Purifying and Positive Selection Influence Patterns of Gene Loss and Gene Expression in the Evolution of a Plant Sex Chromosome System.
Sex chromosomes are unique regions of the genome, with a host of properties that distinguish them from autosomes and from each other. Although there is extensive theory describing sex chromosome formation and subsequent degeneration of the Y chromosome, the relative importance of processes governing degeneration is poorly understood. In particular, it is not known whether degeneration occurs solely as a direct result of inefficient selection due to loss of recombination, or whether adaptive gene silencing on the Y chromosome results in most degeneration occurring neutrally. We used comparative transcriptome data from two related annual plants with highly heteromorphic sex chromosomes, Rumex rothschildianus and Rumex hastatulus, to investigate the patterns and processes underlying Y chromosome degeneration. The rate of degeneration varied greatly between the two species. In R. rothschildianus, we infer widespread gene loss, higher than previously reported for any plant. Gene loss was not random: genes with lower constraint and those not expressed during the haploid phase were more likely to be lost. There was indirect evidence of adaptive evolution on the Y chromosome from the over-expression of Y alleles in certain genes with sex-biased gene expression. There was no complete dosage compensation, but there was evidence for targeted dosage compensation occurring in more selectively constrained genes. Overall, our results are consistent with selective interference playing the dominant role in the degeneration of the Y chromosome, rather than adaptive gene silencing.
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada.
Daisy
D
Crowson
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada.
Spencer C H
SCH
Barrett
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada.
Stephen I
SI
Wright
D000483:Alleles; D005075:Biological Evolution; D032461:Chromosomes, Plant / Q000235:genetics*; D004303:Dosage Compensation, Genetic; D019143:Evolution, Molecular; D017353:Gene Deletion; D018745:Genome, Plant / Q000235:genetics; D010944:Plants / Q000235:genetics; D031804:Rumex / Q000235:genetics*; D012730:Sex Chromosomes / Q000235:genetics*; D059467:Transcriptome / Q000235:genetics
Rumex; Y chromosome degeneration; dosage compensation; gene loss; selective interference; sex-biased gene expression