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

Asexual Reproduction Does Not Apparently Increase the Rate of Chromosomal Evolution: Karyotype Stability in Diploid and Triploid Clonal Hybrid Fish (Cobitis, Cypriniformes, Teleostei)

<div><p>Interspecific hybridization, polyploidization and transitions from sexuality to asexuality considerably affect organismal genomes. Especially the last mentioned process has been assumed to play a significant role in the initiation of chromosomal rearrangements, causing increased rates of karyotype evolution. We used cytogenetic analysis and molecular dating of cladogenetic events to compare the rate of changes of chromosome morphology and karyotype in asexually and sexually reproducing counterparts in European spined loach fish (<i>Cobitis</i>). We studied metaphases of three sexually reproducing species and their diploid and polyploid hybrid clones of different age of origin. The material includes artificial F1 hybrid strains, representatives of lineage originated in Holocene epoch, and also individuals of an oldest known age to date (roughly 0.37 MYA). Thereafter we applied GISH technique as a marker to differentiate parental chromosomal sets in hybrids. Although the sexual species accumulated remarkable chromosomal rearrangements after their speciation, we observed no differences in chromosome numbers and/or morphology among karyotypes of asexual hybrids. These hybrids possess chromosome sets originating from respective parental species with no cytogenetically detectable recombinations, suggesting their integrity even in a long term. The switch to asexual reproduction thus did not provoke any significant acceleration of the rate of chromosomal evolution in <i>Cobitis</i>. Asexual animals described in other case studies reproduce ameiotically, while <i>Cobitis</i> hybrids described here produce eggs likely through modified meiosis. Therefore, our findings indicate that the effect of asexuality on the rate of chromosomal change may be context-dependent rather than universal and related to particular type of asexual reproduction.</p></div

Ultrametric phylogenetic tree demonstrating estimated speciation times of parental species and the Hybrid clade I.

<p>Species-specific karyotypes arranged from Giemsa stained chromosomes are shown along the right side of cladogram. Confidence intervals of nodes of interest are in grey colour. TT, <i>C</i>. <i>taenia</i>; NN, <i>C</i>. <i>tanaitica</i>; EE, <i>Cobitis elongatoides</i>. Chromosomes were arranged in a decreasing size order and classified in four morphological groups: metacentric (m), submetacentric (sm), subtelocentric (st) and acrocentric (a).</p

Representative karyotypes of hybrid biotypes after GISH and/or DAPI/Giemsa staining.

<p>(A) EN hybrid metaphase with hybridization pattern of <i>Cobitis elongatoides</i> gDNA in green, <i>C</i>. <i>tanaitica</i> gDNA in red. (B) ET hybrid with <i>C</i>. <i>elongatoides</i> in red, <i>C</i>. <i>taenia</i> in green. (C) EEN hybrid with <i>C</i>. <i>elongatoides</i> in green, <i>C</i>. <i>tanaitica</i> in red. (D) EET hybrid with <i>C</i>. <i>elongatoides</i> in red, <i>C</i>. <i>taenia</i> in green. (E) ENN hybrid with <i>C</i>. <i>elongatoides</i> in red, <i>C</i>. <i>tanaitica</i> in green. (F) ETT hybrid with <i>C</i>. <i>elongatoides</i> in red, <i>C</i>. <i>taenia</i> in green. Capital letters represent haploid genome sets: E, <i>C</i>. <i>elongatoides</i>; N, <i>C</i>. <i>tanaitica</i>; T, <i>C</i>. <i>taenia</i>. Chromosomes were arranged in a decreasing size order and classified in four morphological groups: metacentric (m), submetacentric (sm), subtelocentric (st) and acrocentric (a). Probes labelled with biotin-16-dUTP were detected with FITC-streptavidin (green signals on chromosomes); probes labelled with digoxigenin-11-dUTP were detected with anti-digoxigenin-rhodamin (red signals on chromosomes). To visualize the morphology of chromosomes DAPI (A, B, C, D) or Giemsa (E, F) stained karyotype was used. Captured DAPI stained karyotypes were inverted. Bars equal 5 μm. Detail information about individuals used is provided in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0146872#pone.0146872.s004" target="_blank">S1 Table</a>.</p

Dynamic Formation of Asexual Diploid and Polyploid Lineages: Multilocus Analysis of <em>Cobitis</em> Reveals the Mechanisms Maintaining the Diversity of Clones

<div><p>Given the hybrid genomic constitutions and increased ploidy of many asexual animals, the identification of processes governing the origin and maintenance of clonal diversity provides useful information about the evolutionary consequences of interspecific hybridization, asexuality and polyploidy. In order to understand the processes driving observed diversity of biotypes and clones in the <em>Cobitis taenia</em> hybrid complex, we performed fine-scale genetic analysis of Central European hybrid zone between two sexual species using microsatellite genotyping and mtDNA sequencing. We found that the hybrid zone is populated by an assemblage of clonally (gynogenetically) reproducing di-, tri- and tetraploid hybrid lineages and that successful clones, which are able of spatial expansion, recruit from two ploidy levels, i.e. diploid and triploid. We further compared the distribution of observed estimates of clonal ages to theoretical distributions simulated under various assumptions and showed that new clones are most likely continuously recruited from ancestral populations. This suggests that the clonal diversity is maintained by dynamic equilibrium between origination and extinction of clonal lineages. On the other hand, an interclonal selection is implied by nonrandom spatial distribution of individual clones with respect to the coexisting sexual species. Importantly, there was no evidence for sexually reproducing hybrids or clonally reproducing non-hybrid forms. Together with previous successful laboratory synthesis of clonal <em>Cobitis</em> hybrids, our data thus provide the most compelling evidence that 1) the origin of asexuality is causally linked to interspecific hybridization; 2) successful establishment of clones is not restricted to one specific ploidy level and 3) the initiation of clonality and polyploidy may be dynamic and continuous in asexual complexes.</p> </div

Observed and simulated distribution of clonal age estimators.

<p>(a) Correlation between the observed values of <i>dist.bp</i> and Tomiuk and Loeschcke’s <i>I</i>; (b, d) Distributions of Hartigan’s <i>D</i> values calculated from simulated <i>dist.bp</i> histograms at every 200^th generation of the simulation. Each value was calculated from a 50∶50 mixture of sympatric and allopatric clones. Arrows indicate the observed value; frequency distributions of the observed values of <i>dist.bp,</i> and <i>I</i>, respectively (c, e).</p