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Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiati...

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Autores principales: Darolti, Iulia, Wright, Alison E., Sandkam, Benjamin A., Morris, Jake, Bloch, Natasha I., Farré, Marta, Fuller, Rebecca C., Bourne, Godfrey R., Larkin, Denis M., Breden, Felix, Mank, Judith E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6754558/
https://www.ncbi.nlm.nih.gov/pubmed/31484763
http://dx.doi.org/10.1073/pnas.1905298116
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author Darolti, Iulia
Wright, Alison E.
Sandkam, Benjamin A.
Morris, Jake
Bloch, Natasha I.
Farré, Marta
Fuller, Rebecca C.
Bourne, Godfrey R.
Larkin, Denis M.
Breden, Felix
Mank, Judith E.
author_facet Darolti, Iulia
Wright, Alison E.
Sandkam, Benjamin A.
Morris, Jake
Bloch, Natasha I.
Farré, Marta
Fuller, Rebecca C.
Bourne, Godfrey R.
Larkin, Denis M.
Breden, Felix
Mank, Judith E.
author_sort Darolti, Iulia
collection PubMed
description Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged roughly 20 million years ago. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.
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spelling pubmed-67545582019-10-01 Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers Darolti, Iulia Wright, Alison E. Sandkam, Benjamin A. Morris, Jake Bloch, Natasha I. Farré, Marta Fuller, Rebecca C. Bourne, Godfrey R. Larkin, Denis M. Breden, Felix Mank, Judith E. Proc Natl Acad Sci U S A Biological Sciences Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged roughly 20 million years ago. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation. National Academy of Sciences 2019-09-17 2019-09-04 /pmc/articles/PMC6754558/ /pubmed/31484763 http://dx.doi.org/10.1073/pnas.1905298116 Text en Copyright © 2019 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Darolti, Iulia
Wright, Alison E.
Sandkam, Benjamin A.
Morris, Jake
Bloch, Natasha I.
Farré, Marta
Fuller, Rebecca C.
Bourne, Godfrey R.
Larkin, Denis M.
Breden, Felix
Mank, Judith E.
Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers
title Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers
title_full Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers
title_fullStr Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers
title_full_unstemmed Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers
title_short Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers
title_sort extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6754558/
https://www.ncbi.nlm.nih.gov/pubmed/31484763
http://dx.doi.org/10.1073/pnas.1905298116
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