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Proc Natl Acad Sci U S A. 2019 Sep 17;116(38):19031-19036. doi: 10.1073/pnas.1905298116. Epub 2019 Sep 4.

Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers.

Author information

1
Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom; iulia.darolti.15@ucl.ac.uk.
2
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, United Kingdom.
3
Department of Zoology, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
4
Department of Genetics, Evolution and Environment, University College London, London WC1E 6BT, United Kingdom.
5
Department of Biomedical Engineering, University of Los Andes, Bogotá 111711, Colombia.
6
School of Biosciences, University of Kent, Canterbury CT2 7NJ, United Kingdom.
7
Department of Animal Biology, University of Illinois at Urbana-Champaign, Urbana, IL 61801.
8
Department of Biology, University of Missouri-St. Louis, St. Louis, MO 63105.
9
Department of Comparative Biomedical Sciences, Royal Veterinary College, London NW1 0TU, United Kingdom.
10
Department of Biological Science, Simon Fraser University, Burnaby, BC V5A 1S6, Canada.
11
Department of Organismal Biology, Uppsala University, Uppsala 752 36, Sweden.

Abstract

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.

KEYWORDS:

Y degeneration; dosage compensation; poeciliids; recombination

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