Kotusz, J. | bioRxiv Science

bioRxiv2020

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

AbstractHybridization 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 orthologs 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.

evolutionary biology↗

bioRxiv2019

Parthenogenesis as a solution to hybrid sterility: the mechanistic basis of meiotic distortions in clonal and sterile hybrids

Formation of species generally occurs in a continuum from potentially intermixing populations to independent entities isolated from other species by pre- and postzygotic barriers. Especially the establishment of hybrid sterility (HS) is a hallmark of speciation, which usually emerges at different rates between hybrid sexes. However, although HS is frequently observed, the underlying molecular mechanisms remain poorly understood. Here we report that speciation proceeds through a previously unnoticed stage at which gene flow is completely interrupted on side of both hybrids sexes, although only male hybrids are sterile, while female fertility is rescued due to a particular gametogenetic deviation leading to the formation of clonal gametes. Specifically, analysis of gametogenetic pathways in hybrids between fish species Cobitis elongatoides and C. taenia revealed that male HS resulted from extensive asynapses and crossover reduction among elongatoides-taenia chromosomal pairs followed by apoptosis. By contrast, hybrid females exhibited premeiotic genome endoreplication which ensured proper formation of bivalents between identical chromosomal copies. This deviation ultimately restored fertility in females but since it simultaneously leads to the production of unreduced clonal gametes, it restricts interspecific gene flow thereby directly contributing to speciation. In conclusion, our data demonstrate that the emergence of asexuality may remedy HS in a sex-specific manner and is intermingled with the speciation process. Although gametogenetic mechanisms employed by asexual animals and plants have rarely been scrutinized, available evidence suggests that premeiotic endoreplication is relatively widespread. This suggests that observed link between HS and clonality may have general validity in taxa able of asexual reproduction.\n\nAuthors summarySpecies are fundamental evolutionary units that presumably evolve in a continuum from potentially intermixing populations to independent entities isolated from other species by pre- and postzygotic barriers. Especially the establishment of hybrid sterility (HS) is a hallmark of speciation, which usually emerges at different rates between hybrid sexes. However, although HS is frequently observed, the underlying molecular mechanisms remain poorly understood. Here we report the existence of a previously unnoticed stage of speciation at which gene flow is completely interrupted, although only male hybrids are sterile, while female fertility is rescued due to a particular gametogenetic deviation leading to formation of clonal gametes. Specifically, HS resulted from extensive asynapses in male gonads, but in females the hybridization provoked premeiotic endoreplication which rescued chromosome pairing and fertility. Simultaneously, this meiotic deviation caused clonal transmission of maternal genome, thereby effectively restricting the interspeficic gene flow. Our results emphasize that emergence of clonality is a type of hybrid incompatibility that is intermingled with the formation of biological species and may remedy hybrid sterility in a sex-specific manner.

evolutionary biology↗