notably delayed compared to autosomes. Interestingly, the Y chromosome only incorporates RPA and RAD51 in a reduced fraction of spermatocytes, indicating a particular DNA repair dynamic on this chromosome. The analysis of segregation revealed that sex chromosomes are associated until metaphase-I just by a chromatin contact. Unexpectedly, both sex chromosomes remain labelled with γH2AX during first meiotic division. This chromatin contact is probably enough to maintain sex chromosome association up to anaphase-I and, therefore, could be relevant to ensure their reductional segregation. The results presented suggest that the regulation of both DNA repair and epigenetic modifications in the sex chromosomes can have a great impact on the divergence of sex chromosomes and their proper transmission, widening our understanding on the relationship between meiosis and the evolution of sex chromosomes in mammals. View Full-Text
Keywords: sex chromosomes; meiosis; evolution; pygmy mouse; Mus mattheyi sex chromosomes; meiosis; evolution; pygmy mouse; Mus mattheyi
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MDPI and ACS Style

Gil-Fernández, A.; Ribagorda, M.; Martín-Ruiz, M.; López-Jiménez, P.; Laguna, T.; Gómez, R.; Parra, M.T.; Viera, A.; Veyrunes, F.; Page, J. Meiotic Behavior of Achiasmate Sex Chromosomes in the African Pygmy Mouse Mus mattheyi Offers New Insights into the Evolution of Sex Chromosome Pairing and Segregation in Mammals. Genes 2021, 12, 1434. https://doi.org/10.3390/genes12091434

AMA Style

Gil-Fernández A, Ribagorda M, Martín-Ruiz M, López-Jiménez P, Laguna T, Gómez R, Parra MT, Viera A, Veyrunes F, Page J. Meiotic Behavior of Achiasmate Sex Chromosomes in the African Pygmy Mouse Mus mattheyi Offers New Insights into the Evolution of Sex Chromosome Pairing and Segregation in Mammals. Genes. 2021; 12(9):1434. https://doi.org/10.3390/genes12091434

Chicago/Turabian Style

Gil-Fernández, Ana, Marta Ribagorda, Marta Martín-Ruiz, Pablo López-Jiménez, Tamara Laguna, Rocío Gómez, María T. Parra, Alberto Viera, Frederic Veyrunes, and Jesús Page. 2021. "Meiotic Behavior of Achiasmate Sex Chromosomes in the African Pygmy Mouse Mus mattheyi Offers New Insights into the Evolution of Sex Chromosome Pairing and Segregation in Mammals" Genes 12, no. 9: 1434. https://doi.org/10.3390/genes12091434

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