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Inbreeding depression resulting from partially recessive deleterious alleles is thought to be the main genetic factor preventing self-fertilizing mutants from spreading in outcrossing hermaphroditic populations. However, deleterious alleles may also generate an advantage to selfers in terms of more efficient purging, while the effects of epistasis among those alleles on inbreeding depression and mating system evolution remain little explored. In this article, we use a general model of selection to disentangle the effects of different forms of epistasis (additive-by-additive, additive-by-dominance, and dominance-by-dominance) on inbreeding depression and on the strength of selection for selfing. Models with fixed epistasis across loci, and models of stabilizing selection acting on quantitative traits (generating distributions of epistasis) are considered as special cases. Besides its effects on inbreeding depression, epistasis may increase the purging advantage associated with selfing (when it is negative on average), while the variance in epistasis favors selfing through the generation of linkage disequilibria that increase mean fitness. Approximations for the strengths of these effects are derived, and compared with individual-based simulation results.

Seed banking (or dormancy) is a widespread bet-hedging strategy, generating a form of population overlap, which decreases the magnitude of genetic drift. The methodological complexity of integrating this trait implies it is ignored when developing tools to detect selective sweeps. But, as dormancy lengthens the ancestral recombination graph (ARG), increasing times to fixation, it can change the genomic signatures of selection. To detect genes under positive selection in seed banking species it is important to 1) determine whether the efficacy of selection is affected, and 2) predict the patterns of nucleotide diversity at and around positively selected alleles. We present the first tree sequence-based simulation program integrating a weak seed bank to examine the dynamics and genomic footprints of beneficial alleles in a finite population. We find that seed banking does not affect the probability of fixation and confirm expectations of increased times to fixation. We also confirm earlier findings that, for strong selection, the times to fixation are not scaled by the inbreeding effective population size in the presence of seed banks, but are shorter than would be expected. As seed banking increases the effective recombination rate, footprints of sweeps appear narrower around the selected sites and due to the scaling of the ARG are detectable for longer periods of time. The developed simulation tool can be used to predict the footprints of selection and draw statistical inference of past evolutionary events in plants, invertebrates, or fungi with seed banks.

Several methods based on the sequentially Markovian coalescent (SMC) make use of full genome sequence data from samples to infer population demographic history including past changes in population size, admixture, migration events and population structure. More recently, the original theoretical framework has been extended to allow the simultaneous estimation of population size changes along with other life history traits such as selfing or seed banking. The latter developments enhance the applicability of SMC methods to nonmodel species. Although convergence proofs have been given using simulated data in a few specific cases, an in-depth investigation of the limitations of SMC methods is lacking. In order to explore such limits, we first develop a tool inferring the best case convergence of SMC methods assuming the true underlying coalescent genealogies are known. This tool can be used to quantify the amount and type of information that can be confidently retrieved from given data sets prior to the analysis of the real data. Second, we assess the inference accuracy when the assumptions of SMC approaches are violated due to departures from the model, namely the presence of transposable elements, variable recombination and mutation rates along the sequence, and SNP calling errors. Third, we deliver a new interpretation of SMC methods by highlighting the importance of the transition matrix, which we argue can be used as a set of summary statistics in other statistical inference methods, uncoupling the SMC from hidden Markov models (HMMs). We finally offer recommendations to better apply SMC methods and build adequate data sets under budget constraints.

The mating system of a species is expected to have important effects on its genetic diversity. In this article, we explore the effects of partial selfing on the equilibrium genetic variance Vg , mutation load L, and inbreeding depression δ under stabilizing selection acting on a arbitrary number n of quantitative traits coded by biallelic loci with additive effects. When the U/n ratio is low (where U is the total haploid mutation rate on selected traits) and effective recombination rates are sufficiently high, genetic associations between loci are negligible and the genetic variance, mutation load, and inbreeding depression are well predicted by approximations based on single-locus models. For higher values of U/n and/or lower effective recombination, moderate genetic associations generated by epistasis tend to increase Vg , L, and δ, this regime being well predicted by approximations including the effects of pairwise associations between loci. For yet higher values of U/n and/or lower effective recombination, a different regime is reached under which the maintenance of coadapted gene complexes reduces Vg , L, and δ. Simulations indicate that the values of Vg , L, and δ are little affected by assumptions regarding the number of possible alleles per locus.

Phylogenies indicate that the transition from outcrossing to selfing is frequent, with selfing populations being more prone to extinction. The rates of transition to selfing and extinction, acting on different timescales, could explain the observed distributions of extant selfing species among taxa. However, phylogenetic and theoretical studies consider these mechanisms independently, i.e. transitions do not cause extinction. Here, we theoretically explore the demographic consequences of the evolution of self-fertilization. Deleterious mutations and mutations modifying the selfing rate are recurrently introduced and the number of offspring depends on individual fitness, allowing for a demographic feedback. We show that mutational meltdowns can be triggered in populations evolving near strict selfing. Populations having survived the demographic crash are more stable than ancestral outcrossing populations once deleterious mutations are purged. The relatively rapid time-scales in which extinctions occur indicate that during evolutionary transitions the accumulation of deleterious mutations may not be the cause of extinctions observed on longer time scales, which in turn could lead to the underestimation of transition rates from outcrossing to selfing.

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.

Several methods based on the Sequential Markovian coalescence (SMC) have been developed that make use of genome sequence data to uncover population demographic history, which is of interest in its own right and is a key requirement to generate a null model for selection tests. While these methods can be applied to all possible kind of species, the underlying assumptions are sexual reproduction in each generation and non-overlapping generations. However, in many plants, invertebrates, fungi and other taxa, those assumptions are often violated due to different ecological and life history traits, such as self-fertilization or long term dormant structures (seed or egg-banking). We develop a novel SMC-based method to infer 1) the rates/parameters of dormancy and of self-fertilization, and 2) the populations’ past demographic history. Using simulated data sets, we demonstrate the accuracy of our method for a wide range of demographic scenarios and for sequence lengths from one to 30 Mb using four sampled genomes. Finally, we apply our method to a Swedish and a German population of Arabidopsis thaliana demonstrating a selfing rate of ca. 0.87 and the absence of any detectable seed-bank. In contrast, we show that the water flea Daphnia pulex exhibits a long lived egg-bank of three to 18 generations. In conclusion, we here present a novel method to infer accurate demographies and life-history traits for species with selfing and/or seed/egg-banks. Finally, we provide recommendations for the use of SMC-based methods for non-model organisms, highlighting the importance of the per site and the effective ratios of recombination over mutation., Author summary With the rapid advancement of sequencing technologies it has become feasible to use genome sequence data from several individuals per population/species to learn about the past history of populations, such as changes in population size, timing of colonization of a given habitat/continent or past migration events. However, all statistical methods to date rely on a mathematical model built upon characteristics of hominid species. Namely, this model ignores specific ecological traits common to many plant, invertebrate, or fungal species such as self-fertilization and dormancy. The latter is defined as the ability of plant seeds or invertebrates to remain dormant for long periods of time in the soil or sediments. Here we develop a new statistical method which uses several whole genome sequence data per population/species to simultaneously infer 1) the rates of dormancy and of self-fertilization, and 2) past demographic history. We demonstrate the accuracy of our method using extensive simulations. We also apply our method to Arabidopsis thaliana confirming a high rate of selfing and the absence of long term seed dormancy, and to Daphnia Pulex demonstrating a long lived egg bank. We discuss the wide applicability of our method to draw accurate inference of past evolution for non-hominid species.

Standing genetic variation is considered a major contributor to the adaptive potential of species. The low heritable genetic variation observed in self-fertilising 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-fertilising 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.

Inbreeding depression resulting from partially recessive deleterious alleles is thought to be the main genetic factor preventing self-fertilizing mutants from spreading in outcrossing hermaphroditic populations. However, deleterious alleles may also generate an advantage to selfers in terms of more efficient purging, while the effects of epistasis among those alleles on inbreeding depression and mating system evolution remain little explored. In this paper, we use a general model of selection to disentangle the effects of different forms of epistasis (additive-by-additive, additive-by-dominance and dominance-by-dominance) on inbreeding depression and on the strength of selection for selfing. Models with fixed epistasis across loci, and models of stabilizing selection acting on quantitative traits (generating distributions of epistasis) are considered as special cases. Besides its effects on inbreeding depression, epistasis may increase the purging advantage associated with selfing (when it is negative on average), while the variance in epistasis favors selfing through the generation of linkage disequilibria that increase mean fitness. Approximations for the strengths of these effects are derived, and compared with individual-based simulation results.

International audience; How life-history strategies influence the evolution of populations is not well understood. Most existing models stem from the Wright-Fisher model which considers discrete generations and a fixed population size, thus not taking into account any potential consequences of overlapping generations and demographic stochasticity on allelic frequencies. We introduce an individual-based model in which both population size and genotypic frequencies at a single bi-allelic locus are emergent properties of the model. Demographic parameters can be defined so as to represent a large range of r and K life-history strategies in a stable environment, and appropriate fixed effective population sizes are calculated so as to compare our model to the Wright-Fisher diffusion. Our results indicate that models with fixed population size that stem from the Wright-Fisher diffusion cannot fully capture the consequences of demographic stochasticity on allele fixation in long-lived species with low reproductive rates. This discrepancy is accentuated in the presence of demo-genetic feedback. Furthermore, we predict that populations with K life-histories should maintain lower genetic diversity than those with r life-histories.

Previous works has suggested that the harmonic mean population size can summarize the consequences of demographic fluctuations on the genetic frequencies of populations. We test this hypothesis by studying a model in which the demography and genetic composition of the population are both determined by the behavior of the individuals within the population. We propose an effective population size that allows us to compare our model with the classical Wright-Fisher diffusion both for neutral alleles and those under selection. We find that using our approximation for the effective population size, the Wright-Fisher diffusion provides good results for the times to absorption and probabilities of fixation of a given neutral allele and in cases where selection is not too strong. However, the times and laws to fixation are not always well predicted due to large fluctuations in population size caused by small growth rates or strong competition between individuals, that cannot be captured by the constant population size approximation. The discrepancy between our model and the Wright-Fisher diffusion is accentuated in the presence of demo-genetic feed-back. Our results imply that the Wright-Fisher diffusion is not appropriate when studying probabilities and times to fixation in long-lived species with low reproductive rates.

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100041).The mating system of a species is expected to have important effects on its genetic diversity. In this paper, we explore the effects of partial selfing on the equilibrium genetic varianceVg, mutation loadLand inbreeding depressionδunder stabilizing selection acting on a arbitrary numbernof quantitative traits coded by biallelic loci with additive effects. Overall, our model predicts a decrease in the equilibrium genetic variance with increasing selfing rates; however, the relationship between self-fertilization and the variables of interest depends on the strength of associations between loci, and three different regimes are observed. When theU/nratio is low (whereUis the total haploid mutation rate on selected traits) and effective recombination rates are sufficiently high, genetic associations between loci are negligible and the genetic variance, mutation load and inbreeding depression are well predicted by approximations based on single-locus models. For higher values ofU/nand/or lower effective recombination, moderate genetic associations generated by epistasis tend to increaseVg,Landδ, this regime being well predicted by approximations including the effects of pairwise associations between loci. For yet higher values ofU/nand/or lower effective recombination, a different regime is reached under which the maintenance of coadapted gene complexes reducesVg,Landδ. Simulations indicate that the values ofVg,Landδare little affected by assumptions regarding the number of possible alleles per locus.

International audience; Gametophytic self-incompatibility (GSI) is a widespread genetic system, which enables hermaphroditic plants to avoid self-fertilization and mating with close relatives. Inbreeding depression is thought to be the major force maintaining SI; however, inbreeding depression is a dynamical variable that depends in particular on the mating system. In this article we use multilocus, individual-based simulations to examine the coevolution of SI and inbreeding depression within finite populations. We focus on the conditions for the maintenance of SI when self-compatible (SC) mutants are introduced in the population by recurrent mutation, and compare simulation results with predictions from an analytical model treating inbreeding depression as a fixed parameter (thereby neglecting effects of purging within the SC subpopulation). In agreement with previous models, we observe that the maintenance of SI is associated with high inbreeding depression and is facilitated by high rates of self-pollination. Purging of deleterious mutations by SC mutants has little effect on the spread of those mutants as long as most deleterious alleles have weak fitness effects: in this case, the genetic architecture of inbreeding depression has little effect on the maintenance of SI. By contrast, purging may greatly enhance the spread of SC mutants when deleterious alleles have strong fitness effects.