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Evolution of the Degenerated Y-Chromosome of the Swamp Guppy, Micropoecilia picta

The conspicuous colour sexual dimorphism of guppies has made them paradigmatic study objects for sex-linked traits and sex chromosome evolution. Both the X- and Y-chromosomes of the common guppy (Poecilia reticulata) are genetically active and homomorphic, with a large homologous part and a small se...

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Autores principales: Nanda, Indrajit, Schories, Susanne, Simeonov, Ivan, Adolfi, Mateus Contar, Du, Kang, Steinlein, Claus, Alsheimer, Manfred, Haaf, Thomas, Schartl, Manfred
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8997885/
https://www.ncbi.nlm.nih.gov/pubmed/35406682
http://dx.doi.org/10.3390/cells11071118
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author Nanda, Indrajit
Schories, Susanne
Simeonov, Ivan
Adolfi, Mateus Contar
Du, Kang
Steinlein, Claus
Alsheimer, Manfred
Haaf, Thomas
Schartl, Manfred
author_facet Nanda, Indrajit
Schories, Susanne
Simeonov, Ivan
Adolfi, Mateus Contar
Du, Kang
Steinlein, Claus
Alsheimer, Manfred
Haaf, Thomas
Schartl, Manfred
author_sort Nanda, Indrajit
collection PubMed
description The conspicuous colour sexual dimorphism of guppies has made them paradigmatic study objects for sex-linked traits and sex chromosome evolution. Both the X- and Y-chromosomes of the common guppy (Poecilia reticulata) are genetically active and homomorphic, with a large homologous part and a small sex specific region. This feature is considered to emulate the initial stage of sex chromosome evolution. A similar situation has been documented in the related Endler’s and Oropuche guppies (P. wingei, P. obscura) indicating a common origin of the Y in this group. A recent molecular study in the swamp guppy (Micropoecilia. picta) reported a low SNP density on the Y, indicating Y-chromosome deterioration. We performed a series of cytological studies on M. picta to show that the Y-chromosome is quite small compared to the X and has accumulated a high content of heterochromatin. Furthermore, the Y-chromosome stands out in displaying CpG clusters around the centromeric region. These cytological findings evidently illustrate that the Y-chromosome in M. picta is indeed highly degenerated. Immunostaining for SYCP3 and MLH1 in pachytene meiocytes revealed that a substantial part of the Y remains associated with the X. A specific MLH1 hotspot site was persistently marked at the distal end of the associated XY structure. These results unveil a landmark of a recombining pseudoautosomal region on the otherwise strongly degenerated Y chromosome of M. picta. Hormone treatments of females revealed that, unexpectedly, no sexually antagonistic color gene is Y-linked in M. picta. All these differences to the Poecilia group of guppies indicate that the trajectories associated with the evolution of sex chromosomes are not in parallel.
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spelling pubmed-89978852022-04-12 Evolution of the Degenerated Y-Chromosome of the Swamp Guppy, Micropoecilia picta Nanda, Indrajit Schories, Susanne Simeonov, Ivan Adolfi, Mateus Contar Du, Kang Steinlein, Claus Alsheimer, Manfred Haaf, Thomas Schartl, Manfred Cells Article The conspicuous colour sexual dimorphism of guppies has made them paradigmatic study objects for sex-linked traits and sex chromosome evolution. Both the X- and Y-chromosomes of the common guppy (Poecilia reticulata) are genetically active and homomorphic, with a large homologous part and a small sex specific region. This feature is considered to emulate the initial stage of sex chromosome evolution. A similar situation has been documented in the related Endler’s and Oropuche guppies (P. wingei, P. obscura) indicating a common origin of the Y in this group. A recent molecular study in the swamp guppy (Micropoecilia. picta) reported a low SNP density on the Y, indicating Y-chromosome deterioration. We performed a series of cytological studies on M. picta to show that the Y-chromosome is quite small compared to the X and has accumulated a high content of heterochromatin. Furthermore, the Y-chromosome stands out in displaying CpG clusters around the centromeric region. These cytological findings evidently illustrate that the Y-chromosome in M. picta is indeed highly degenerated. Immunostaining for SYCP3 and MLH1 in pachytene meiocytes revealed that a substantial part of the Y remains associated with the X. A specific MLH1 hotspot site was persistently marked at the distal end of the associated XY structure. These results unveil a landmark of a recombining pseudoautosomal region on the otherwise strongly degenerated Y chromosome of M. picta. Hormone treatments of females revealed that, unexpectedly, no sexually antagonistic color gene is Y-linked in M. picta. All these differences to the Poecilia group of guppies indicate that the trajectories associated with the evolution of sex chromosomes are not in parallel. MDPI 2022-03-25 /pmc/articles/PMC8997885/ /pubmed/35406682 http://dx.doi.org/10.3390/cells11071118 Text en © 2022 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
Nanda, Indrajit
Schories, Susanne
Simeonov, Ivan
Adolfi, Mateus Contar
Du, Kang
Steinlein, Claus
Alsheimer, Manfred
Haaf, Thomas
Schartl, Manfred
Evolution of the Degenerated Y-Chromosome of the Swamp Guppy, Micropoecilia picta
title Evolution of the Degenerated Y-Chromosome of the Swamp Guppy, Micropoecilia picta
title_full Evolution of the Degenerated Y-Chromosome of the Swamp Guppy, Micropoecilia picta
title_fullStr Evolution of the Degenerated Y-Chromosome of the Swamp Guppy, Micropoecilia picta
title_full_unstemmed Evolution of the Degenerated Y-Chromosome of the Swamp Guppy, Micropoecilia picta
title_short Evolution of the Degenerated Y-Chromosome of the Swamp Guppy, Micropoecilia picta
title_sort evolution of the degenerated y-chromosome of the swamp guppy, micropoecilia picta
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8997885/
https://www.ncbi.nlm.nih.gov/pubmed/35406682
http://dx.doi.org/10.3390/cells11071118
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