Meiotic dynamics in a unique Australian marsupial provide new insights into the evolution of neo-sex chromosomes in the early stages of differentiation
Understanding the origin and fate of sex chromosomes has been one of the most intriguing questions in biology. In therian (marsupial and eutherian) mammals, most species are characterized by a heteromorphic XX female XY male sex chromosome system. It is commonly accepted that they originated from a...
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Frontiers Media S.A.
2025-03-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2025.1562403/full |
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| author | Laia Marín-Gual Laia Marín-Gual Carolyn J. Hogg J. King Chang Andrew J. Pask Marilyn B. Renfree Paul D. Waters Aurora Ruiz-Herrera Aurora Ruiz-Herrera |
| author_facet | Laia Marín-Gual Laia Marín-Gual Carolyn J. Hogg J. King Chang Andrew J. Pask Marilyn B. Renfree Paul D. Waters Aurora Ruiz-Herrera Aurora Ruiz-Herrera |
| author_sort | Laia Marín-Gual |
| collection | DOAJ |
| description | Understanding the origin and fate of sex chromosomes has been one of the most intriguing questions in biology. In therian (marsupial and eutherian) mammals, most species are characterized by a heteromorphic XX female XY male sex chromosome system. It is commonly accepted that they originated from a pair of autosomes after gaining a sex-determining function, leading to recombination suppression and subsequent Y chromosome degeneration. Unlike eutherian sex chromosomes which share a pseudo-autosomal region (PAR), the marsupial sex chromosomes are typically tiny and lack any homology. However, there is a lack of empirical evidence on biological systems that represent early stages of sex chromosome differentiation. Here, we describe the meiotic dynamics of an XY1Y2 system in the greater bilby (Macrotis lagotis: family Thylacomyidae) that resulted from a fusion between an autosome and the ancestral X chromosome. We compared the similarities and differences in the regulation of meiosis in two other Australian marsupial species with different sex chromosome systems: the tammar wallaby (Macropus eugenii: family Macropodidae) and the fat-tailed dunnart (Sminthopsis crassicaudata: family Dasyuridae), both with the ancestral XY system. We performed a cytological analysis of meiotic prophase I, including the study of chromosome synapsis, double strand break formation (as a proxy of recombination) and meiotic sex chromosome inactivation. Our results suggest that the neo-PAR in the greater bilby represents an early stage of differentiation, providing new insights into sex chromosome evolution. |
| format | Article |
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| institution | Kabale University |
| issn | 2296-634X |
| language | English |
| publishDate | 2025-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj-art-ff88c972e09c4f7f82df7b3118a917a42025-08-20T03:42:55ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2025-03-011310.3389/fcell.2025.15624031562403Meiotic dynamics in a unique Australian marsupial provide new insights into the evolution of neo-sex chromosomes in the early stages of differentiationLaia Marín-Gual0Laia Marín-Gual1Carolyn J. Hogg2J. King Chang3Andrew J. Pask4Marilyn B. Renfree5Paul D. Waters6Aurora Ruiz-Herrera7Aurora Ruiz-Herrera8Departament de Biologia Cel·lular, Fisiologia i Immunologia, Universitat Autònoma de Barcelona, Barcelona, SpainGenome Integrity and Instability Group, Institut de Biotecnologia i Biomedicina, Universitat Autònoma de Barcelona, Barcelona, SpainSchool of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, AustraliaSchool of Biotechnology and Biomolecular Sciences, Faculty of Science, The University of New South Wales, Sydney, NSW, AustraliaSchool of BioSciences, The University of Melbourne, Parkville, VIC, AustraliaSchool of BioSciences, The University of Melbourne, Parkville, VIC, AustraliaSchool of Biotechnology and Biomolecular Sciences, Faculty of Science, The University of New South Wales, Sydney, NSW, AustraliaDepartament de Biologia Cel·lular, Fisiologia i Immunologia, Universitat Autònoma de Barcelona, Barcelona, SpainGenome Integrity and Instability Group, Institut de Biotecnologia i Biomedicina, Universitat Autònoma de Barcelona, Barcelona, SpainUnderstanding the origin and fate of sex chromosomes has been one of the most intriguing questions in biology. In therian (marsupial and eutherian) mammals, most species are characterized by a heteromorphic XX female XY male sex chromosome system. It is commonly accepted that they originated from a pair of autosomes after gaining a sex-determining function, leading to recombination suppression and subsequent Y chromosome degeneration. Unlike eutherian sex chromosomes which share a pseudo-autosomal region (PAR), the marsupial sex chromosomes are typically tiny and lack any homology. However, there is a lack of empirical evidence on biological systems that represent early stages of sex chromosome differentiation. Here, we describe the meiotic dynamics of an XY1Y2 system in the greater bilby (Macrotis lagotis: family Thylacomyidae) that resulted from a fusion between an autosome and the ancestral X chromosome. We compared the similarities and differences in the regulation of meiosis in two other Australian marsupial species with different sex chromosome systems: the tammar wallaby (Macropus eugenii: family Macropodidae) and the fat-tailed dunnart (Sminthopsis crassicaudata: family Dasyuridae), both with the ancestral XY system. We performed a cytological analysis of meiotic prophase I, including the study of chromosome synapsis, double strand break formation (as a proxy of recombination) and meiotic sex chromosome inactivation. Our results suggest that the neo-PAR in the greater bilby represents an early stage of differentiation, providing new insights into sex chromosome evolution.https://www.frontiersin.org/articles/10.3389/fcell.2025.1562403/fullmarsupialsmeiosisneo sex-chromosomesmeiotic sex chromosome inactivationdouble strand breaksrecombination |
| spellingShingle | Laia Marín-Gual Laia Marín-Gual Carolyn J. Hogg J. King Chang Andrew J. Pask Marilyn B. Renfree Paul D. Waters Aurora Ruiz-Herrera Aurora Ruiz-Herrera Meiotic dynamics in a unique Australian marsupial provide new insights into the evolution of neo-sex chromosomes in the early stages of differentiation Frontiers in Cell and Developmental Biology marsupials meiosis neo sex-chromosomes meiotic sex chromosome inactivation double strand breaks recombination |
| title | Meiotic dynamics in a unique Australian marsupial provide new insights into the evolution of neo-sex chromosomes in the early stages of differentiation |
| title_full | Meiotic dynamics in a unique Australian marsupial provide new insights into the evolution of neo-sex chromosomes in the early stages of differentiation |
| title_fullStr | Meiotic dynamics in a unique Australian marsupial provide new insights into the evolution of neo-sex chromosomes in the early stages of differentiation |
| title_full_unstemmed | Meiotic dynamics in a unique Australian marsupial provide new insights into the evolution of neo-sex chromosomes in the early stages of differentiation |
| title_short | Meiotic dynamics in a unique Australian marsupial provide new insights into the evolution of neo-sex chromosomes in the early stages of differentiation |
| title_sort | meiotic dynamics in a unique australian marsupial provide new insights into the evolution of neo sex chromosomes in the early stages of differentiation |
| topic | marsupials meiosis neo sex-chromosomes meiotic sex chromosome inactivation double strand breaks recombination |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2025.1562403/full |
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