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Polyploidy is considered a driving force in plant evolution and domestication. Although in the genus Arachis, several diploid species were traditionally cultivated for their seeds, only the allotetraploid peanut Arachis hypogaea became the successful, widely spread legume crop. This suggests that polyploidy has given selective advantage for domestication of peanut. Here, we study induced allotetraploid (neopolyploid) lineages obtained from crosses between the peanut's progenitor species, Arachis ipaënsis and Arachis duranensis, at earlier and later generations. We observed plant morphology, seed dimensions, and genome structure using cytogenetics (FISH and GISH) and SNP genotyping. The neopolyploid lineages show more variable fertility and seed morphology than their progenitors and cultivated peanut. They also showed sexual and somatic genome instability, evidenced by changes of number of detectable 45S rDNA sites, and extensive homoeologous recombination indicated by mosaic patterns of chromosomes and changes in dosage of SNP alleles derived from the diploid species. Genome instability was not randomly distributed across the genome: the more syntenic chromosomes, the higher homoeologous recombination. Instability levels are higher than observed on peanut lines, therefore it is likely that more unstable lines tend to perish. We conclude that early stages of the origin and domestication of the allotetraploid peanut involved two genetic bottlenecks: the first, common to most allotetraploids, is composed of the rare hybridization and polyploidization events, followed by sexual reproductive isolation from its wild diploid relatives. Here, we suggest a second bottleneck: the survival of the only very few lineages that had stronger mechanisms for limiting genomic instability.

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PREMISE OF THE STUDY: Clonal reproduction is often associated with polyploidy and is expected to influence polyploid establishment success, but the immediate effects of whole-genome duplication (WGD) on clonal reproduction in autopolyploids are unknown. METHODS: We used synthesized neopolyploids to assess the direct effects of WGD on stolon and plantlet production in the wild strawberry Fragaria vesca by (1) comparing absolute clonal investment between diploids and neotetraploids under high and low resource conditions in the greenhouse and (2) determining realized clonal plantlet establishment and genet spatial structure using artificial field populations comprising both cytotypes. KEY RESULTS: Neotetraploids produced fewer stolons and plantlets than diploids at slower weekly rates in the greenhouse when resources were high, resulting in lower total investment in clonal reproduction. Low resources led to smaller reductions in clonal biomass for neotetraploids and less pronounced differences between cytotypes. Comparisons between neotetraploids representing 13 independent WGD events and close diploid relatives revealed considerable variation in the response to polyploidization for some clonal traits. Field populations corroborated greenhouse results; neotetraploid genets were smaller than diploid genets, containing 28% fewer stolons and 46% fewer rooted plantlets. CONCLUSIONS: WGD significantly decreases the clonal output of neotetraploid F. vesca, which is likely attributable to slower whole-plant growth of the neotetraploids than the diploids. In natural populations, smaller neotetraploid genets could decrease the probability of polyploid establishment in this species. However, variation between separate neopolyploid lines emphasizes that the response of clonal investment to WGD may not be uniform across polyploid origins.

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Polyploid genomes evolve and follow a series of dynamic transfigurations along with adaptation and speciation. The initial formation of a new polyploid individual within a diploid population usually involves a triploid bridge, a two-step mechanism of cell fusions between ubiquitous (reduced) and rare (unreduced) gametes. The primary fusion event creates an intermediate triploid individual with unbalanced genome sets, a situation of genomic-shock characterized by gene expression dysregulation, high dosage sensitivity, disturbed cell divisions, and physiological and reproductive attributes drastically altered. This near-sterile neotriploid must produce (even) eupolyploids through secondary fusion events to restore genome steadiness, meiotic balance, and fertility required for the demographic establishment of a nascent lineage. Natural conditions locate several difficulties to polyploid establishment, including the production of highly unbalanced and rarely unreduced (euploid) gametes, frequency-dependent disadvantages (minority cytotype exclusion), severe fitness loss, and ecological competition with diploid parents. Persistence and adaptation of neopolyploids depend upon genetic and phenotypic novelty coupled to joint selective forces that preserve shock-induced genomic changes (subgenome homeolog partitioning) and drive meiotic (reproductive) stabilization and ecological diversification. Thus, polyploid establishment through the triploid bridge is a feasible but not ubiquitous process that requires a number of low-probability events and singular circumstances. Yet, frequencies of polyploids suggest that polyploid establishment is a pervasive process. To explain this disparity, and supported in experimental evidence, I propose that situations like hybridization and ploidy-state transitions associated to genomic shock and substantial developmental alterations can transiently activate apomixis as a mechanism to halt genomic instability and cancel factors restraining neopolyploid's sexual fertility, particularly in triploids. Apomixis -as a temporal alternative to sex- skip meiosis and syngamy, and thus can freeze genomic attributes, avoid unbalanced chromosomal segregation and increase the formation of unreduced euploid gametes, elude frequency-dependent reproductive disadvantages by parthenogenetic development of the embryo and permissive development of endosperm during seed formation, and increase the effective population size of the neopolyploid lineage favoring the formation rate of eupolyploids compared to aneuploids. The subsequent action of genome resilience mechanisms that alleviate transcriptomic shock and selection upon gene interactions might restore a stable meiosis and sexual fertility within few generations, as observed in synthetic polyploids. Alternatively, provided that resilience mechanisms fail, the neopolyploid might retain apomixis and hold genomically and transcriptionally altered states for many generations.

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The hypothesis of genetic additivity states that the effects of different alleles, or different genes, add up to produce the phenotype. When considering the F1 progeny of a cross, the hypothesis of additivity of the genetic dosages provided by the parents is tested against the mid-parent value (MPV), which is the average of parental phenotypes and represents the reference value for genetic additivity. Non-additive effects (genetic interactions) are typically measured as deviations from MPV. Recently, however, the use of MPV has been directly transposed to the study of genetic additivity in newly synthesized plant polyploids, assuming that they should as well display mid-parent expression patterns for additive traits. It is shown here that this direct transposition is incorrect. It is suggested that, in neo-polyploids, mid-parent expression has to be reconsidered in terms of reduced genetic additivity. Homeostatic mechanisms are deemed to be the obvious ones responsible for this effect. Genomes are therefore ruled by negative epistasis, and heterosis in allopolyploids is due to a decreased interaction of the parental repressive systems. It is contended that focalizing on the right perspective has relevant theoretical consequences and makes the studies of neo-polyploids very important for our understanding of how genomes work.

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