Genetic degeneration of old and young Y chromosomes in the flowering plant Rumex hastatulus.
Heteromorphic sex chromosomes have originated independently in many species, and a common feature of their evolution is the degeneration of the Y chromosome, characterized by a loss of gene content and function. Despite being of broad significance to our understanding of sex chromosome evolution, the genetic changes that occur during the early stages of Y-chromosome degeneration are poorly understood, especially in plants. Here, we investigate sex chromosome evolution in the dioecious plant Rumex hastatulus, in which X and Y chromosomes have evolved relatively recently and occur in two distinct systems: an ancestral XX/XY system and a derived XX/XY1Y2 system. This polymorphism provides a unique opportunity to investigate the effect of sex chromosome age on patterns of divergence and gene degeneration within a species. Despite recent suppression of recombination and low X-Y divergence in both systems, we find evidence that Y-linked genes have started to undergo gene loss, causing ∼ 28% and ∼ 8% hemizygosity of the ancestral and derived X chromosomes, respectively. Furthermore, genes remaining on Y chromosomes have accumulated more amino acid replacements, contain more unpreferred changes in codon use, and exhibit significantly reduced gene expression compared with their X-linked alleles, with the magnitude of these effects being greatest for older sex-linked genes. Our results provide evidence for reduced selection efficiency and ongoing Y-chromosome degeneration in a flowering plant, and indicate that Y degeneration can occur soon after recombination suppression between sex chromosomes.
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2 josh.hough@utoronto.ca.
Josh
J
Hough
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2.
Jesse D
JD
Hollister
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2.
Wei
W
Wang
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2.
Spencer C H
SC
Barrett
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2.
Stephen I
SI
Wright
D019943:Amino Acid Substitution / Q000235:genetics; D043171:Chromosomal Instability / Q000235:genetics*; D032461:Chromosomes, Plant / Q000235:genetics*; D019143:Evolution, Molecular; D008957:Models, Genetic; D010802:Phylogeny; D020641:Polymorphism, Single Nucleotide / Q000235:genetics; D031804:Rumex / Q000235:genetics*; D012641:Selection, Genetic; D012730:Sex Chromosomes / Q000235:genetics*; D059467:Transcriptome
dioecy; molecular evolution; sex linkage