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The contribution of non-additive genetic effects to the genetic architecture of fitness and to the evolutionary potential of populations has been a topic of theoretical and empirical interest for a long time. Yet, the empirical study of these effects in natural populations remains scarce, perhaps because measuring dominance and epistasis relies heavily on experimental line crosses. In this study, we explored the contribution of dominance and epistasis in natural alpine populations of Arabidopsis thaliana for 2 fitness traits, the dry biomass and the estimated number of siliques, measured in a greenhouse. We found that, on average, crosses between inbred lines of A. thaliana led to mid-parent heterosis for dry biomass but outbreeding depression for an estimated number of siliques. While heterosis for dry biomass was due to dominance, we found that outbreeding depression for an estimated number of siliques could be attributed to the breakdown of beneficial epistatic interactions. We simulated and discussed the implication of these results for the adaptive potential of the studied populations, as well as the use of line-cross analyses to detect non-additive genetic effects., (© The Author(s) 2024. Published by Oxford University Press on behalf of the European Society of Evolutionary Biology. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.)

Whole-genome duplication is a common mutation in eukaryotes with far-reaching phenotypic effects, the resulting morphological and fitness consequences and how they affect the survival of polyploid lineages are intensively studied. Another important factor may also determine the probability of establishment and success of polyploid lineages: inbreeding depression. Inbreeding depression is expected to play an important role in the establishment of neopolyploid lineages, their capacity to colonize new environments, and in the simultaneous evolution of ploidy and other life-history traits such as self-fertilization. Both theoretically and empirically, there is no consensus on the consequences of polyploidy on inbreeding depression. In this meta-analysis, we investigated the effect of polyploidy on the evolution of inbreeding depression, by performing a meta-analysis within angiosperm species. The main results of our study are that the consequences of polyploidy on inbreeding depression are complex and depend on the time since polyploidization. We found that young polyploid lineages have a much lower amount of inbreeding depression than their diploid relatives and their established counterparts. Natural polyploid lineages are intermediate and have a higher amount of inbreeding depression than synthetic neopolyploids, and a smaller amount than diploids, suggesting that the negative effect of polyploidy on inbreeding depression decreases with time since polyploidization.

Whole-genome duplication is common in plants and is considered to have a broad range of effects on individuals' phenotypes and genomes and to be an important driver of plant adaptation and speciation. Despite their increased capacity to cope with challenging environments, polyploid lineages are generally as prone to extinction, and sometimes more prone, than their diploid progenitors. Although several explanations have been proposed to explain the short- and long-term disadvantages of polyploidy on the survival probability of populations, the consequences of whole-genome doubling on the heritable variance remain poorly studied. Whole-genome doubling can have major effects not only on the genetics, but also on the ecology and life history of the populations. Modifications of other properties of populations can reverse the effects of polyploidization per se on heritable variance. In this synthesis, I summarize the empirical and theoretical knowledge about the multifarious consequences of genome doubling on the heritable variance of quantitative traits and on the evolutionary potential of polyploid populations compared to their diploid progenitors. I propose several ways to decipher the consequences of whole-genome doubling on survival probability and to study the further consequences of shifting the ecological niche and life-history traits of a population. I also highlight some practical considerations for comparing the heritable variance of a trait among different cytotypes. Such investigations appear to be timely and necessary to understand more about the paradoxical aspects of polyploidization and to understand the evolutionary potential of polyploid lineages in a global warming context., (© 2022 Botanical Society of America.)

It is broadly assumed that polyploidy success reflects an increase in fitness associated with whole-genome duplication (WGD), due to higher tolerance to stressful conditions. Nevertheless, WGD also arises with several costs in neo-polyploid lineages, like genomic instability, or cellular mis-management. In addition to these costs, neo-polyploid individuals also face frequency dependent selection because of frequent low-fitness triploids formed by cross-ploidy pollinations when tetraploids are primarily rare in the population. Interestingly, the idea that polyploidy can be fixed by genetic drift as a neutral or deleterious mutation is currently underexplored in the literature. To test how and when polyploidy can fix in a population by chance, we built a theoretical model in which autopolyploidization occurs through the production of unreduced gametes, a trait modelled as a quantitative trait that is allowed to vary through time. We found that when tetraploid individuals are less or as fit as their diploid progenitors, fixation of polyploidy is only possible when genetic drift is stronger than natural selection. The necessity of drift for tetraploid fixation holds even when polyploidy confers a selective advantage, except for scenarios where tetraploids are much fitter than diploids. Finally, we found that self-fertilization is less beneficial for tetraploid establishment than previously thought, notably when polyploids harbour an initial decrease in fitness. Our results bring a novel, non-exclusive explanation for the unequal temporal and spatial distribution of polyploid species., (© 2022 European Society for Evolutionary Biology.)

Whole-genome duplication is a common mutation in eukaryotes with far-reaching phenotypic effects. The resulting morphological, physiological and fitness consequences and how they affect the survival probability of polyploid lineages are intensively studied, but little is known about the effect of genome doubling on the evolutionary potential of populations. Historically, it has been argued polyploids should be less able to adapt because gene duplication dilutes the effects of alleles, such that polyploids are less likely to evolve new adaptive gene complexes compared with diploids. In this paper, I investigate the short- and long-term consequences of genome doubling on the additive genetic variance of populations. To do so, I extended the classical models of quantitative traits under stabilizing selection to study the evolution of the additive variance of the trait under study after a shift from diploidy to tetraploidy. I found that, for realistic allele-dosage effects, polyploidization is associated with an initial decrease in adaptive potential. In the long term, the better masking of recessive deleterious mutations associated with polyploidy compensates for the initial decrease in additive variance. The time for the tetraploid populations to reach or exceed the additive variance of their diploid progenitors is generally lower than 200 generations. These results highlight that polyploidization per se has a negligible negative effect on the adaptive potential of populations in the short term, and a substantial positive effect in the long term., (© 2022 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.)

Premise: Whole-genome duplication (WGD) is ubiquitous in plants. Recent reviews and meta-analyses, aiming to understand how such phenotypic transition could facilitate neopolyploid establishment, demonstrated multifarious immediate effects of WGD on fitness and reproductive traits. Yet, little is known about how short-term modifications evolve through time. Such a comparison among new and established polyploid lineages is crucial to understand which effects of WGD promote or impede polyploid survival., Methods: We performed a meta-analysis to determine how WGD affects morphological, cellular, and fitness traits in autotetraploid individuals compared to their diploid progenitors. We studied how established tetraploids differed from diploids compared to neotetraploids, to further learn about the fate of WGD-associated phenotypic effects during polyploid establishment., Results: The short-term effects of WGD were an increase in size of morphological traits and cells, accompanied by a decrease in fitness and the number of cells. After establishment, the morphological effect persisted, but cellular and fitness components reverted back to the values observed in the diploid ancestors., Conclusions: Our results suggest that the larger morphology of autotetraploids is not a constraint to establishment. However, other observable effects of genome doubling disappeared with time, suggesting that solving cellular and fitness constraints are critical aspects for polyploid establishment., (© 2021 Botanical Society of America.)

Studying the consequences of hybridization on plant performance is insightful to understand the adaptive potential of populations, notably at local scales. Due to reduced effective recombination, predominantly selfing species are organized in highly homozygous multi-locus-genotypes (or lines) that accumulate genetic differentiation both among- and within-populations. This high level of homozygosity facilitates the dissection of the genetic basis of hybrid performance in highly selfing species, which gives insights into the mechanisms of reproductive isolation between lines. Here, we explored the fitness consequences of hybridization events between natural inbred lines of the predominantly selfing species Medicago truncatula, at both within- and among-populations scales. We found that hybridization has opposite effects pending on studied fitness proxies, with dry mass showing heterosis, and seed production showing outbreeding depression. Although we found significant patterns of heterosis and outbreeding depression, they did not differ significantly for within- compared to among-population crosses. Family-based analyses allowed us to determine that hybrid differentiation was mostly due to dominance and epistasis. Dominance and/or dominant epistatic interactions increased dry mass, while decreasing seed production, and recessive epistatic interactions mostly had a positive effect on both fitness proxies. Our results illustrate how genetic incompatibilities can accumulate at a very local scale among multi-locus-genotypes, and how non-additive genetic effects contribute to heterosis and outbreeding depression., (© 2021. The Author(s), under exclusive licence to The Genetics Society.)

Recurrent self-fertilization is thought to lead to reduced adaptive potential by decreasing the genetic diversity of populations, thus leading selfing lineages down an evolutionary "blind alley." Although well supported theoretically, empirical support for reduced adaptability in selfing species is limited. One limitation of classical theoretical models is that they assume pure additivity of the fitness-related traits that are under stabilizing selection, despite ample evidence that quantitative traits are subject to dominance. Here, we relax this assumption and explore the effect of dominance on a fitness-related trait under stabilizing selection for populations that differ in selfing rates. By decomposing the genetic variance into additional components specific to inbred populations, we show that dominance components can explain a substantial part of the genetic variance of inbred populations. We also show that ignoring these components leads to an upward bias in the predicted response to selection. Finally, we show that when considering the effect of dominance, the short-term evolutionary potential of populations remains comparable across the entire gradient in outcrossing rates, and genetic associations can even make selfing populations more evolvable on the longer term, reconciling theoretical, and empirical results., (© 2021 The Authors. Evolution © 2021 The Society for the Study of Evolution.)

Standing genetic variation is considered a major contributor to the adaptive potential of species. The low heritable genetic variation observed in self-fertilizing populations has led to the hypothesis that species with this mating system would be less likely to adapt. However, a non-negligible amount of cryptic genetic variation for polygenic traits, accumulated through negative linkage disequilibrium, could prove to be an important source of standing variation in self-fertilizing species. To test this hypothesis, we simulated populations under stabilizing selection subjected to an environmental change. We demonstrate that, when the mutation rate is high (but realistic), selfing populations are better able to store genetic variance than outcrossing populations through genetic associations, notably due to the reduced effective recombination rate associated with predominant selfing. Following an environmental shift, this diversity can be partially remobilized, which increases the additive variance and adaptive potential of predominantly (but not completely) selfing populations. In such conditions, despite initially lower observed genetic variance, selfing populations adapt as readily as outcrossing ones within a few generations. For low mutation rates, purifying selection impedes the storage of diversity through genetic associations, in which case, as previously predicted, the lower genetic variance of selfing populations results in lower adaptability compared to their outcrossing counterparts. The population size and the mutation rate are the main parameters to consider, as they are the best predictors of the amount of stored diversity in selfing populations. Our results and their impact on our knowledge of adaptation under high selfing rates are discussed., (© 2020 European Society For Evolutionary Biology. Journal of Evolutionary Biology © 2020 European Society For Evolutionary Biology.)

Most theoretical works predict that selfing should reduce the level of additive genetic variance available for quantitative traits within natural populations. Despite a growing number of quantitative genetic studies undertaken during the last two decades, this prediction is still not well supported empirically. To resolve this issue and confirm or reject theoretical predictions, we reviewed quantitative trait heritability estimates from natural plant populations with different rates of self-fertilization and carried out a meta-analysis. In accordance with models of polygenic traits under stabilizing selection, we found that the fraction of additive genetic variance is negatively correlated with the selfing rate. Although the mating system explains a moderate fraction of the variance, the mean reduction of narrow-sense heritability values between strictly allogamous and predominantly selfing populations is strong, around 60%. Because some nonadditive components of genetic variance become selectable under inbreeding, we determine whether self-fertilization affects the relative contribution of these components to genetic variance by comparing narrow-sense heritability estimates from outcrossing populations with broad-sense heritability estimated in autogamous populations. Results suggest that these nonadditive components of variance may restore some genetic variance in predominantly selfing populations; it remains, however, uncertain how these nonadditive components will contribute to adaptation., (© 2019 The Author(s). Evolution © 2019 The Society for the Study of Evolution.)