Prior selfing occur in larger flowers in a mixed mating species with delayed selfing

Theory predicts that prior self-pollination (prior selfing) should not evolve in mixed mating species that enable delayed selfing. In this study, we test the hypotheais that prior selfing has evolved under severe pollinator limitation in the mixed mating species Commelina communis which can reproduce via delayed selfing. The hypothesis predicts that prior selfing occurs more frequently in populations with very low pollinator availability and/or in smaller flowers which receive infrequent visitations. We tested the predictions by comparing the degree of prior selfing among ten populations experiencing various levels of pollinator limitation and by examining a relationship between individual flower size and the occurrence of prior selfing. Populations with higher pollinator availability had higher prior selfing rate. Moreover, prior selfing occurs more frequently in larger flowers. These findings were totally opposite patterns of the predictions and the previous findings. We proposed new hypotheses that prior selfing has been maintained by the presence of reproductive interference from the congener and/or propotency in C. communis to explain our unexpected findings. We should verify potential effects of reproductive interference and propotency in future to elucidate the mystery of prior selfing in this mixed mating species with delayed selfing.

Self-Fertilization, Inbreeding, and Yield in Alfalfa Seed Production

Selfing (self-pollination) is the ultimate form of inbreeding, or mating among close relatives. Selfing can create yield loss when inbreeding depression, defined as a lower survival and reproduction of inbred relative to outbred progeny, is present. To determine the impact of selfing in alfalfa (Medicago sativa L.), we quantified the selfing rate of 32 alfalfa seed production fields located in three regions, namely, the Pacific Northwest (PNW), the Central Valley of California (CEV), and the Imperial Valley of California (IMP). Selfing rates (the proportion of selfed seeds) varied between 5.3 and 30% with an average of 12.2% over the 32 seed production fields. In both the parents and their progeny, we observed an excess of heterozygotes relative to Hardy–Weinberg expectations. We detected notable levels of inbreeding in parents (0.231 ± 0.007 parental inbreeding coefficient) and progeny (0.229 ± 0.005). There were a 15% decrease in the number of seeds per stem (seed set) and a 13% decline in the number of seeds per pod in selfed relative to outcrossed stems, but negligible inbreeding depression for pods per raceme and seed weight. The number of racemes on selfed stems increased significantly in fields with greater selfing rates, supporting the presence of geitonogamous or among flower selfing. Despite the significant level of inbreeding depression, seed set did not decrease in fields with higher selfing rates, where the greater number of racemes on the selfed stems increased the seed set. The effects of the field selfing rate on the seed yield metrics were mostly indirect with direct effects of the number of racemes per stem. Available data indicate that the majority of selfing in alfalfa is pollinator-mediated, and thus, eliminating selfing in alfalfa seed production would require the selection of self-incompatible varieties, which, by eliminating inbreeding depression, would provide a 15% potential increase in seed yield and an increase in future hay yield.

Genetic load may increase or decrease with selfing depending upon the recombination environment

Theory predicts that the ability for natural selection to remove deleterious mutations from a population, and prevent the accumulation of genetic load, is a function of the effective population size (Ne). Shifts from random mating to self-fertilization (selfing) are predicted to decrease Ne through a variety of genomic changes - including a reduction in effective recombination and an increase in homozygosity. While a long history of theory suggests that the efficacy of selection, particularly against non-recessive mutations, should decrease with selfing rate, comparisons of genomic-based estimates of the efficacy of selection between related outcrosser-selfer pairs have revealed conflicting results. We address this paradox by simulating the evolution of strongly deleterious recessive and weakly deleterious additive mutations across a range of recombination, mutation and selective parameter combinations. We find that the genetic load of a population can either increase, decrease, or not vary with selfing rate. Genetic load is higher in selfers only when recombination rates are greater than mutation rates. When recombination rates are lower than mutation rates, an accumulation of recessive mutations leads to pseudo-overdominance, a type of balancing selection, in outcrossing populations. Using both simulations and analytical theory, we show that pseudo-overdominance has strong negative effects on the efficacy of selection against linked additive mutations and that a threshold level of selfing prevents pseudo-overdominance. Our results show that selection can be more or less effective in selfers as compared to outcrossers depending on the relationship between the deleterious mutation rate and gene density, and therefore different genomic regions in different taxa could show differing results.

Mating system of Datura inoxia: association between selfing rates and herkogamy within populations

Plant mating system determines, to a great extent, the demographic and genetic properties of populations, hence their potential for adaptive evolution. Variation in plant mating system has been documented between phylogenetically related species as well between populations of a species. A common evolutionary transition, from outcrossing to selfing, is likely to occur under environmental spatial variation in the service of pollinators. Here, we studied two phenotypically (in floral traits) and genetically (in neutral molecular markers) differentiated populations of the annual, insect-pollinated, plant Datura inoxia in Mexico, that differ in the service of pollinators (Mapimí and Cañada Moreno). First, we determined the populations’ parameters of phenotypic in herkogamy, outcrossing and selfing rates with microsatellite loci, and assessed between generation (adults and seedlings) inbreeding, and inbreeding depression. Second, we compared the relationships between parameters in each population. Results point strong differences between populations: plants in Mapimí have, on average, approach herkogamy, higher outcrossing rate (tm = 0.68), lower primary selfing rate (r = 0.35), and lower inbreeding at equilibrium (Fe = 0.24) and higher inbreeding depression (δ = 0.25), than the populations of Cañada. Outcrossing seems to be favored in Mapimí while selfing in Cañada. The relationship between r and Fe were negatively associated with herkogamy in Mapimí; here, progenies derived from plants with no herkogamy or reverse herkogamy had higher selfing rate and inbreeding coefficient than plants with approach herkogamy. The difference Fe–F is positively related to primary selfing rate (r) only in Cañada Moreno which suggests inbreeding depression in selfing individuals and then genetic purging. In conclusion, mating system evolution may occur differentially among maternal lineages within populations of Datura inoxia, in which approach herkogamy favors higher outcrossing rates and low levels of inbreeding and inbreeding depression, while no herkogamy or reverse herkogamy lead to the evolution of the “selfing syndrome” following the purge of deleterious alleles despite high inbreeding among individuals.

How and When Does Outcrossing Occur in the Predominantly Selfing Species Medicago truncatula?

Empirical studies on natural populations of Medicago truncatula revealed selfing rates higher than 80%, but never up to 100%. Similarly, several studies of predominantly selfing species show variability in the level of residual outcrossing between populations and also between temporal samples of the same population. However, these studies measure global selfing rates at the scale of the population and we do not know whether there is intra-population variation and how outcrossing events are distributed, between genotypes, plants, flowers, or seeds. Theoretical studies predict the maintenance of residual outcrossing in highly selfing species due to environmental (e.g., pollen biology) and/or genetic determinants and decompositions of the variation in outcrossing rate using experimental data can be very informative to test these hypotheses. Here, we focus on one natural population of M. truncatula in order to describe precisely its mating system. In particular, we investigated the determinants of the selfing rate by testing for seasonal variations (environmental determinism) and variations between genotypes (genetic determinism). We measured selfing rates in maternal progenies from plants collected widely across a natural population. For each plant, we collected pods from flowers produced at the beginning and at the end of the flowering season to test for a seasonal variation in the outcrossing rate. For each collected offspring, we also estimated the likelihood that it was issued from a self-fertilization event and assessed the genetic component of variation of this mating system measure. We found a significant, albeit small, increase in outcrossing rate in progenies collected at the end [tm = 0.137 (SD = 0.025)] compared to those collected at the beginning [tm = 0.083 (0.016)] of the flowering season. A significant between genotypes variation in selfing rate was also detected, resulting in a heritability of 9% for the rate of residual outcrossing. Altogether, our work shows that despite a predominantly selfing reproductive mode, M. truncatula displays variation in residual outcrossing rate, and that this trait is likely under a complex determinism combining environmental and genetic factors. We discuss the evolutionary implications of our results for the population.

The genetic basis of adaptation through the evolution of self-fertilization

Although adaptation can be realized through the fixation of beneficial alleles that increase viability, many plant populations may adapt through the evolution of self-fertilization, especially when pollination becomes inefficient. However, the genetic basis of adaptation through the evolution of selfing remains unclear. Using population genetic models, I study adaptation through the fixation of alleles that increase the selfing rate (selfing modifiers) from new mutations or/and standing variation. For adaptive alleles unrelated to selfing, it is known that selfing promotes adaptation from a new mutation only when the beneficial alleles are recessive, and the probability of adaptation from standing variation is nearly independent of dominance, and always decreases with the selfing rate. In contrast, for adaptation through the evolution of selfing, when it occurs by fixation of a newly arisen mutation, a population that already has a high selfing rate may be more (less) likely to adapt than outcrossers even when the modifier is dominant (recessive) if the modifier is weakly (strongly) selected. Also, adaptation from standing variation is more likely through recessive modifier alleles, with the highest fixation probability found in partially selfing populations, but fixation is fastest when dominance is intermediate. When there are multiple modifiers, adaptation through new mutations is more likely when selfing is controlled by few large-effect rather than many slight-effect modifiers. This study suggests that to understand the genetic basis of adaptation, it is necessary to determine the ecological and genetic advantages of adaptive alleles.Significance statementThis study, by deriving the selective coefficient and effective population size, investigated the genetic basis of adaptation through fixation of modifier alleles that increase the selfing rate, which is shown to differ in several aspects from that through evolution of mating-unrelated alleles. Specifically, when adaptation is from new mutations, the dominance of a selfing modifier allele below which selfing increases the fixation probability depends on the strength of pollen limitation and pollen discounting. Adaptation from standing variation is more likely through recessive modifier alleles and in populations with an intermediate selfing rate. This work suggests it is important to have a mechanistic understanding of how adaptive alleles increase individual fitness in environment that is unfavorable to the population.

Eco-evolutionary dynamics of prior selfing rate promotes the coexistence without niche partitioning under reproductive interference

When the two or more plants species share the same pollinators, pollinator-mediated reproductive interference make coexistence difficult. Recent studies suggested prior autonomous selfing mitigate reproductive interference, could enabling coexistence without pollination niche partitioning (pre-emptive selfing hypothesis). However, there are no studies to test whether evolution of prior selfing promote the coexistence, considering eco-evolutionary dynamics of population size, selfing rate and inbreeding depression.To examine conditions that the evolution of prior selfing promote coexistence under mutual reproductive interference especially in the point of view for pollinator availability and dynamics of inbreeding depression, we constructed individual-based model in which two plant species compete against each other in the form of mutual reproductive interference and can evolve prior autonomous selfing rate. We expected that purging of deleterious mutations could cause evolutionary rescue because inferior species could rescue population density through the evolution of prior selfing if the strength of inbreeding depression decreases with an increase of population’s selfing rate.Our simulation demonstrated that the evolution of prior selfing could promote the coexistence while reproductive interference caused competitive exclusion without evolution. We found that lower pollinator availability tended to prefer rapid evolutionary shift to higher prior selfing rate, it neutralizes the negative effect of reproductive interference, and population dynamics exhibit neutral random walk in both species. When the strength of inbreeding depression decreased with an increase in population’s selfing rate, moderate pollinator availability resulted in long-term coexistence in which relative-abundance-dependent selection on the prior selfing rate rescue population density of inferior species intermittently.Synthesis. We showed that the evolution of prior selfing could increase population growth rate of inferior species and consequently enable the long-term coexistence with evolutionary rescue. This is the new mechanisms explaining co-evolutionary coexistence of closely related plant species without niche partitioning and consistent with recent studies reported that closely related mixed-mating species are sympatrically growing even under the mutual reproductive interference.

Effect of partial selfing and polygenic selection on establishment in a new habitat

This paper analyzes how partial selfing in a large source population influences its ability to colonize a new habitat via the introduction of a few founder individuals. Founders experience inbreeding depression due to partially recessive deleterious alleles as well as maladaptation to the new environment due to selection on a large number of additive loci. I first introduce a simplified version of the Inbreeding History Model (Kelly, 2007) in order to characterize mutation-selection balance in a large, partially selfing source population under selection involving multiple non-identical loci. I then use individual-based simulations to study the eco-evolutionary dynamics of founders establishing in the new habitat under a model of hard selection. The study explores how selfing rate shapes establishment probabilities of founders via effects on both inbreeding depression and adaptability to the new environment, and also distinguishes the effects of selfing on the initial fitness of founders from its effects on the long-term adaptive response of the populations they found. A high rate of (but not complete) selfing is found to aid establishment over a wide range of parameters, even in the absence of mate limitation. The sensitivity of the results to assumptions about the nature of polygenic selection are discussed.