The effect of mating system differences on nucleotide diversity at the phosphoglucose isomerase locus in the plant genus Leavenworthia.

To test the theoretical prediction that highly inbreeding populations should have low neutral genetic diversity relative to closely related outcrossing populations, we sequenced portions of the cytosolic phosphoglucose isomerase (PgiC) gene in the plant genus Leavenworthia, which includes both self-incompatible and inbreeding taxa. On the basis of sequences of intron 12 of this gene, the expected low diversity was seen in both populations of the selfers Leavenworthia uniflora and L. torulosa and in three highly inbreeding populations of L. crassa, while high diversity was found in self-incompatible L. stylosa, and moderate diversity in L. crassa populations with partial or complete self-incompatibility. In L. stylosa, the nucleotide diversity was strongly structured into three haplotypic classes, differing by several insertion/deletion sequences, with linkage disequilibrium between sequences of the three types in intron 12, but not in the adjacent regions. Differences between the three kinds of haplotypes are larger than between sequences of this gene region from different species. The haplotype divergence suggests the presence of a balanced polymorphism at this locus, possibly predating the split between L. stylosa and its two inbreeding sister taxa, L. uniflora and L. torulosa. It is therefore difficult to distinguish between different potential causes of the much lower sequence diversity at this locus in inbreeding than outcrossing populations. Selective sweeps during the evolution of these populations are possible, or background selection, or merely loss of a balanced polymorphism maintained by overdominance in the populations that evolved high selfing rates.     

Inbreeding depression in self-incompatible and self-compatible populations of Leavenworthia alabamica

Inbreeding depression is one of the leading factors preventing the evolution of self-fertilization in plants. In populations where self-fertilization evolves, theory suggests that natural selection against partially recessive deleterious alleles will reduce inbreeding depression. The purpose of this study was to evaluate this hypothesis by comparing the magnitude of inbreeding depression in self-incompatible and self-compatible populations of Leavenworthia alabamica. Within-population crosses were conducted to compare the quantity and quality of offspring produced by outcrossing and self-fertilization. These progeny were grown in a common greenhouse and inbreeding depression was measured in germination, survival, biomass, transition rate to flowering, flower number, petal length, pollen grains/anther, pollen viability, and ovule number. In comparison to outcrossing, self-fertilization led to the production of fewer and smaller seeds within self-incompatible populations. Moreover, inbreeding depression was observed in eight of 11 offspring traits within self-incompatible populations of L. alabamica. In contrast, there was significant inbreeding depression only in flower number within self-compatible populations. The results of this study are consistent with the idea that self-fertilization selectively removes partially recessive deleterious alleles causing inbreeding depression in natural plant populations. However, in plant species such as L. alabamica where self-compatibility may evolve in small populations following long-distance dispersal, declines in inbreeding depression may also be facilitated by genetic drift.     

THE EVOLUTION OF SELF-FERTILIZATION AND INBREEDING DEPRESSION IN PLANTS. II. EMPIRICAL OBSERVATIONS

A bimodal distribution of outcrossing rates was observed for natural plant populations, with more primarily selfing and primarily outcrossing species, and fewer species with intermediate outcrossing rate than expected by chance. We suggest that this distribution results from selection for the maintenance of outcrossing in historically large, outcrossing populations with substantial inbreeding depression, and from selection for selfing when increased inbreeding, due to pollinator failure or population bottlenecks, reduces the level of inbreeding depression. Few species or populations are fixed at complete selfing or complete outcrossing. A low level of selfing in primarily outcrossing species is unlikely to be selectively advantageous, but will not reduce inbreeding depression to the level where selfing is selectively favored, particularly if accompanied by reproductive compensation. Similarly, occasional outcrossing in primarily selfing species is unlikely to regularly provide sufficient heterosis to maintain selection for outcrossing through individual selection. Genetic, morphological and ecological constraints may limit the potential for outcrossing rates in selfers to be reduced below some minimum level.     

Microsatellite variation and evolution in the Mimulus guttatus species complex with contrasting mating systems

Mutational variability at microsatellite loci is shaped by both population history and the mating system. In turn, alternate mating systems in flowering plants can resolve aspects of microsatellite loci evolution. Five species of yellow monkeyflowers (Mimulus sect. Simiolis) differing for historical rates of inbreeding were surveyed for variation at six microsatellite loci. High levels of diversity at these loci were found in both outcrossing and selfing taxa. In line with allozyme studies, inbreeders showed more partitioning of diversity among populations, and diversity in selfing taxa was lower than expected from reductions in effective population size due to selfing alone, suggesting the presence of either population bottlenecks or background selection in selfers. Evaluation of the stepwise mutation model (a model of DNA replication slippage) suggests that these loci evolve in a stepwise fashion. Inferred coalescent times of microsatellite alleles indicate that past bottlenecks of population size or colonization events were important in reducing diversity in the inbreeding taxon.      

Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants

A compilation of studies using RAPD markers for evaluating population differentiation resulted in 78 estimates of AMOVA-derived Φ_ST and 31 estimates of Nei's G_ST, as well as in 41 estimates of Nei's within-population diversity. In outcrossing taxa, estimates of between-population diversity were closely correlated with maximum geographic distance between sampled populations. A corresponding association was not found in selfing taxa. These results suggest that RAPD can be a sensitive method for detection of genetic structuring according to the isolation-by-distance model. However, it also means that sampling strategies, as applied in individual studies, can seriously influence the resulting estimates of between-population diversity. Other sampling strategies, like number of plants per population and number of scored polymorphic markers, do not seem to impart any serious artefacts. As previously verified with allozyme data, RAPD markers showed that long-lived, outcrossing, late successional taxa retain most of their genetic variability within populations. By contrast, annual, selfing and/or early successional taxa allocate most of the genetic variability among populations. Estimates for between- and within-population diversity, respectively, proved to be negatively correlated, as previously reported for allozyme data. The only major discrepancy between allozymes and RAPD markers concerns geographic range; within-population diversity was strongly affected by distributional range of the investigated species in the allozyme data but not in the RAPD data. Moreover, RAPD-based values for between-population diversity increased with increasing distributional range whereas the opposite has been reported in a large allozyme data compilation. Contrary to allozymes, RAPD marker-derived within-population diversity is probably therefore not a very good predictor of total species genetic diversity.     

Inbreeding depression and low between-population heterosis in recently diverged experimental populations of a selfing species

In fragmented populations, genetic drift and selection reduce genetic diversity, which in turn results in a loss of fitness or in a loss of evolvability. Genetic rescue, that is, controlled input of diversity from distant populations, may restore evolutionary potential, whereas outbreeding depression might counteract the positive effect of this strategy. We carried out self-pollination and crosses within and between populations in an experimental subdivided population of a selfing species, Triticum aestivum L., to estimate the magnitude of these two phenomena. Surprisingly, for a self-fertilizing species, we found significant inbreeding depression within each population for four of the six traits studied, indicating that mildly deleterious mutations were still segregating in these populations. The progeny of within- and between-population crosses was very similar, indicating low between-population heterosis and little outbreeding depression. We conclude that relatively large population effective sizes prevented fixation of a high genetic load and that local adaptation was limited in these recently diverged populations. The kinship coefficient estimated between the parents using 20 neutral markers was a poor predictor of the progeny phenotypic values, indicating that there was a weak link between neutral diversity and genes controlling fitness-related traits. These results show that when assessing the viability of natural populations and the need for genetic rescue, the use of neutral markers should be complemented with information about the presence of local adaptation in the subdivided population.     

INBREEDING DEPRESSION,GENETIC LOAD,AND THE EVOLUTION OF OUTCROSSING RATES IN A MULTILOCUS SYSTEM WITH NO LINKAGE

We studied deterministic models of multilocus systems subject to mutation–selection balance with all loci unlinked, and with multiplicative interactions of the loci affecting fitness, in partially self-fertilizing populations. The aim was to examine the fitnesses of the zygotes produced by outcrossing and by selling, and the magnitude of inbreeding depression, in populations with different levels of inbreeding. The fates of modifiers of the outcrossing rate were also examined. With biologically plausible parameter values, inbreeding depression can be very large in moderately selfing populations, particularly when the mutant alleles are fairly recessive and selection is weak. A modifier allele reducing the selfing rate can be favored under these circumstances. In more inbred populations, inbreeding depression is lower, and selection favors alleles that increase the selfing rate. When inbreeding depression is caused by mutant alleles with strong selective disadvantage, modifiers causing large increases in selfing can often be favored even when the inbreeding depression exceeds one-half, though in these circumstances modifiers increasing selfing by smaller amounts are usually eliminated. Weaker selection appears to be more favorable to the maintenance of outcrossing.     

The effect of linkage and population size on inbreeding depression due to mutational load.

Using a stochastic model of a finite population in which there is mutation to partially recessive detrimental alleles at many loci, we study the effects of population size and linkage between the loci on the population mean fitness and inbreeding depression values. Although linkage between the selected loci decreases the amount of inbreeding depression, neither population size nor recombination rate have strong effects on these quantities, unless extremely small values are assumed. We also investigate how partial linkage between the loci that determine fitness affects the invasion of populations by alleles at a modifier locus that controls the selfing rate. In most of the cases studied, the direction of selection on modifiers was consistent with that found in our previous deterministic calculations. However, there was some evidence that linkage between the modifier locus and the selected loci makes outcrossing less likely to evolve; more losses of alleles promoting outcrossing occurred in runs with linkage than in runs with free recombination. We also studied the fate of neutral alleles introduced into populations carrying detrimental mutations. The times to loss of neutral alleles introduced at low frequency were shorter than those predicted for alleles in the absence of selected loci, taking into account the reduction of the effective population size due to inbreeding. Previous studies have been confined to outbreeding populations, and to alleles at frequencies close to one-half, and have found an effect in the opposite direction. It therefore appears that associations between neutral and selected loci may produce effects that differ according to the initial frequencies of the neutral alleles.     

EVOLUTION OF THE MAGNITUDE AND TIMING OF INBREEDING DEPRESSION IN PLANTS

Estimates of inbreeding depression obtained from the literature were used to evaluate the association between inbreeding depression and the degree of self-fertilization in natural plant populations. Theoretical models predict that the magnitude of inbreeding depression will decrease with inbreeding as deleterious recessive alleles are expressed and purged through selection. If selection acts differentially among life history stages and deleterious effects are uncorrelated among stages, then the timing of inbreeding depression may also evolve with inbreeding. Estimates of cumulative inbreeding depression and stage-specific inbreeding depression (four stages: seed production of parent, germination, juvenile survival, and growth/reproduction) were compiled for 79 populations (using means of replicates, N = 62) comprising 54 species from 23 families of vascular plants. Where available, data on the mating system also were collected and used as a measure of inbreeding history. A significant negative correlation was found between cumulative inbreeding depression and the primary selfing rate for the combined sample of angiosperms (N = 35) and gymnosperms (N = 9); the correlation was significant for angiosperms but not gymnosperms examined separately. The average inbreeding depression in predominantly selfing species (δ = 0.23) was significantly less (43%) than that in predominantly outcrossing species (δ = 0.53). These results support the theoretical prediction that selfing reduces the magnitude of inbreeding depression. Most self-fertilizing species expressed the majority of their inbreeding depression late in the life cycle, at the stage of growth/reproduction (14 of 18 species), whereas outcrossing species expressed much of their inbreeding depression either early, at seed production (17 of 40 species), or late (19 species). For species with four life stages examined, selfing and outcrossing species differed in the magnitude of inbreeding depression at the stage of seed production (selfing δ = 0.05, N = 11; outcrossing δ = 0.32, N = 31), germination (selfing δ = 0.02, outcrossing δ = 0.12), and survival to reproduction (selfing δ = 0.04, outcrossing δ = 0.15), but not at growth and reproduction (selfing δ = 0.21, outcrossing δ = 0.27); inbreeding depression in selfers relative to outcrossers increased from early to late life stages. These results support the hypothesis that most early acting inbreeding depression is due to recessive lethals and can be purged through inbreeding, whereas much of the late-acting inbreeding depression is due to weakly deleterious mutations and is very difficult to purge, even under extreme inbreeding.     

Evolution of sociality in spiders leads to depleted genomic diversity at both population and species levels

Across several animal taxa, the evolution of sociality involves a suite of characteristics, a “social syndrome,” that includes cooperative breeding, reproductive skew, primary female‐biased sex ratio, and the transition from outcrossing to inbreeding mating system, factors that are expected to reduce effective population size (Ne). This social syndrome may be favoured by short‐term benefits but come with long‐term costs, because the reduction in Ne amplifies loss of genetic diversity by genetic drift, ultimately restricting the potential of populations to respond to environmental change. To investigate the consequences of this social life form on genetic diversity, we used a comparative RAD‐sequencing approach to estimate genomewide diversity in spider species that differ in level of sociality, reproductive skew and mating system. We analysed multiple populations of three independent sister‐species pairs of social inbreeding and subsocial outcrossing Stegodyphus spiders, and a subsocial outgroup. Heterozygosity and within‐population diversity were sixfold to 10‐fold lower in social compared to subsocial species, and demographic modelling revealed a tenfold reduction in Ne of social populations. Species‐wide genetic diversity depends on population divergence and the viability of genetic lineages. Population genomic patterns were consistent with high lineage turnover, which homogenizes the genetic structure that builds up between inbreeding populations, ultimately depleting genetic diversity at the species level. Indeed, species‐wide genetic diversity of social species was 5–8 times lower than that of subsocial species. The repeated evolution of species with this social syndrome is associated with severe loss of genomewide diversity, likely to limit their evolutionary potential.     

Antagonism between local dispersal and self-incompatibility systems in a continuous plant population

Many self-incompatible plant species exist in continuous populations in which individuals disperse locally. Local dispersal of pollen and seeds facilitates inbreeding because pollen pools are likely to contain relatives. Self-incompatibility promotes outbreeding because relatives are likely to carry incompatible alleles. Therefore, populations can experience an antagonism between these forces. In this study, a novel computational model is used to explore the effects of this antagonism on gene flow, allelic diversity, neighbourhood sizes, and identity by descent. I confirm that this antagonism is sensitive to dispersal levels and linkage. However, the results suggest that there is little to no difference between the effects of gametophytic and sporophytic self-incompatibility systems (GSI and SSI) on unlinked loci. More importantly, both GSI and SSI affect unlinked loci in a manner similar to obligate outcrossing without mating types. This suggests that the primary evolutionary impact of self-incompatibility systems may be to prevent selfing, and prevention of biparental inbreeding might be a beneficial side-effect.     

Genetic diversity and population structure of the Italian fungi belonging to the taxa Pleurotus eryngii (DC.:Fr.) Quèl and P. ferulae (DC.:Fr.) Quèl

A study using allozymes and PCR fingerprinting was conducted to estimate the genetic diversity of Italian populations of two economically important cultivated fungal taxa, Pleurotus eryngii and P. ferulae. Very little is known about the genetic diversity distribution pattern of these taxa. Heterozygote deficiency was observed at few loci; in fact the inbreeding coefficients were not high, which demonstrates that mechanisms restrain the inbreeding act at the local level. Estimates of genetic differentiation indicated a pattern of greater variation within, rather than between, populations. These results were supported by AMOVA analysis, which attributed a low proportion of the total genetic variation to large geographical scale divergence, and indicated that most of the genetic diversity was because of differences within populations. This distribution pattern of genetic variation of P. eryngii and P. ferulae populations seems to be the result of high gene flow, by efficient basidiospore dispersal, and outcrossing mechanisms, which restrain inbreeding within populations.     

THE EVOLUTION OF SELF-FERTILIZATION AND INBREEDING DEPRESSION IN PLANTS. I. GENETIC MODELS

The amounts of inbreeding depression upon selfing and of heterosis upon outcrossing determine the strength of selection on the selfing rate in a population when this evolves polygenically by small steps. Genetic models are constructed which allow inbreeding depression to change with the mean selfing rate in a population by incorporating both mutation to recessive and partially dominant lethal and sublethal alleles at many loci and mutation in quantitative characters under stabilizing selection. The models help to explain observations of high inbreeding depression (> 50%) upon selfing in primarily outcrossing populations, as well as considerable heterosis upon outcrossing in primarily selfing populations. Predominant selfing and predominant outcrossing are found to be alternative stable states of the mating system in most plant populations. Which of these stable states a species approaches depends on the history of its population structure and the magnitude of effect of genes influencing the selfing rate.     

STRONG INBREEDING DEPRESSION IN TWO SCANDINAVIAN POPULATIONS OF THE SELF‐INCOMPATIBLE PERENNIAL HERB ARABIDOPSIS LYRATA

Inbreeding depression is a key factor influencing mating system evolution in plants, but current understanding of its relationship with selfing rate is limited by a sampling bias with few estimates for self‐incompatible species. We quantified inbreeding depression (δ) over two growing seasons in two populations of the self‐incompatible perennial herb Arabidopsis lyrata ssp. petraea in Scandinavia. Inbreeding depression was strong and of similar magnitude in both populations. Inbreeding depression for overall fitness across two seasons (the product of number of seeds, offspring viability, and offspring biomass) was 81% and 78% in the two populations. Chlorophyll deficiency accounted for 81% of seedling mortality in the selfing treatment, and was not observed among offspring resulting from outcrossing. The strong reduction in both early viability and late quantitative traits suggests that inbreeding depression is due to deleterious alleles of both large and small effect, and that both populations experience strong selection against the loss of self‐incompatibility. A review of available estimates suggested that inbreeding depression tends to be stronger in self‐incompatible than in self‐compatible highly outcrossing species, implying that undersampling of self‐incompatible taxa may bias estimates of the relationship between mating system and inbreeding depression.     

Digest: Exposing the role of rare alleles in inbreeding depression in monkeyflower*

Outcrossing is maintained in many hermaphroditic species despite theoretical work suggesting that alleles increasing selfing should invade outcrossing populations. Brown and Kelly (2019) identify reasons why this may not have occurred in an outcrossing population of monkeyflower, namely that inbreeding depression causes strong reductions in fitness, resulting in selection for the maintenance of outcrossing. They find that genetic load imposed by rare alleles is inversely correlated with fitness-associated traits, providing evidence that recessive, deleterious alleles contribute to inbreeding depression.     

The genetic basis and experimental evolution of inbreeding depression in Caenorhabditis elegans

Determining the genetic basis of inbreeding depression is important for understanding the role of selection in the evolution of mixed breeding systems. Here, we investigate how androdioecy (a breeding system characterized by partial selfing and outcrossing) and dioecy (characterized by obligatory outcrossing) influence the experimental evolution of inbreeding depression in Caenorhabditis elegans. We derived inbred lines from ancestral and evolved populations and found that the dioecious lineages underwent more extinction than androdioecious lineages. For both breeding systems, however, there was selection during inbreeding because the diversity patterns of 337 single-nucleotide polymorphisms (SNPs) among surviving inbred lines deviated from neutral expectations. In parallel, we also followed the evolution of embryo to adult viability, which revealed similar starting levels of inbreeding depression in both breeding systems, but also outbreeding depression. Under androdioecy, diversity at a neutral subset of 134 SNPs correlated well with the viability trajectories, showing that the population genetic structure imposed by partial selfing affected the opportunity for different forms of selection. Our findings suggest that the interplay between the disruptions of coevolved sets of loci by outcrossing, the efficient purging of deleterious recessive alleles with selfing and overdominant selection with outcrossing can help explain mixed breeding systems.     

MUTATIONAL MELTDOWN IN SELFING ARABIDOPSIS LYRATA

The majority of plant species and many animals are hermaphrodites, with individuals expressing both female and male function. Although hermaphrodites can potentially reproduce by self‐fertilization, they have a high prevalence of outcrossing. The genetic advantages of outcrossing are described by two hypotheses: avoidance of inbreeding depression because selfing leads to immediate expression of recessive deleterious mutations, and release from drift load because self‐fertilization leads to long‐term accumulation of deleterious mutations due to genetic drift and, eventually, to extinction. I tested both hypotheses by experimentally crossing Arabidopsis lyrata plants (self‐pollinated, cross‐pollinated within the population, or cross‐pollinated between populations) and measuring offspring performance over 3 years. There were 18 source populations, each of which was either predominantly outcrossing, mixed mating, or predominantly selfing. Contrary to predictions, outcrossing populations had low inbreeding depression, which equaled that of selfing populations, challenging the central role of inbreeding depression in mating system shifts. However, plants from selfing populations showed the greatest increase in fitness when crossed with plants from other populations, reflecting higher drift load. The results support the hypothesis that extinction by mutational meltdown is why selfing hermaphroditic taxa are rare, despite their frequent appearance over evolutionary time.     

花蔺和黄花蔺居群遗传结构比较研究

采用垂直板型聚丙烯酰胺凝胶电泳技术,分别通过１９和２１个等位酶位点测定了花蔺３个居群和黄花蔺４个居群的遗传结构与基因流。两类群都维持较高水平的遗传多样性。花蔺居群期望杂合度、固定指数、异交率和遗传分化分别为０．１４４、０．１７４、９４．０％和０．２００,显示出异交繁育系统类型。黄花蔺居群期望杂合度、固定指数、异交率和遗传分化分别为０．０７６、０．４１５、５８．５％和０．３９１。表明其异交＋自交的敏     

High gene flow and outcrossing within populations of two cryptic fungal pathogens on a native and non-native host in Cameroon

In this study, we determined the genetic diversity of 126 isolates representing both Lasiodiplodia theobromae and Lasiodiplodia pseudotheobromae, collected from Theobroma cacao and Terminalia spp. in Cameroon, using simple sequence repeat (SSR) markers. SSR alleles showed clear genetic distinction between L. theobromae and L. pseudotheobromae, supporting their earlier separation as sister species. Both L. theobromae and L. pseudotheobromae populations from Cameroon had high levels of gene diversity, moderate degrees of genotypic diversity, and high levels of gene flow between isolates from T. cacao and Terminalia spp. There was no evidence for geographic substructure in these populations across the region studied, and the SSR alleles were randomly associated in both species, suggesting outcrossing. The significant levels of aggressiveness, evolutionary potential represented by high levels of diversity, outcrossing and gene flow between geographically and host defined populations, identify these fungi as high-risk pathogens for their native and non-native hosts in Cameroon.     

Genetic diversity,sexual condition,and microhabitat preference determine mating patterns in Sphagnum (Sphagnaceae) peat‐mosses

In bryophytes, the possibility of intragametophytic selfing creates complex mating patterns that are not possible in seed plants, although relatively little is known about patterns of inbreeding in natural populations. In the peat‐moss genus Sphagnum, taxa are generally bisexual (gametophytes produce both sperm and egg) or unisexual (gametes produced by separate male and female plants). We sampled populations of 14 species, aiming to assess inbreeding variation and inbreeding depression in sporophytes, and to evaluate correlations between sexual expression, mating systems, and microhabitat preferences. We sampled maternal gametophytes and their attached sporophytes at 12–19 microsatellite loci. Bisexual species exhibited higher levels of inbreeding than unisexual species but did generally engage in some outcrossing. Inbreeding depression did not appear to be common in either unisexual or bisexual species. Genetic diversity was higher in populations of unisexual species compared to populations of bisexual species. We found a significant association between species microhabitat preference and population genetic diversity: species preferring hummocks (high above water table) had populations with lower diversity than species inhabiting hollows (at the water table). We also found a significant interaction between sexual condition, microhabitat preference, and inbreeding coefficients, suggesting a vital role for species ecology in determining mating patterns in Sphagnum populations. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 96–113.