Incest versus abstinence: reproductive trade‐offs between mate limitation and progeny fitness in a self‐incompatible invasive plant

Plant mating systems represent an evolutionary and ecological trade‐off between reproductive assurance through selfing and maximizing progeny fitness through outbreeding. However, many plants with sporophytic self‐incompatibility systems exhibit dominance interactions at the S‐locus that allow biparental inbreeding, thereby facilitating mating between individuals that share alleles at the S‐locus. We investigated this trade‐off by estimating mate availability and biparental inbreeding depression in wild radish from five different populations across Australia. We found dominance interactions among S‐alleles increased mate availability relative to estimates based on individuals that did not share S‐alleles. Twelve of the sixteen fitness variables were significantly reduced by inbreeding. For all the three life‐history phases evaluated, self‐fertilized offspring suffered a greater than 50% reduction in fitness, while full‐sib and half‐sib offspring suffered a less than 50% reduction in fitness. Theory indicates that fitness costs greater than 50% can result in an evolutionary trajectory toward a stable state of self‐incompatibility (SI). This study suggests that dominance interactions at the S‐locus provide a possible third stable state between SI and SC where biparental inbreeding increases mate availability with relatively minor fitness costs. This strategy allows weeds to establish in new environments while maintaining a functional SI system.     

THE POPULATION GENETICS OF SPOROPHYTIC SELF‐INCOMPATIBILITY IN THREE HYBRIDIZING SENECIO (ASTERACEAE) SPECIES WITH CONTRASTING POPULATION HISTORIES

Hybridization generates evolutionary novelty and spreads adaptive variation. By promoting outcrossing, plant self‐incompatibility (SI) systems also favor interspecific hybridization because the S locus is under strong negative frequency‐dependent balancing selection. This study investigates the SI mating systems of three hybridizing Senecio species with contrasting population histories. Senecio aethnensis and S. chrysanthemifolius native to Sicily, form a hybrid zone at intermediate altitudes on Mount Etna, and their neo‐homoploid hybrid species, S. squalidus, has colonized disturbed urban habitats in the UK during the last 150 years. We show that all three species express sporophytic SI (SSI), where pollen incompatibility is controlled by the diploid parental genome, and that SSI is inherited and functions normally in hybrids. Large‐scale crossing studies of wild sampled populations allowed direct comparison of SSI between species and found that the main impacts of colonization in S. squalidus compared to Sicilian Senecio was a reduced number of S alleles, increased S allele frequencies, and increased interpopulation S allele sharing. In general, many S alleles were shared between species and the S locus showed reduced intra‐ and interspecific population genetic structure compared to molecular genetic markers, indicative of enhanced effective gene flow due to balancing selection.     

MATE AVAILABILITY AND FECUNDITY SELECTION IN MULTI-ALLELIC SELF-INCOMPATIBILITY SYSTEMS IN PLANTS

We investigate mate availability in different models of multiallelic self-incompatibility systems in mutation-selection-drift balance in finite populations. Substantial differences among self-incompatibility systems occur in average mate availability, and in variances of mate availability among individual plants. These differences are most pronounced in small populations in which low mate availability may reduce seed set in some types of sporophytic self-incompatibility. In cases where the pollination system causes a restriction in the number of pollen genotypes available to an individual plant, the fecundity of that plant depends on the availability of compatible pollen, which is determined by its genotype at the incompatibility locus. This leads to an additional component of selection acting on self-incompatibility systems, which we term “fecundity selection.” Fecundity selection increases the number of alleles maintained in finite populations and increases mate availability in small populations. The strength of fecundity selection is dependent on the type of self-incompatibility. In some cases, fecundity selection markedly alters the equilibrium dynamics of self-incompatibility alleles. We discuss the population genetic consequences of mate availability and fecundity selection in the contexts of conservation management of self-incompatible plant species and experimental investigations on self-incompatibility in natural populations.     

DOES MATE LIMITATION IN SELF‐INCOMPATIBLE SPECIES PROMOTE THE EVOLUTION OF SELFING? THE CASE OF LEAVENWORTHIA ALABAMICA

Genetic diversity at the S‐locus controlling self‐incompatibility (SI) is often high because of negative frequency‐dependent selection. In species with highly patchy spatial distributions, genetic drift can overwhelm balancing selection and cause stochastic loss of S‐alleles. Natural selection may favor the breakdown of SI in populations with few S‐alleles because low S‐allele diversity constrains the seed production of self‐incompatible plants. We estimated S‐allele diversity, effective population sizes, and migration rates in Leavenworthia alabamica, a self‐incompatible mustard species restricted to discrete habitat patches in rocky glades. Patterns of polymorphism were investigated at the S‐locus and 15 neutral microsatellites in three large and three small populations with 100‐fold variation in glade size. Populations on larger glades maintained more S‐alleles, but all populations were estimated to harbor at least 20 S‐alleles, and mate availabilities typically exceeded 0.80, which is consistent with little mate limitation in nature. Estimates of the effective size (N_e) in each population ranged from 600 to 1600, and estimated rates of migration (m) ranged from 3 × 10⁻⁴ to nearly 1 × 10⁻³. According to theoretical models, there is limited opportunity for genetic drift to reduce S‐allele diversity in populations with these attributes. Although pollinators or resources limit seed production in small glades, limited S‐allele diversity does not appear to be a factor promoting the incipient breakdown of SI in populations of this species that were studied.     

A one‐locus model of androdioecy with two homomorphic self‐incompatibility groups: expected vs. observed male frequencies

Androdioecy, the occurrence of males and hermaphrodites in a single population, is a rare breeding system because the conditions for maintenance of males are restrictive. In the androdioecious shrub Phillyrea angustifolia, high male frequencies are observed in some populations. The species has a sporophytic self‐incompatibility (SI) system with two self‐incompatibility groups, which ensures that two groups of hermaphrodites can each mate only with the other group, whereas males can fertilize hermaphrodites of both groups. Here, we analyse a population genetic model to investigate the dynamics of such an androdioecious species, assuming that self‐incompatibility and sex phenotypes are determined by a single locus. Our model confirms a previous prediction that a slight reproductive advantage of males relative to hermaphrodites allows the maintenance of males at high equilibrium frequencies. The model predicts different equilibria between hermaphrodites of the two SI groups and males, depending on the male advantage, the initial composition of the population and the population size, whose effect is studied through stochastic simulations. Although the model can generate high male frequencies, observed frequencies are considerably higher than the model predicts. We finally discuss how this model may help explain the large male frequency variation observed in other androdioecious species of Oleaceae: some species show only androdioecious populations, as P. angustifolia, whereas others show populations either completely hermaphrodite or androdioecious.     

Pollen tube growth in the self‐compatible sweet cherry genotype, ‘Cristobalina’, is slowed down after self‐pollination

Sweet cherry is a self‐incompatible fruit tree species in the Rosaceae. As other species in the family, sweet cherry exhibits S‐RNase‐based gametophytic self‐incompatibility. This mechanism is genetically determined by the S‐locus that encodes the pollen and pistil determinants, SFB and S‐RNase, respectively. Several self‐compatible sweet cherry genotypes have been described and most of them have mutations at the S‐locus leading to self‐compatibility. However, ‘Cristobalina’ sweet cherry is self‐compatible due to a mutation in a pollen function modifier that is not linked to the S‐locus. To investigate the physiology of self‐compatibility in this cultivar, S‐locus segregation in crosses involving ‘Cristobalina’ pollen, and pollen tube growth in self‐ and cross‐pollinations, were studied. In the crosses with genotypes sharing only one S‐haplotype, the non‐self S‐haplotype was inherited more frequently than the self S‐haplotype. Pollen tube growth studies revealed that the time to travel the whole length of the style was longer for self‐pollen tubes than for cross‐pollen tubes. Together, these results suggest that ‘Cristobalina’ pollen tube growth is slower after self‐pollination than after cross‐pollination. This reproductive strategy would allow self‐fertilisation in the absence of compatible pollen but would promote cross‐fertilisation if cross‐compatible pollen is available, a possible case of cryptic self‐incompatibility. This bet‐hedging strategy might be advantageous for an ecotype that is native to the mountains of the Spanish Mediterranean coast, in the geographical limits of the distribution of this species. ‘Cristobalina’ blooming takes place very early in the season when mating possibilities are scarce and, consequently, self‐compatibility may be the only possibility for this genotype to produce offspring.     

The loss of self‐incompatibility in a range expansion

It is commonly observed that plant species' range margins are enriched for increased selfing rates and, in otherwise self‐incompatible species, for self‐compatibility (SC). This has often been attributed to a response to selection under mate and/or pollinator limitation. However, range expansion can also cause reduced inbreeding depression, and this could facilitate the evolution of selfing in the absence of mate or pollinator limitation. Here, we explore this idea using spatially explicit individual‐based simulations of a range expansion, in which inbreeding depression, variation in self‐incompatibility (SI), and mate availability evolve. Under a wide range of conditions, the simulated range expansion brought about the evolution of selfing after the loss of SI in range‐marginal populations. Under conditions of high recombination between the self‐incompatibility locus (S‐locus) and viability loci, SC remained marginal in the expanded metapopulation and could not invade the range core, which remained self‐incompatible. In contrast, under low recombination and migration rates, SC was frequently able to displace SI in the range core by maintaining its association with a genomic background with purged genetic load. We conclude that the evolution of inbreeding depression during a range expansion promotes the evolution of SC at range margins, especially under high rates of recombination.?     

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.     

Paternal‐specific S‐allele transmission in sweet cherry (Prunus avium L.): the potential for sexual selection

Homomorphic self‐incompatibility is a well‐studied example of a physiological process that is thought to increase population diversity and reduce the expression of inbreeding depression. Whereas theoretical models predict the presence of a large number of S‐haplotypes with equal frequencies at equilibrium, unequal allele frequencies have been repeatedly reported and attributed to sampling effects, population structure, demographic perturbation, sheltered deleterious mutations or selection pressure on linked genes. However, it is unclear to what extent unequal segregations are the results of gametophytic or sexual selection. Although these two forces are difficult to disentangle, testing S‐alleles in the offspring of controlled crosses provides an opportunity to separate these two phenomena. In this work, segregation and transmission of S‐alleles have been characterized in progenies of mixed donors and fully compatible pollinations under field conditions in Prunus avium. Seed set patterns and pollen performance have also been characterized. The results reveal paternal‐specific distorted transmission of S‐alleles in most of the crosses. Interestingly, S‐allele segregation within any given paternal or maternal S‐locus was random. Observations on pollen germination, pollen tube growth rate, pollen tube cohort size, seed set dynamics and transmission patterns strongly suggest post‐pollination, prezygotic sexual selection, with male–male competition as the most likely mechanism. According to these results, post‐pollination sexual selection takes precedence over frequency‐dependent selection in explaining unequal S‐haplotype frequencies.     

Fewer S‐alleles are maintained in plant populations with sporophytic as opposed to gametophytic self‐incompatibility

Plants use self‐incompatibility to reject pollen bearing alleles in common at the S‐locus. These systems are classified as gametophytic (GSI) if recognition involves haploid pollen or sporophytic (SSI) if recognition involves diploid paternal genotypes. Dominance in SSI systems reduces the number of S‐alleles, but it has not been clear which system should maintain greater diversity when all else is equal. We simulated finite populations to compare the equilibrium number of S‐alleles in populations with either GSI or a co‐dominant SSI system. When population size was constant, SSI systems maintained more S‐alleles than GSI systems. When populations fluctuated in response to an S‐Allee effect, fewer S‐alleles were observed in SSI systems when S‐allele diversity was low, and SSI populations were vulnerable to extinction over a broader range of parameters. Turnover rates at the S‐locus were also faster in SSI populations experiencing strong S‐Allee effects. Given the variable expectations concerning S‐allele diversity in these systems, we reviewed published estimates of S‐allele diversity. GSI populations have significantly more S‐alleles on average than SSI populations (GSI = 25.70 and SSI = 16.80). Dominance likely contributes to this pattern, although the demographic consequences of the S‐Allee effect may be important in populations with fewer than 10 S‐alleles.     

Paternity tests support a diallelic self‐incompatibility system in a wild olive (Olea europaea subsp. laperrinei,Oleaceae)

Self‐incompatibility (SI) is the main mechanism that favors outcrossing in plants. By limiting compatible matings, SI interferes in fruit production and breeding of new cultivars. In the Oleeae tribe (Oleaceae), an unusual diallelic SI system (DSI) has been proposed for three distantly related species including the olive (Olea europaea), but empirical evidence has remained controversial for this latter. The olive domestication is a complex process with multiple origins. As a consequence, the mixing of S‐alleles from two distinct taxa, the possible artificial selection of self‐compatible mutants and the large phenological variation of blooming may constitute obstacles for deciphering SI in olive. Here, we investigate cross‐genotype compatibilities in the Saharan wild olive (O. e. subsp. laperrinei). As this taxon was geographically isolated for thousands of years, SI should not be affected by human selection. A population of 37 mature individuals maintained in a collection was investigated. Several embryos per mother were genotyped with microsatellites in order to identify compatible fathers that contributed to fertilization. While the pollination was limited by distance inside the collection, our results strongly support the DSI hypothesis, and all individuals were assigned to two incompatibility groups (G1 and G2). No self‐fertilization was observed in our conditions. In contrast, crosses between full or half siblings were frequent (ca. 45%), which is likely due to a nonrandom assortment of related trees in the collection. Finally, implications of our results for orchard management and the conservation of olive genetic resources are discussed.     

Neighbouring‐group composition and within‐group relatedness drive extra‐group paternity rate in the European badger (Meles meles)

Extra‐group paternity (EGP) occurs commonly among group‐living mammals and plays an important role in mating systems and the dynamics of sexual selection; however, socio‐ecological and genetic correlates of EGP have been underexplored. We use 23 years of demographic and genetic data from a high‐density European badger (Meles meles) population, to investigate the relationship between the rate of EGP in litters and mate availability, mate incompatibility and mate quality (heterozygosity). Relatedness between within‐group assigned mothers and candidate fathers had a negative quadratic effect on EGP, whereas the number of neighbouring‐group candidate fathers had a linear positive effect. We detected no effect of mean or maximum heterozygosity of within‐group candidate fathers on EGP. Consequently, EGP was associated primarily with mate availability, subject to within‐group genetic effects, potentially to mitigate mate incompatibility and inbreeding. In badgers, cryptic female choice, facilitated by superfecundation, superfoetation and delayed implantation, prevents males from monopolizing within‐group females. This resonates with a meta‐analysis in group‐living mammals, which proposed that higher rates of EGP occur when within‐group males cannot monopolize within‐group females. In contrast to the positive meta‐analytic association, however, we found that EGP associated negatively with the number of within‐group assigned mothers and the number of within‐group candidate fathers; potentially a strategy to counter within‐group males committing infanticide. The relationship between the rate of EGP and socio‐ecological or genetic factors can therefore be intricate, and the potential for cryptic female choice must be accounted for in comparative studies.     

Rapid loss of self‐incompatibility in experimental populations of the perennial outcrossing plant Linaria cavanillesii

Transitions from self‐incompatibility to self‐compatibility in angiosperms may be frequently driven by selection for reproductive assurance when mates or pollinators are rare, and are often succeeded by loss of inbreeding depression by purging. Here, we use experimental evolution to investigate the spread of self‐compatibility from one such population of the perennial plant Linaria cavanillesii into self‐incompatible (SI) populations that still have high inbreeding depression. We introduced self‐compatible (SC) individuals at different frequencies into replicate experimental populations of L. cavanillesii that varied in access to pollinators. Our experiment revealed a rapid shift to self‐compatibility in all replicates, driven by both greater seed set and greater outcross siring success of SC individuals. We discuss our results in the light of computer simulations that confirm the tendency of self‐compatibility to spread into SI populations under the observed conditions. Our study illustrates the ease with which self‐compatibility can spread among populations, a requisite for species‐wide transitions from self‐incompatibility to self‐compatibility.     

Recent hybrid origin and invasion of the British Isles by a self-incompatible species, Oxford ragwort (Senecio squalidus L., Asteraceae)

Senecio squalidus is a diploid hybrid species which originated in the British Isles following the introduction of material collected from a hybrid zone on Mount Etna, Sicily, approximately 300 years ago. Introduced hybrid material was cultivated in the Oxford Botanic Garden and gave rise to the stabilized diploid hybrid species, which later spread throughout much of the UK and into some parts of Ireland. Unusually for an invasive species, S. squalidus has a strong system of sporophytic self-incompatibility (SSI) that may have become modified as a result of its recent hybrid origin and spread. First, S. squalidus contains relatively few S alleles (between 2 and 6 S alleles within individual UK populations) compared to other species with SSI (estimates average ~17 S alleles per population). This most probably reflects the population bottleneck experienced by introduced hybrid material. Second, dominance relationships among S. squalidus S alleles are more extensive than those reported in other species with SSI. Third, although pseudo-self-compatibility occurs sporadically in S. squalidus, it is not widespread, indicating that SSI is maintained in the species despite potential mate availability restrictions imposed by low numbers of S alleles. Surveys of other forms of genetic diversity in S. squalidus show that allozyme variation is reduced relative to that within the progenitor species, but Randomly Amplified Polymorphic DNA variation is relatively high. Both types of genetic variation show little or no pattern of isolation-by-distance between populations in keeping with the recent range expansion of the species. During its spread in the British Isles, S. squalidus has hybridized with the native self-compatible (SC) tetraploid species, S. vulgaris, which has led to the origin of three new SC hybrid taxa: a radiate form of S. vulgaris (var. hibernicus), a tetrapoid hybrid species (S. eboracensis) and an allohexaploid (S. cambrensis).     

INTERSPECIFIC INCOMPATIBILITY IN SOLANUM SPECIES

Pandey , K.K. (Crop Res. Div., D.S. & I.R., Lincoln, Christchurch, New Zealand.) Interspecific incompatibility in Solanum species. Amer. Jour. Bot. 49(8): 874–882. Illus. 1962.—A diallel cross involving 11 self-incompatible and 3 self-compatible species of Solanum was made to study the genetic basis of interspecific incompatibility. Interspecific incompatibility was not limited to crosses in which a self-compatible species was used as the male parent onto a self-incompatible species (unilateral incompatibility). A number of crosses between self-incompatible species were incompatible. In one cross, Q vernei X verrucosum, a self-compatible species was successful as a pollen parent with a self-incompatible species. Unlike other hybrids between self-compatible and self-incompatible species, which are self-incompatible, these F₁ hybrids were self-fertile, and cross-fertile among themselves and with both parents. The self-fertile S. polyadenium was cross-incompatible as a female as well as a male parent with all other species. It is suggested that the unilateral incompatibility is a property of the allele S_C which originated as a consequence of one kind of breakdown of the S_I gene; the S_C allele produces “bare” pollen growth substances which are inactivated in an incompatible style. It is proposed that the failure of the principle of unilateral interspecific incompatibility in solanaceous species may be due to the action of alleles at the second incompatibility locus revealed in certain Mexican species. It is assumed that the South American species are selected intraspecifically only for the action of S alleles but that in certain interspecific crosses and rarely in intraspecific crosses the alleles at the second locus may be expressed, thus interfering with the usual action of S alleles. The F₁ hybrids Q verrucosum (self-fertile) X simplicifolium (self-sterile) were self-incompatible at the tetraploid as well as the diploid level, and their cross-compatibility behavior was consistent with the expected activity of the S_C and S_I alleles of the 2 parents respectively.     

Evolutionary dynamics of mating system shifts in Arabidopsis lyrata

Outcrossing is the prevalent mode of reproduction in plants and animals despite its substantial costs, while selfing and mixed mating occur at much lower frequency. Comparative research on plants has demonstrated the lability of self‐incompatibility, but there is little information about the transition on a within‐species level from self‐incompatibility to predominant selfing. We studied variation in mating system among 18 populations of Arabidopsis lyrata within a phylogenetic context to shed light on the evolution of selfing. Realized and potential mating systems were assessed by genetic analysis with microsatellite markers and hand‐self‐pollinations on 30 plants from each population. The fraction of self‐incompatible plants in a population was highly correlated with the outcrossing rate, showing that the spread of self‐compatibility is accompanied by or soon followed by an increase in the rate of selfing. The four predominantly selfing populations (outcrossing rates < 0.25) fell into more than one phylogenetic cluster, suggesting that the transition to selfing occurred more than once independently. Hence, A. lyrata offers an opportunity for the comparative analysis of outcrossing as a predominant mode of reproduction in plants and of the causes of the shift to selfing.     

Genetic studies of self incompatibility in the garden chrysanthemum,Chrysanthemum morifolium ramat

Summary Self incompatibility was investigated in the hexaploid garden chrysanthemum, a member of Compositae. Nine sibling clones selected from a highly compatible cross were all self incompatible. 14.8% of the crosses between these sibs in diallel were compatible, but one sib, 67-111-42, accounted for 10 of the 12 compatible crosses. 67-111-42 was also more compatible than the remaining 8 sibs in crosses to other closely related plants. Crosses of the 9 sibs to 12 unrelated tester clones indicated that none were male or female sterile. Inbreeding via pseudocompatibility was successful in increasing homozygosity at the S loci. The percentage of compatible crosses obtained in 3 sib diallels of I ₂ clones from crosses of 67-111-42I ₁ plants approached that of the original 9 × 9 diallel, but no one individual accounted for most of the compatible crosses. It was possible to separate the 9 sibs into 9 incompatibility patterns from the pollinations made in this study. The evidence suggests that the self-incompatibility reaction in the garden chrysanthemum is sporophytic and involves more than 1 locus.Scientific Journal Series Paper Number 7882 of the Minnesota Agricultural Experiment Station.Lyndon W. Drewlow was a National Science Foundation Trainee.     

Integrating population demography, genetics and self-incompatibility in a viability assessment of the Wee Jasper Grevillea (Grevillea iaspicula McGill., Proteaceae)

Grevillea iaspicula is an endangered shrub known from only eight small populations (<250 individuals) in south-eastern Australia. The species is threatened by combined ecological and genetic factors, e.g. land conversion, weed invasion, low recruitment and low gene flow among populations. The populations also show large variance in male fitness and limited mate availability which are thought to arise as a consequence of gametophytic self-incompatibility (GSI). This study has used an individual-based, spatially explicit simulation model to explore the interaction between GSI and mate limitation in this species, as well as its effect on long-term population viability. The model was parameterised with demographic and genetic data obtained from 2 years of population monitoring. Simulation results identified extremely low establishment rates as the most critical factor currently influencing the persistence of G. iaspicula populations and indicated that the extant populations are at serious risk of extinction in the near future unless this is altered by, at very least, an order of magnitude higher. SI was shown to affect the magnitude of variation in establishment but this effect was masked when establishment was critically low. Disassortative mating, owing to low allelic richness at the S-locus, had the negative demographic effect of restricting mating to relatively few compatible plants. Restricted mate availability imposed additional limitations to the viability of populations but, given a 20-fold increase in establishment rate, population fluctuations stabilised. The long-term viability of G. iaspicula is bleak without artificial augmentation of the populations but management planning must also consider genetic processes, including SI, to ensure such strategies optimise the benefits gained.     

Genetic analysis of incompatibility in the diploid Ipomoea species closely related to the sweet potato

Summary In order to identify the genotypic constitutions of incompatibility in the diploid species, Ipomoea leucantha Jacq. (K221), which is most closely related to the sweet potato, the progenies derived from the reciprocal crosses, backcrosses and testcrosses were analysed. All the plants examined were self-incompatible, and pollen germination was inhibited on the stigma after incompatible pollinations. No reciprocal differences were found in the incompatibility reactions. In the progenies three incompatibility groups were observed which showed the rather simple segregation ratios. The homozygous plants for incompatibility alleles were obtained in the progenies. The experimental results demonstrated a sporophytic type of incompatibility controlled by a single locus with multiple S-alleles exhibiting a dominance relationship in both the pollen and the stigma. The plants obtained in the progenies had the following genotypes: S ₁ S ₂, S ₁ S ₃, S ₂ S ₂, S ₂ S ₃ and S ₃ S ₃.     

Non-additive effects of pollen limitation and self-incompatibility reduce plant reproductive success and population viability

Background and Aims

Mating system is a primary determinant of the ecological and evolutionary dynamics of wild plant populations. Pollen limitation and loss of self-incompatibility genotypes can both act independently to reduce seed set and these effects are commonly observed in fragmented landscapes. This study used a simulation modelling approach to assess the interacting effects of these two processes on plant reproductive performance and population viability for a range of pollination likelihood, self-incompatibility systems and S-allele richness conditions.

Methods

A spatially explicit, individual-based, genetic and demographic simulation model parameterized to represent a generic self-incompatible, short-lived perennial herb was used to conduct simulation experiments in which pollination probability, self-incompatibility type (gametophytic and sporophytic) and S-allele richness were systematically varied in combination to assess their independent and interacting effects on the demographic response variables of mate availability, seed set, population size and population persistence.

Key Results

Joint effects of reduced pollination probability and low S-allele richness were greater than independent effects for all demographic response variables except population persistence under high pollinator service (>50 %). At intermediate values of 15–25 % pollination probability, non-linear interactions with S-allele richness generated significant reductions in population performance beyond those expected by the simple additive effect of each independently. This was due to the impacts of reduced effective population size on the ability of populations to retain S alleles and maintain mate availability. Across a limited set of pollination and S-allele conditions (P = 0·15 and S = 20) populations with gametophytic SI showed reduced S-allele erosion relative to those with sporophytic SI, but this had limited effects on individual fecundity and translated into only modest increases in population persistence.

Conclusions

Interactions between pollen limitation and loss of S alleles have the potential to significantly reduce the viability of populations of a few hundred plants. Population decline may occur more rapidly than expected when pollination probabilities drop below 25 % and S alleles are fewer than 20 due to non-additive interactions. These are likely to be common conditions experienced by plants in small populations in fragmented landscapes and are also those under which differences in response between gameptophytic and sporophtyic systems are observed.