Genome fractionation and loss of heterozygosity in hybrids and polyploids: mechanisms, consequences for selection, and link to gene function

Abstract: Hybridization and genome duplication have played crucial roles in the evolution of many animal and plant taxa. During their evolution, the subgenomes of parental species undergo considerable changes in hybrids and polyploids, which often selectively eliminate segments of one subgenome. However, the mechanisms underlying these changes are not well understood, particularly when the hybridization is linked with asexual reproduction that may enforce specific evolutionary pathways. We studied the genome evolution in asexual diploid and polyploid hybrids between fish from the genus Cobitis . Comparing exome sequencing with published cytogenetic and RNAseq data revealed that clonal genomes remain static on chromosome-scale levels but undergo considerable small-scale restructurations owing to two major processes; hemizygous deletions and gene conversions. Interestingly, polyploids were much more tolerant to accumulating deletions than diploid asexuals where gene conversions prevailed. The genomic restructurations accumulated preferentially in genes characterized by high transcription levels, relatively strong purifying selection and some specific functions such as interacting with intracellular membranes. The likelihood of an ortholog’s retention or loss correlated with its parental-species ancestry, GC content, and expression. Furthermore, all hybrids showed a strong bias towards the retention of one parental subgenome. Contrary to expectations, however, the preferentially retained subgenome was not transcriptionally dominant as all hybrids were phenotypically more similar to the other parent. The present study demonstrated that the fate of subgenomes in asexual hybrids and polyploids depends on the complex interplay of selection and several molecular mechanisms whose impact depends on ploidy, sequence composition, gene expression as well as parental ancestry.