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

Hybridization and genome duplication have played crucial roles in the evolution of many animal and plant taxa. 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 opens up unexpected evolutionary pathways. To elucidate this problem, we compared published cytogenetic and RNAseq data with exome sequences of asexual diploid and polyploid hybrids between three fish species; Cobitis elongatoides, C taenia, and C tanaitica. Clonal genomes remained generally static at chromosome-scale levels but their heterozygosity gradually deteriorated at the level of individual genes owing to allelic deletions and conversions. Interestingly, the impact of both processes varies among animals and genomic regions depending on ploidy level and the properties of affected genes. Namely, polyploids were more tolerant to deletions than diploid asexuals where conversions prevailed, and genomic restructuring events accumulated preferentially in genes characterized by high transcription levels and GC-content, strong purifying selection and specific functions like interacting with intracellular membranes. Although hybrids were phenotypically more similar to C taenia, we found that they preferentially retained C elongatoides alleles. This demonstrates that favored subgenome is not necessarily the transcriptionally dominant one. This study demonstrated that subgenomes in asexual hybrids and polyploids evolve under a complex interplay of selection and several molecular mechanisms whose efficiency depends on the organism's ploidy level, as well as functional properties and parental ancestry of the genomic region.Web of Science38125274525

speciation through asexuality in fish: postzygotic reproductive isolation may be completed in spite of fertility of hybrids

Speciation process often occurs in the face of hybridisation between forming species. Hybrid genomic constitution of many clonal organisms including fish, amphibians and reptiles also indicates tight linkage between hybridization, clonality and malfunction of sex in hybrids. To address the causal links between these phenomena, we investigated the evolution of asexuality and postzygotic reproductive isolation mechanisms (postRIMs) in the Cobitis loaches, which involves three sister species (C. taenia, C. pontica and C. tanaitica) and their distant relative, C. elongatoides. Interspecific crossings revealed that initiation of asexuality is causally linked to hybridization but does not require involvement of any particular genome. Rather, it depends on genetic distance between hybridizing parental taxa: crossings of distantly related elongatoides-taenia pair produced sterile males and fertile clonal females, while crossings of closely related species, C. pontica and C. taenia, produced fertile sexually reproducing hybrids of both sexes, with only rarely occurring clonal biotypes. Previous study of elongatoides-taenia hybrid zone together with current population genetic analysis of elongatoides-tanaitica hybrid zone demonstrated the completion of speciation: no BC or F2 hybrids have been revealed and inferred F1 hybrids were clonal. However, phylogenomic analysis revealed that gene flow between these species has been quite intensive in the past, leading to massive historical introgressions. Altogether, it appears that initiation of hybrid asexuality and the completion of speciation process through formation of postRIMs are interconnected phenomena. Both processes are linked to the genetic divergence of hybridizing taxa: initially, hybridization between little diverged species leads to recombinant and fertile hybrids allowing intensive gene flow. As the hybridizing taxa continue to diverge, clonally reproducing hybrid females and sterile males become dominant and the gene flow ceases. The speciation may therefore be completed through asexuality of hybrids The work was supported by grant no. 13-12580S provided by the Czech Science Foundation (www.gacr.cz). Further support was provided by the Academy of Sciences of the Czech Republic (www.cas.cz) by the grant no. RVO 6798590

Table S9. SNP statistics

Summary statistics for within-species and between-species genetic distances

Table S6. Oocyte analysis

For each female we indicate her biotype, origin, allozyme profile and the number of analyzed eggs